The Pennsylvania State University The Graduate School Department of Neuroscience
THE NEURAL SUBSTRATES OF HUMAN SOCIALITY IN CHILDREN AND ADOLESCENTS: AN FMRI INVESTIGATION
A Dissertation in Neuroscience
by Melissa Long
! 2009 Melissa Long
Submitted in Partial Fulfillment
of the Requirements
for the Degree of
Doctor of Philosophy
August 2009 ii The dissertation of Melissa Long was reviewed and approved* by the following:
Paul Eslinger Professor of Neurology Dissertation Advisor Chair of Committee
Patricia Grigson Associate Professor of Neural and Behavioral Science
Jianli Wang Assistant Professor of Radiology Special Member
Robert Milner Professor of Neural and Behavioral Science Head of the Neuroscience Graduate Program
Charles Lang Professor of Cellular and Molecular Physiology
*Signatures are on file in the Graduate School
iii ABSTRACT
Sociality is indissociable from human life and experience. Humans are constantly engaged in social interaction, whether it be in actuality or imagined, and are particularly sensitive to social stimuli. This high degree of social interaction and sensitivity is a byproduct of human biology and culture and contributes to healthy growth, maturation, and the majority of the joy experienced throughout one’s life.
Unfortunately, it also accounts for much of an individual’s pain and suffering. Due to the importance and pervasiveness of sociality to human life, it is certainly worthy of research. Although behavioral studies comprise the majority of the studies on sociality to date, only recently has research been devoted to the underlying neural substrates supporting social phenomena. Even more scarce are studies investigating these substrates in children and adolescents. In the current research, substrates underlying sociality were investigated in children and adolescents using functional magnetic resonance imaging
(fMRI). In particular, three components of sociality were investigated: Agency, Moral
Judgments, and Social Emotions. Agency involves the way we come to understand ourselves as causes of actions and consequences and is the precursor to more complex human social constructs. A !"#$%&'()*!+,-&./&)+0.,+)&$/&-1+&2$3$2.-4&-"&!$5+&
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iv behavioral, imaging, electrophysiology, and lesion studies, these components and their underlying neural circuitry play vital roles in social information processing and behavior and when abnormal, result in severe social deficits. Written vignettes endowed with social moral and/or social moral emotional content were utilized in the current research to investigate these typically developing neural networks in children and adolescents. In the
Agency and Moral Judgment task, the participants were required to respond to these vignettes as to whether the social interaction was morally “right” or “wrong.” Participants were required to only passively read the vignettes in the Social Emotion task. A shared network was identified between the Agency, Moral Judgment, and Social Emotions conditions including medial prefrontal cortex (PFC), medial parietal, and lateral temporal regions. Although similarities were marked, clearly identifiable differences were noted between social constructs. Select frontal and limbic/subcortical neural activations were observed to be influenced by age. Meanwhile, the shared network between constructs remained steadily recruited across the developmental sample. In conclusion, the results revealed the complex interplay of cognitive and affective processing, both statically and developmentally, subserving the core components of social moral behavior. These findings will be most helpful in the early detection, intervention, and prevention of social disorders, such as autism, adolescent-onset schizophrenia, sociopathy, and others.
v TABLE OF CONTENTS
LIST OF FIGURES ...... ix
LIST OF TABLES...... xviii
ACKNOWLEDGEMENTS...... xx
Chapter 1 Introduction ...... 1
Social Features Unique to Human Primates……………………………….…1
Sociality and Human Health……………………………………………….…7
What is Morality?……………………………………………………………10
What is State of Morality Considering it’s Purpose?...... 11
Antisocial Personality Disorder, Sociopaths, and Psychopaths……...12
Autism, Williams Syndrome, Schizophrenia, and ADHD…………...14
Lesions to the ‘Social Brain’…………………………………………20
Frontal Temporal Dementia………………………………………….27
Notes on Discussed Dysfunctions……………………………………………28
Investigating Morality………………………………………………………..30
Behavioral Development…………………………………………………….32
Why Children and Adolescent Focus?……………………………………….37
Factors Influencing Development……………………………………………44
Social Constructs and Neural Correlates of Interest…………………………46
vi Chapter 2 Agency ...... 51
Introduction…………………………………………………………………..51
Methods………………………………………………………………………56
Results………………………………………………………………………...62
Discussion…………………………………………………………………….72
Moral Self-Agency and Moral Other-Agency………………………..73
Moral Agency Development………………………………………….80
Summary and Conclusion………………………………………….….81
Chapter 3 Moral Judgment ...... 82
Introduction……………………………………………………………………82
Methods……………………………………………………………………..…87
Results…………………………………………………………………………93
Discussion…………………………………………………………………….107
Polar PFC in Social Moral Processing……………………………..…107
OFC in Social Moral Processing………………………………...……109
Developmental Findings………………………………………………112
Social Moral Sub-Domain Differences…………………………..……115
Theory of Mind…………………………………………………..……117
Left Lateralizations and Social Moral Implications…………..…….…118
Summary and Conclusion…………………………………………...…120
vii
Chapter 4 Social Emotions……………………………………………………..…...…123
Introduction……………………………………………………….…………….123
Methods…………………………………………………………………………131
Results…………………………………………………………………..………137
Discussion………………………………………………………………………149
Lateralization of Social Emotions………………………………………151
Posterior Brain Activations……………………………..………………153
Limbic Sensitivity with Age……………………………………………156
Prosocial Emotions………………………………………..……………157
Antisocial Emotions……………………………………….……………161
Developmental Findings………………………………………..………162
Summary and Conclusion………………………………………………164
Chapter 5 Final Discussion ...... 166
Cross-Sectional Post-Hoc Analyses…………………………….………………166
Cross-Sectional Results Summarized………………………………..…………172
Anterior Activations………………………………………………..…...………177
Posterior Activations……………………………………………………………180
Developmental Implications……………………………………………………183
viii Highlights………………………………………………………….…………186
Theory of Mind………………………………………………………187
Language……………………………………………………..………192
Models Supporting Summarized Findings……………………………...……195
Limitations in the Presented Studies…………………………………………198
Importance of the Presented Research…………………………………….…200
Future Questions and Directions………………………………………..……201
Appendix………………………………………………………………….…………205
References...... 210
CurriculumVitae……………………………………………………………….…….256
ix LIST OF FIGURES
Figure 1-1: From: Opinion:The neural basis of human moral cognition. Moll et al., 2005...... 47
Figure 1-2: From: The neurobiology of social cognition. Adolphs et al., ..……………47
Figure 1-3: Dodge’s sequential step model of social decision-making represented in an organizational chart with the social and emotional moral behaviors to be studied in the current research…………………………………………………………………………49
Figure 2-1: The presented schematic is only to aid in understanding the block design used for the current experiment. All blocks are not presented here. The experimental blocks (Moral Self-Agency and Moral Other-Agency) are interleaved with Baseline/Non-
Moral blocks. Rest periods are evenly dispersed throughout the paradigm………………………………………………………………………..………60
Figure 2-2: When averaging across the Moral Right and Moral Wrong statements that included the role of self-agency and subtracting out the baseline (Non-moral judgments) in a one-sample t-test (p<0.005, v>10), the following regions of activation were observed: medial frontal polar cortex, anterior cingulate cortex, superior temporal sulcus,
x bilateral temporal parietal junction, Right anterior temporal pole, and medial precuneus/posterior cingulate. The activation cluster in the medial precuneus/posterior cingulate region was particularly prominent, closely followed by the mPFC, areas involved in self-referential thinking and episodic memory retrieval. The activated regions are commonly reported in adult studies investigating agency and mentalizing/ToM. A. Activations overlayed on a 3D-rendered template image. B.
Activations overlayed on axial slices…………………………………………………………………………………….64
Figure 2-3: The average activation map (one-sample t-test (p<0.005, v>10)), for the
Other-Agency condition statements in comparison to baseline revealed activation in the superior medial polar frontal cortex, bilateral anterior temporal poles, medial precuneus, and L temporal parietal junction. Similar to the Moral Self-Agency condition, there were prominent activation clusters in the medial precuneus and the medial prefrontal cortex.
As in the Moral Self-Agency task, these areas of activation have been demonstrated by adult studies to be recruited for agency and related constructs, such as mentalizing/ToM.
A. Activations overlayed on a 3D-rendered template image. B. Activations overlayed on axial slices……………………………………………………………………………….66
Figure 2-4: The average activation map of the Self-Agency (red) (p<0.005, v>10) and
Other-Agency (green) (p<0.005, v>10) are overlayed on a 3D-rendered template image.
Similar areas of activation between Self and Other Agency are represented in yellow.
xi Shared activations include the L temporal parietal junction (TPJ), medial precuneus, and medial prefrontal cortex (mPFC). The R TPJ activation is specific to the Moral Self-
Agency condition. The mPFC and medial precuneus activations are larger in the Moral
Self-Agency condition and include the anterior cingulated and posterior cingulated, respectively. The L temporal pole is activated in the Moral Other-Agency condition and not in the Moral Self-Agency condition. These activations suggest that although underlying neural networks are similar for self and other processing, distinctions exist……………………………………………………………………………………...67
Figure 2-5: Activations associated with Moral Self-Agency and Moral Other-Agency were more specifically contrasted in a paired t-test (p<0.01, v >10). In this analysis, the self-agency condition was found to recruit significantly greater activity in the R dorsal lateral prefrontal cortex. The contrast of Moral Other-Agency to Moral Self-Agency
(p<0.01, v >10) revealed small activations in the L cerebellum, and parietal-occipital junction………………………………………………………………………………….69
Figure 3-1: The presented schematic is only to aid in understanding the block design used for the current experiment. All blocks are not presented here. The experimental blocks
(Rule-Based and Ambiguous) are interleaved with Baseline/Non-Moral blocks. Rest periods are evenly dispersed throughout the paradigm………………………………………………………………………………..91
xii Figure 3-2: When averaging across the moral activation tasks (Rule-Based, and
Ambiguous) and subtracting out the baseline/nonmoral statements in a one-sample t-test
(FWE p<0.05, v>10), a medial frontal and parietal network with additional left- lateralized anterior temporal, lateral temporal, and inferior parietal activations, was recruited. The following regions of activation were observed: L anterior temporal pole, lateral orbital frontal cortex, precuneus/posterior cingulate, L superior temporal sulcus, L temporo-parietal junction, medial prefrontal cortex, and superior medial prefrontal cortex.
A. Activation overlayed on a 3-D rendered template image. B. Activations overlayed on axial slices……………………………………………………………………………..95
Figure 3-3: When comparing Rule-Based activation to baseline/nonmoral statement activation in a one-sample t-test (p<0.001, v>10), activations are observed in the precuneus/posterior cingulate, L superior temporal sulcus (STS), bilateral temporal- parietal junction (TPJ), superior medial prefrontal cortex (mPFC), anterior cingulate cortex, L superior PFC, and R middle temporal. Medial regions in the PFC and precuneus/posterior cingulate regions, as well as the L STS/TPJ were prominent clusters in this condition. Activations are overlayed on a 3D-rendered template image……...96
Figure 3-4: A one-sample t-test (FWE p<0.05, v>10) comparing the Ambiguous condition to the baseline/nonmoral statements resulted in activation patterns similar to the
Rule-Based condition but with more robust and additional activation in the ventral lateral and superior prefrontal cortex (PFC), and temporal pole regions. Ambiguous activations
xiii included the superior medial PFC, medial PFC, anterior cingulate cortex, supplementary motor cortex, L superior temporal sulcus, L temporal-parietal junction, medial precuneus/posterior cingulate, L anterior temporal pole, and L LOFC. Activations are overlayed on a 3D-rendered template image…………………………………………..98
Figure 3-5: At a shared p<0.001, v>10, average activation maps of the Ambiguous
(green), Rule-based (red) and Nonmoral (blue) conditions are overlayed on a 3D- rendered template image…………………………………………………………….....99
Figure 3-6: After conducting an age regression analysis (p<0.01, v>10) between age and the Moral Judgment condition activations, activation increased with age in the mid cingulate cortex, and the frontal polar, cerebellum, angular gyrus, dorsal lateral prefrontal cortex, and supplementary motor cortices in the left hemisphere. The most prominent cluster observed was in the L frontal polar cortex. B. Linear Regression displaying the signal change percentage in the L frontal polar cortex (MNI -28, 56, 20) as children and adolescents age (p<0.01)……………………………………………………………...101
Figure 3-7: After conducting an age regression analysis (p<0.001, v>10) between age and the Ambiguous condition activations, activation increased with age in the L angular guys, anterior cingulate cortex, R caudate, posterior insula/posterior temporal gyrus/sylvian fissure, superior medial frontal, R cerebellum, and supplementary motor
xiv cortex. The most prominent cluster was in the L angular gyrus, followed by the anterior cingulate...... …………………... ……102
Figure 3-8: Linear regression of the signal change percentage in the R amygdala (MNI
24, 4, -30) as children age
(p<0.01)………………………………………………………………………………...103
Figure 4-1: The presented schematic is only to aid in understanding the block design used for the current experiment. All blocks are not presented here. The experimental blocks (Gratitude, Pity, Guilt, Anger, Fear, Disgust) are interleaved with Baseline/Non-
Moral blocks. Rest periods are evenly dispersed throughout the paradigm……………135
Figure 4-2: Averaging across all emotions investigated in the present study (guilt, pity, gratitude, fear, anger, and disgust) compared to the baseline condition of neutral statements in a one-sample t-test (p<0.005, v>10) yielded activations in the L superior temporal sulcus, bilateral temporal parietal junction, frontal polar, bilateral middle temporal, bilateral anterior temporal poles, R lingual, medial precuneus, L fusiform, L dorsal lateral prefrontal cortex. The most prominent clusters were observed in the L superior temporal sulcus/temporal parietal junction and the frontal polar cortex, followed by the R TPJ and the bilateral anterior temporal poles. A. Activation overlayed on a 3-D rendered template image. B. Activations overlayed on axial slices…………….……..139
xv Figure 4-3: After conducting a one-sample t-test (p<0.005, v>10) on the prosocial emotions (green) (guilt, pity, and gratitude) contrasted to baseline, activation was observed in the bilateral superior temporal sulcus/temporal parietal junction, L ventral lateral prefrontal cortex, R anterior temporal pole, mPFC, and medial precuneus. The most prominent clusters in this condition were the bilateral superior temporal sulcus/temporal parietal junction (STS/TPJ) region, followed by the L ventral lateral prefrontal cortex (VLPFC). After conducting a one-sample t-test (p<0.005, v>10) on the antisocial emotions (red) (fear, anger, disgust) contrasted to baseline, activation was observed in the L inferior occipital, L STS/TPJ, dorsal LPFC, VLPFC, dorsal medial
PFC, and R lingual gyrus, with the most prominent cluster in the L inferior occipital cortex, followed by the L STS/TPJ. Activations are overlayed on a 3D-rendered template image. Common areas of activation between the Prosocial and Antisocial conditions are represented in yellow…………………………………………………………………...141
Figure 4-4: After conducting a paired t-test (p<0.01, v>10), contrasting Prosocial and
Antisocial conditions, activation in premotor, motor associative, and motor and emotional regulative areas was observed. These activations were as follows: R precuneus, putamen/lenticular nucleus, pre and postcentral gyri, and the paracentral lobule.
Activations are overlayed on axial slices………………………………………..……..143
Figure 4-5: A. A linear regression analysis was conducted between contrast (indicative of signal change between baseline and the experimental task) in the R amygdala (MNI
xvi 24, -4, -15) and age for each subject. Data point colors correspond to gender of participants (Female=Pink, Male=Blue). B. A positive age regression analysis (p<0.01) yielded activations in the R amygdala. Activation is overlayed on a template image displayed in three planes…………………………………………………....……..……144
Figure 4-6: A. A linear regression analysis was conducted between contrast (indicative of signal change between baseline and the experimental task) in the L hippocampus/parahippocampus region (MNI -28, -34, -7) and emotional intelligence
(EQ) for each subject. Data point colors correspond to gender of participants
(Female=Pink, Male=Blue). B. A positive regression analysis (p<0.01) yielded activations in the L hippocampus/parahippocampus region (MNI -28, -34, -7). Activation is overlayed on a template image displayed in three planes…………...……...…….….146
Figure 5-1: After conducting a conjunction analysis between the three social moral construct conditions, we found the L superior temporal sulcus/temporal parietal junction, superior medial prefrontal cortex, middle and anterior temporal gyri, and medial precuneus to be activated (p < 0.001). Activations are overlayed on a 3D-rendered template image………………………………………………………………………….169
Figure 5-2: When contrasting the Moral Judgment and Social Emotion conditions in a paired t-test, Moral Judgment activations were observed in the precuneus, posterior cingulate, bilateral occipito-parietal junction, R angular, anterior cingulated cortex, L
xvii insula, L cerebellum, R and L superior and anterior temporal gyri (p<0.005, v>10). This activation pattern highlights the heightened activation needed for the integration of processing streams subserving explicit decision-making. Activations overlayed on a 3D- rendered template image………………………………………………………………170
Figure 5-3: The Social emotion condition contrasted to the Moral Judgment condition, recruited the L lateral dorsal/ventral prefrontal cortex, L temporo-parieto-occipital junction (p < 0.01). This contrast yielded much less robustness and activations than the opposite contrast, indicating reduced recruitment for social moral processing when passively viewing social moral stimuli. However, slight distinctions in key areas are observed in the displayed contrast. Activations are overlayed on a 3D-rendered template image……………………………………………………………………………………171
xviii LIST OF TABLES
Table 2-1: Examples of the Moral Self-Agency, Moral Other-Agency, and Baseline stimuli used for this study. The experimental tasks are listed on the...... 61
Table 2-2: Average activation map, paired t-tests, and Age Regression Analyses localizations for the Self-Agency and Other-Agency conditions are displayed. MNI coordinates, voxel sizes (k), t-values, and Brodmann areas (BA) are reported. P-values are for each condition are specified and listed to the right of the respective condition.
Temporal parietal junction (TPJ), superior temporal sulcus (STS), medial prefrontal cortex (mPFC), dorsal lateral prefrontal cortex (DLPFC), ventral tegmental area
(VTA)………………………………………………………………………….……….71
Table 3-1: Examples of the moral stimuli used for this study. The experimental tasks are listed on the left and one example of each corresponding stimulus is presented on the right………………………………………………………………………………...…..92
Table 3-2: Average activation maps, paired t-tests, and Age Regression Analyses localizations for the Moral Judgment, Ambiguous, and Rule-based conditions are displayed. MNI coordinates, voxel sizes (k), t-values, and Brodmann areas (BA) are reported. Prefrontal cortex (PFC), temporal parietal junction (TPJ), superior temporal
xix sulcus (STS), medial prefrontal cortex (mPFC), dorsal lateral prefrontal cortex (DLPFC), anterior temporal cortex (ACC)...... 105-106
Table 4-1: Below are example statements representing each of the six different Social
Emotion conditions as well as an example of a Neutral/Baseline statement……….136
Table 4- 2: Average activation maps, paired t-tests, and Age Regression Analyses localizations for the Social Emotions, Prosocial, and Antisocial conditions are displayed.
MNI coordinates, voxel sizes (k), t-values, and Brodmann areas (BA) are reported
…………………………………………………………………………………...... 147-149
xx ACKNOWLEDGEMENTS
Pennsylvania Department of Health- Pennsylvania State University Tobacco
Settlement Fund, Grant #4100020604
Children’s Miracle Network
Pennsylvania State University, Social Science Research Institute- Quantitative
Social Science Research Institute Fellowship 2007-2008
1
Chapter 1
Introduction
Social Features Unique to Human Primates
The number of individuals comprising the human social network exceeds the number of individuals in any other societal species (Dunbar 1992). In these group societies, Ralph Adolphs, an expert in social neuroscience, suggests that there are two opposing factors within these large societies: within-group competition and group cohesion and cooperation (Adolphs 2001). Within-group competition may be damaging to the group, whereas the cooperative, protective nature of a group is advantageous for the chances of survival and propagation of the species. Adolphs goes on to suggest that societal species deal with these competing factors in one of two ways: rigid, eusocial behavior, found in animals such as bees, wasps, and termites or complex, flexible behavior found in primates (Thorne 1997). The flexible behavior observed in primates allows more of a volitional approach to social interactions. Instead of automatic social behavior, primates, and with much more sophistication and profoundness, humans, have highly sophisticated and vastly more social abilities that allow for flexible, adaptive social behavior in response to a dynamic complex social system. A few examples of those capabilities are being able to perceive distinct “you” and “other” representations, depicting social meanings and intentions of behaviors, engaging in emotional and
2 behavioral regulation, and having an extensive highly complicated repertoire of social emotions bridging affective and cognitive domains. (Eisenberg 1995; Haidt 2003; Moll, de Oliveira-Souza et al. 2005; Saxe 2006). The underlying neural manifestations provide a platform for flexible social behavior as well as a guide to plan and execute such behaviors. (Adolphs 2001; Moll, de Oliveira-Souza et al. 2007).
While we are closely linked to other species in our social behavior in that our capabilities are not completely novel, it must be acknowledged that in both affective and cognitive domains, an exceedingly higher degree of sophistication is exhibited in humans.
Around the age of three or four, humans surpass other primates in that they are at the apex of all species in their cognitive skills and social sensitivities (Tomasello 1999; Moll, de
Oliveira-Souza et al. 2003). Beginning in early development, children as young as two months old show a preference for human faces to other non-human face objects (Fantz
1961). This affinity for faces is observed in an area of the brain shared with other primates and in the human cortex contains what is known as the ‘fusiform face area’ which is known to be crucial for computing and integrating the complex details of each face for the recognition, identification, and differentiation of faces (Haxby, Hoffman et al.
2000; Kanwisher 2000). Another neuronal phenomenon that is believed to contribute to human social capabilities are specialized neurons described as ‘large-spindle shaped’ neurons. They have been discovered in primates and have been found to be the most prominent in the anterior cingulate cortex of humans, in lesser number in chimpanzees and apes, and are absent in all other species. It has been speculated that the size of these neurons makes them capable of integrating neural information across spatially distant locations in the brain (Nimchinsky, Gilissen et al. 1999). Not surprisingly, humans,
3 require the integration of highly processed information from various subsystems to be exchanged, represented, and manipulated to produce complex social behaviors, which may require such cells. Another type of specialized cell found in the brain of primates via means of single-unit recordings and neuroimaging, are known as ‘mirror-neurons’; these neurons fire when an action is executed by self or another person (Gallese, Fadiga et al.
1996; Rizzolatti, Fadiga et al. 1996; Grezes, Armony et al. 2003) and enable one to simulate an action of another being. A dedicated neural network that includes these
‘mirror neurons’ has been identified and includes similar structures in monkeys and humans, such as the ventral premotor cortex, superior temporal sulcus (STS), and the inferior parietal lobule. Although similarities exist, the human ‘mirror neuron system’ is thought to be more extensive and include affective regions, such as the anterior cingulate gyrus, frontal operculum, and insula (Wicker, Keysers et al. 2003; Morrison, Lloyd et al.
2004). In humans, it is thought that the mirror neuron system is responsible for the imitation that infants utilize in to rapidly learn from their caretakers (Rizzolatti, Fadiga et al. 1999). Additionally, the sophistication of this system in humans is thought to account for the degree of simulation humans engage in, in both social and emotional interpersonal contexts. Researchers conducted further studies indicating that selective mirror neurons responded before the action was even executed, which suggested these cells additionally played a role in inferring the intention of another being. It is probable that this system is a fundamental building block for higher-order social constructs, such as Theory of Mind
(ToM) (Arbib 2005), or the ability to attribute mental states to other people in order to predict their behavior (Frith and Frith 2003), which is one of the most distinguishing features separating humans from other primates (in level of sophistication) (Call and
4
Tomasello 1999). This ability is pivotal for social causality, learning, and predictive behavior. Moreover, empathy, of which ToM is a key ingredient, has been shown to be directly proportional to the degree of activation of mirror neurons (Gazzola, Aziz-Zadeh et al. 2006). Additionally, research has demonstrated dysfunction in this system in multiple social disorders and that the degree of dysfunction be indicative to the severity of the disorder (Iacoboni and Dapretto 2006). From this mirror system, which is crucial to social learning and contributes largely to the basis for human culture, we learn to know and predict what others will think, feel, or do in response to our action or some other event
(Rizzolatti, Fadiga et al. 1999). These examples of neurons and brain regions, present in select primates, and more specifically in humans, seem to be specialized for the complex social behaviors observed in humans and leave little question that each human being is innately wired to be one part of the collective whole of human society.
Another feature possessed by humans and also shared with other mammals is the brainstem/limbic axis or what cognitive neuroscientists, Casebeer & Churchland (2003), term the “regulatory core.” This core is shared by mammals, is an automatic subcortical system that controls regulatory functions such as breathing, blood pressure, arousal, body temperature, wake/sleep cycles, and basic emotion and motivational states. These states are relatively “closed” interoceptive states that when brought to the perception level, guide survival behaviors such as foraging for food. Of course, humans, being mammals, have this “regulatory core” but it is mushroomed by a cortex that enables a much higher degree of “open circuits” that are vulnerable to contextual/environmental stimuli and thus demand flexible adaptable behaviors. This “openness” introduces the vast amount of
5 learning that humans undertake during the course of life, such as language, physical and mental causality, and social learning.
Perhaps the most important development contributing to these “open” circuits and the associated flexible behavior is the extension of the frontal lobes, or the prefrontal cortex (PFC) region, and the regulatory cores’ innervation of this frontal region. The PFC is not a homogenous tissue but is differentiated based on cytoarchitecture and function
(Davidson 2004). Selective neurons specific to the PFC have been shown to fire over extended periods of time and across events (Bodner, Kroger et al. 1996; Levy and
Goldman-Rakic 2000), suggesting that the information they represent can be held over time for long-term goal planning (Fuster 1997), a characteristic unique to humans.
Pyramidal cells in the PFC, compared to these cells found in other non-PFC brain regions, were found to be more spinous, which was postulated to be due to the extensive excitatory inputs to this region and the integration of multiple inputs (Elston 2000). Gathered from these data, the various sectors of the PFC and the innervations to it allow for the complex integration of preferences, drives, and choices which guide decision-making and behavior
(Koechlin 2007). With this plethora of information, the PFC coordinates stimulus- independent thought with stimulus-oriented thought, or interceptive and exteroceptive cues, which enables predictive behavior and complex motor planning directed at guiding social behavior in a dynamic social environment (Casebeer 2003; Burgess 2007).
Although humans share basic emotional cognitive constructs with other mammals and primates, it is the PFC, and more specifically the integration and representation of these constructs in this region, that is needed for the profound social cognitive and emotional processing observed in humans. The high degree of integration of not only non-PFC
6 regions to the PFC, but PFC sectors to each other allows for the complex knowledge representations, abstract thinking, such as long-term goal planning, and the dissociable social cognitive and emotional constructs observed in human beings (Wood and Grafman
2003). Through this elaborate network of connections, the PFC has the ability to bind information temporally and retrieve, represent, and manipulate these knowledge units according to changing contexts (Grafman 1995). This ability is essential for social contexts because of the demand for the integration of featural, emotional, and event knowledge, and personal values and future goals (Moll, de Oliveira-Souza et al. 2005).
Generally speaking, the PFC region, which is the most developed in humans (Moll,
Eslinger et al. 2001), is known for the “executive” functions it possesses (Welsh 1988;
Eslinger 1996; Eslinger 1997). Holistically, these function to maintain an appropriate problem-solving set for attainment of future goals and include functions such as decision- making, cost-benefit analysis, inhibitory control of behavior, attention shifting, planning and programming future actions, otherwise known as prospective memory, and maintaining these representations in mind until implemented, otherwise known as working memory. In essence, executive functions play the role of integrating perceptions, emotions, and value and belief systems to maintain and uphold long-term goals while addressing and adhering to present immediate or short-term goals. As might be suggested from this executive role, humans have the ability, to some degree, to volitionally regulate affective and motivational systems. It is suggested that this kind of regulation is why humans are capable of regulating impulsive, violent behavior that is detrimental to human society (Davidson, Jackson et al. 2000). It is our societal knowledge of this regulatory or
7 volitional capability that allows us to judge ourselves and others, and hence create and enforce mandates punishing violent behavior.
Sociality and Human Health
So far, I have noted that humans are a social species and that we possess complex social features that are unique in comparison to other species in their degree of sophistication. One may inquire why humans are endowed with these highly social capabilities.
Evidenced by the countless educational programs, emphasis on health care quality, intense biomedical and psychological research, and rehabilitation and treatment facilities, the highest goal for our species is to live in a healthy, cohesive, prosocial society. We live in a vast dynamic society, and are capable of as well as benefit from large amounts of social interaction; humans thrive in a social environment (House, Landis et al. 1988).
For example, several studies have demonstrated benefits of our being social in providing evidence that socially isolated persons have higher rates of tuberculosis, accidents, psychiatric disorders, and ultimately higher mortality rates (House, Landis et al. 1988;
Seeman 2000; House 2002; Loucks, Berkman et al. 2006). Humans are particularly salient to social stimuli and are naturally inclined to strive for meaningful social relationships (Bernston 2006). Typically, humans behave in ways that are appropriate for the purpose of approval and the subsequent fostering and maintaining of intimate social relationships (Cialdini and Goldstein 2004). As infants, attachment is a powerful
8 biological drive that sets the foundation for these relationships (Bowlby 1958; Bowlby
1980). Another example of social interaction and its distinguishable correlation to health is that social stressors opposed to non-social stressors seem to be differentiated by the body. An example of this was demonstrated in a study identifying social stressors in comparison to other stressors, to reactivate latent herpes simplex virus type I in humans.
Restraint and shock stress could not induce the reactivations, whereas social reorganization induced reactivations (Padgett, Sheridan et al. 1998).
Humans seem to have a natural “knowing” that health and happiness are highly correlated with our degree of sociality and healthy relationships. The knowledge of the correlation between optimal human health for each individual as well as for society as whole has contributed to a new branch of science that attracts scientists from several seemingly disparate fields, such as anthropology, sociology, psychology, psychiatry, biochemistry, genetics, neuroscience, philosophy, etc. This new branch is known as
Social Neuroscience and focuses on trying to discover the “social brain” (Brothers 2002).
According to Insel & Fernald (Insel and Fernald 2004), the emergence of this branch can be attributed to three major developments 1) cellular and molecular level research demonstrating social behaviors such as filial imprinting, maternal care, and mate preference 2) abnormal social disorders such as autism, Williams syndrome, and schizophrenia 3) and how social isolation effects health. In addition, I would add lesion studies as another development contributing to this field of study.
We, too, are interested in investigating the human “social brain” because of the lack of understanding of these networks and because of the implications that an understanding of these networks will yield to human lives and society. In particular, we
9 are interested in the moral nature or “laws” that guide and regulate complex human social interactions that do not seem to be experienced by other animals (Moll, de Oliveira-Souza et al. 2007). The moral nature of humans is so inseparable to human life that research has shown that we tend to anthropomorphize interactions between inanimate objects, such as triangles, designed to move in a way that is perceived as moral (Weylman, Brownell et al.
1988). In other words, the innate and automatic nature of humans to perceive and judge intentions and actions as “right” or “wrong” is so pervasive that we even tend to translate this behavior to non-human objects. This moral nature that is unique to humans is most likely the result of the emergence of the PFC and related EF functions, and the intricate connectedness observed between cortical and subcortical structures (Eslinger, Grattan et al. 1992; Eslinger, Flaherty-Craig et al. 2004; Eslinger, Robinson-Long et al. 2009).
These developments allow for the acquisition, representation, and integration of social concepts and emotions, the sensitivity and simulation we have to and for others, our amazing capacity for social communication, and our inherent investment in social order.
It is the culmination of these human developments that yields the phenomenon known as morality. It is my interest to investigate this social phenomenon with a particular focus on the involved neural correlates. In the following paragraphs I will explain this phenomenon and will end this introduction by focusing on precisely what I intend to study and why.
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What is Morality?
Before one reads on, it is important to define morality and be able to differentiate it from other forms of social conduct. In layperson terms, morality is typically defined as the general consensus of right and wrong behavior. Although this definition may be acceptable, the true definition of morality is highly complex and remains to be agreed upon by scientists. Lawrence Kholberg (1964), who introduced the study of morality into the realm of empirical research, spent much of his career attempting to discover universal moral laws, or human morality. Later research helped in demonstrating that although morality is clearly a social phenomenon, one needs to be careful as to what differentiates moral laws and rules from social conventions. Decades of research indicate that right and wrong within a society is multi-faceted and can be roughly organized, both conceptually and developmentally (Turiel 1983; Nucci 1997). Individuals tend to have a hierarchy of social behavior, so that some social behaviors are considered to be universal to all social groups and cultures, some are considered to be determined by the individual’s social group and culture, and yet some are considered to be relative to the personal choice of the individual (Turiel 1983; Nucci 1997). Although the boundaries between the levels of this hierarchy are not discrete, the level that includes social behaviors that are typically considered to be universal is the level that most sociologists and psychologists agree comprises morality. These social behaviors would generally include behaviors that compromise or promote the safety and well-being of others and supersede social conventions. Larry Nucci (1997), a pioneer in social cognitive development, defines morality as one’s concept, reasoning, and actions which pertain to the welfare, rights and
11 fair treatment of persons. Conceptually, Nucci’s definition paints morality as the ‘mental coordination’ (Gibbs 2003) of several of the highly complex human social constructs such as learned event sequences, causalities, decision-making, ToM, behavior selection, and inhibitory control that are purposeful in the progression of the human species.
What is the State of Morality Considering it’s Purpose?
As indicated, humans seem to possess the phenomenon known as morality. What is known as the ‘social brain’ has been indicated to generate this phenomenon. Most would agree that the ‘social brain’ network, when optimally functioning, directs social behavior to be cooperative and to strive for the health, safety, and well-being of all persons. When faced with a moral dilemma, most adults tend to do a cost/benefit analysis that yields behavior that reinforces social cooperation (Rilling, Gutman et al. 2002). One must ask “Is this what is observed throughout the human species?” Any cognizant person would have to answer “No.” As with any living system, there are occasional breakdowns.
Scientists have found this to be the case in the ‘social brain’ network. Dysfunction in this neurophysiological network has provided evidence for its existence and encourage future research investigating the involved neural correlates. Four examples of these dysfunctions will be described below and include persons with 1) sociopathy, psychopathy, and antisocial personality disorder, 2) genetic and developmental disorders 3) brain lesions and 4) degenerative disorders.
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1) Antisocial personality disorder, Sociopaths, and psychopaths
The disorders mentioned above are used interchangeably by many scientists, yet by others are thought to differ in minor ways in their severity and behavioral intentions. For example, upwards to 50% of criminals are thought to have antisocial personality disorder, but only 1/3 of those are thought to have psychopathy (Dietz 1992;
Hart 1996). Another example is that persons with psycopathy and persons with sociopathy may commit similar crimes but most often the psychopath’s action is instrumental and purposefully directed and planned to take advantage of someone (Cornell
1996). The sociopath, on the other hand, most often has reactive, but not instrumental aggression that usually interferes with inhibition and may yield a heinous crime (Blair
1995). Regardless of these subtle differences, antisocial personality disorder, sociopathy, and psychopathy share the commonality of an antisocial tendency which has been referred to as a ‘rule-breaking’ tendency (Raine and Yang 2006). Research indicates the majority of human suffering is due to antisocial behaviors, ranging from cheating to murder
(Goodwin and Guze 1996; Douglas and Olshaker 2000). Persons suffering from these disorders typically demonstrate developmental behavior patterns that are ‘immoral’ in the sense that they go against the goal of social cooperation, conformity, and safety for all persons (Augstein 1996; Raine and Yang 2006). Support of the notion that antisocial behavior has ‘immoral’ implications has been longstanding such that psycopathy when first characterized was referred to as ‘moral insanity.’ Between 5-10% of the population exhibit disorders characterized by antisocial behavior (AMN 2006) and that number jumps to 80-85% in criminal populations (Hare 1993). Studies have shown that persons with
13 antisocial personality disorder and psychopathy display a reduced grey-to-white matter ratio in the PFC, reduced autonomic activity (Raine, Lencz et al. 2000), and abnormal orbitofrontal cortex (OFC), amygdala, temporal pole and other brain region activations involved in moral cognition and emotions (Blair 2001; Brower and Price 2001; Kiehl,
Smith et al. 2001). In summary, due to the cortical and subcortical integration and recruitment involvement in social moral and emotional processing, deficits can occur at multiple levels of processing. For example, specific PFC dysfunctions can result in impulsivity and poor decision-making, whereas lesions to limbic and paralimbic regions can impair basic motivational states, such as sexual drive, attachment, and aggressiveness, with both deficits leading to moral violations (Weissenberger, Dell et al. 2001; Eslinger,
Flaherty-Craig et al. 2004). To further complicate identifying the cause(s) of ‘immoral’ behavior, neural damage can affect individuals differently. For example, the ventromedial
PFC (vmPFC), which is the most prototypical region with atypical activation in psychopaths, does not always result in antisocial psychopathic behavior (Barrash, Tranel et al. 2000; Trauner, Nass et al. 2001). Additionally, the way the deficit was acquired can affect behavior, demonstrated by the noted difference between acquired and developmental psychopaths in that the latter is more callous and enacts instrumental aggression directed at taking advantage of others. These complications in cause and effect remain vague, and are in much need of further research.
Typically, individuals act in a general accordance to their beliefs and values. However, there is a noticeable inconsistency or dissociation between moral knowledge and behavior in developmental sociopaths (Blair 1995). Reports show that these individuals are often socially intelligent and clearly know the difference between
14 right and wrong (Link, Scherer et al. 1977). However, their behavior is in opposition to this knowledge. Perhaps, discrepancies can be explained by these persons frequently observed impairment in moral emotions guiding behavior (Blair, 1995). Furthermore, in these populations, Norris & Wilson (2003) found a correlation between animal abuse in childhood and interpersonal violent activity, such as homicides and rape cases, in adulthood. In relation to this finding, forty-five percent of individuals involved in school shootings have a history of animal abuse. In summary, these findings suggest there is a clear link between amoral socially deviant behavior and dysfunction in these networks and that there are probable accompanying developmental implications.
2) Autism, Williams syndrome, Schizophrenia, and Attention Deficit Hyperactive
Disorder (ADHD)
Whereas psychopaths seem to have a specific localized deficiency in social moral processing and behavior (Blair, 1995), it has been proposed that autistics have a more general social impairment (Frith and Frith 1999). Although there is a spectrum of different types/levels of autism, including Autism, Asperger’s Syndrome, and Pervasive
Developmental Disorder Not Otherwise Specified (PDD-NOS), they are all characterized by a triad of symptoms: abnormal social interaction, abnormal social communication, and repetitive and fixated behaviors (Treffert 2006; Lam and Aman 2007). For the purpose of this discussion, I will focus on Autism because of the more profound social cognitive and social emotional deficits that occur in comparison to the other autistic classifications.
Autism is a neurodevelopmental disorder that is usually apparent by the age of three years
15 and has an estimated frequency of 6/1000 in the population (Charman 2002). This percentage has reportedly steadily increased since the 1980’s (Newschaffer, Croen et al.
2007) (this may be due mainly to the broader diagnostic criteria). The cause of autism is still, for the most part, unclear, although it is thought to derive from an early genetic mutation (Abrahams and Geschwind 2008). Post-mortem, morphometric, and functional imaging studies provide substantial evidence of brain abnormalities in autistics. For example, a post-mortem study found that there was increased amygdala cell density in autistic persons in comparison to normal amygdala cell density (Bauman 1988; Rapin and
Katzman 1998). Other studies have shown this increase in cell density yet a decrease in amygdala volume because of reduced neuronal size (Bauman 1988). Brain weight and volume has also been shown to be more profound in autistics (Courchesne, Redcay et al.
2004; DiCicco-Bloom, Lord et al. 2006). Functional imaging studies have shown several structures to exhibit abnormal activation, such as the STS, temporal parietal junction
(TPJ), medial PFC (mPFC), amygdala, anterior cingulate cortex (ACC), cerebellum, and hippocampus (DeLong 1992; Bauman and Kemper 1994; Courchesne 1994; Rapin and
Katzman 1998; Abell, Krams et al. 1999; Allison, Puce et al. 2000). For example, Di
Martino et al. (2009) concluded in a meta-analysis of functional imaging studies that the
ACC and insula were both hypoactivated during social tasks in an autistic group when compared to a control group. More recently, researchers claim that autism is characterized by a ToM deficit (Frith 2001) and that these deficits often produce inappropriate, amoral social behaviors (Capps, Yirmiya et al. 1992; Hillier and Allinson
2002). Given these observations, the study of the social deficiencies present in autistics should provide more insight into the correlation between ToM and moral judgments
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(Young, Cushman et al. 2007). As mentioned earlier, the ‘mirror neuron system’ is thought to be foundational to ToM. Not surprisingly, some researchers have speculated that the characterizations of autism are the result of “broken mirrors,” or dysfunction in this system (Ramachandran and Oberman 2006). Oberman et al. (2005) presented convincing research supporting this notion in an electroencepholography (EEG) study analyzing the mu wave (8-13 Hz), which is known be suppressed in motor neurons implicated in this mirror system. He compared the suppression of the amplitude of the mu wave in a group of autistic children and a group of control children in response to opening and closing one’s own hand and watching another perform the same action. It was found that the mu wave observed in motor neurons was suppressed in the typical children group to both self and other action, but was only suppressed in the self- action in the autistic group, suggesting that a deficit exists in the ability to simulate others. Additionally, the
ACC and insula have implications in the ‘mirror neuron system’ and as mentioned above, atypical activations exist in these regions during social information processing. In accordance to the mirror system, ToM, and related cognitive and emotional social processing deficits observed in autistics, it is not surprising that they also perform poorly on empathizing tasks (Decety and Meyer 2008). A final impairment reported, which is also most likely related to social difficulties, is a significant language impairment (Landa
2007). This impairment is supported by functional imaging studies of atypical hemispheric lateralization in language tasks performed by persons with autism (Kleinhans,
Muller et al. 2008). Based on these data, autism is an excellent model to understand social cognitive and emotional processing and how atypical development of the underlying neural substrates can severely influence social perception and interaction.
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While autistic persons tend to be less engaged in social interaction and communication, persons with Williams Syndrome are quite the opposite. One of the major characterizations of Williams Syndrome is extreme friendliness, extraversion, and empathy. Other less fortunate characterizations are abnormal facial features, mental retardation, hyperactivity, peer difficulties, and cardiovascular problems (Williams,
Barratt-Boyes et al. 1961; Beuren, Apitz et al. 1962). Williams Syndrome occurs in anywhere from 1 in 7,500 to 1 in 20,000 people (Wang, Samos et al. 1997; Stromme,
Bjornstad et al. 2002) and is caused by a deletion of 26 genes on the long arm of chromosome 7 (Peoples, Franke et al. 2000). Neuroanatomical differences have been identified and may explain some of the abnormal cognitive, emotional, and social behaviors observed in these persons. For example, Reis et al. (2003) found that there was increased gray matter in the orbital and medial prefrontal cortices and the amygdala.
Other reports have found reductions in gray matter in the OFC (Meyer-Lindenberg, Kohn et al. 2004). Still others (Reiss, Eliez et al. 2000; Reiss, Eckert et al. 2004), have found the ratio of brain volume to be higher for frontal cortex and lower in the occipital and parietal areas, while limbic function remains normal. Jerningan et al. (1993) concluded that this latter finding could explain the affective component of these persons and their hypersociability.
Schizophrenia is a complex disorder that displays symptoms in the adolescent and early adulthood years, characterized by delusions, abnormal perceptions, cognitive disorganization, and significant abnormal social behavior, and affects approximately 2.4 million Americans (Castle, Wessely et al. 1991; Goldner, Hsu et al.
2002). Enlarged ventricles, increased amounts of cerebral spinal fluid (CSF), and
18 decreased amounts of gray matter are hallmarks of schizophrenia (Pfefferbaum and Marsh
1995; Cannon 1996). In a diffusion tensor imaging (DTI) study of a group of adolescent- onset schizophrenics, Kumra et al. (2005) found that the white matter tracts in the ACC had lower fractional anisotropy (FA) values than that of controls, suggesting less efficient processing in this group of individuals. This was the only region in which a significant difference was found. Kumra et al. raised the possibility that this abnormality could be the cause of the motivational, attentional, memory, and higher-order cognitive deficits common to schizophrenics. A meta-analysis conducted by Ellison-Wright & Bullmore
(2009) identified two more areas that had reduced FA values. The white matter regions were in the left frontal and temporal lobes and included tracts that connected frontal, thalamic, and cingulate regions, and frontal, insula, hippocampus-amygdala, temporal, and occipital regions, respectively. As indicated in these DTI studies, the frontal lobes, and more specifically, the PFC is a region that is known to be a site of dysfunction in schizophrenics (Pauly, Seiferth et al. 2008), a dysfunction commonly referred to as the
‘hypofrontality hypothesis.’ This hypothesis refers to a frontal-striatal dopaminergic pattern constituting an inversely proportional relationship between striatal and frontal dopamine levels. As the hypothesis name suggests, striatal dopamine is higher and frontal dopamine is lower, a relationship that is not observed in normal controls (Meyer-
Lindenberg, Miletich et al. 2002). More recent knowledge of PFC reorganization and refinement during late adolescence have scientists interested in the correlation between schizophrenia and PFC development (Lewis 1997). In particular, the dorsal lateral PFC
(DLPFC) (Weinberger, Berman et al. 1986; Park 1992), has been a site of interest,
19 although, many other regions in the frontal and temporal areas are also implicated in this disorder.
Interestingly, ADHD, the most common mental disorder in children and adolescents (NIMH, 2009), shares several neurologic abnormalities with schizophrenia, such as lower frontal lobe volume, striatal abnormalities, and hypofrontality (Castellanos,
Giedd et al. 1996; Filipek 1996; Casey, Castellanos et al. 1997). Another study showed that ADHD-like symptoms had a higher frequency in young relatives of schizophrenics than in the general population (Keshavan, Sujata et al. 2003). Likewise, studies show that a large percentage of adult schizophrenics, when children, exhibit common ADHD symptoms such as inattention, hyperactivity, and impulsivity (Spencer and Campbell
1994; Alaghband-Rad, McKenna et al. 1995; Rubia, Overmeyer et al. 2000). Due to the known abnormalities common to both schizophrenic and ADHD persons, it is not surprising that a characterization common to both is difficulty in social interactions.
Although similarities exist between schizophrenia and ADHD, which were important to mention for the purpose of this discussion, they are different disorders in onset, severity, manifestations, and symptom control. Many of the symptoms of ADHD are thought to be expressions of frontal lobe malfunction that is the result of delayed maturation (Rubia,
Overmeyer et al. 2000). Dopaminergic projections are known to support the normal development of the frontal lobes (Schmidt, Beyer et al. 1996; Levitt, Harvey et al. 1997), and it is thought that this system is not working properly is the root of the pathogenesis of
ADHD (Ernst, Zametkin et al. 1998; Swanson, Sunohara et al. 1998). Hypofrontality is the hallmark physiological malfunction of this disorder and causes the reduction in higher- order executive control associated with ADHD (Rubia, Overmeyer et al. 2000; APA
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1994), which can often lead to inappropriate social behavior. Conduct disorder (CD)
(which is often considered the ‘under 18’ classification of sociopathy and/or psychopathy) with the comorbidity of ADHD is the strongest indicator of criminality and delinquent behavior (Wilson 2003). Taken together, these findings provide strong evidence that structures, such as the PFC, play a key role in healthy social behavior and when malfunctioning can severely impact one’s ability to navigate in the social world and in some cases, pose a threat to society.
3) Lesions to parts of the ‘social brain’
The prototypical case study of brain damage resulting in social and emotional behavior abnormalities is the case of Phineas Gage (Harlow 1868).
Neuroscientist, Antonio Damasio (1994), credited this case to the “the historical beginning of the study of the biological basis of behavior.” In 1848, Gage, a railroad construction foreman, encountered a severe accident when a tamping iron shot from the ground through his jaw bone, eye, and prefrontal cortex, before exiting his skull. Amazingly,
Gage survived, but suffered drastic changes in personality and decision-making. After the accident, he became impulsive, impatient, unable to keep a job, poor at decision-making, and had substantial social and emotional impairments. Since Gage’s case, there have been numerous cases reinforcing the notion that brain locality and function are linked and more specifically, that the PFC is a region constituting various subregions functioning together to play an executive interactive role in one’s life. Numerous brain lesions studies have demonstrated that damage can be localized to specific regions yielding social impairments
21 while other constructs, such as memory and crystallized intelligence, continue to function normally. For example, Eslinger and Damasio (1985) presented a case study on patient
EVR, who at the age of 35, underwent surgery to remove an OFC meningioma. Prior to this incident, EVR was a stable worker, reliable family man and role model. After the surgery, he demonstrated traits similar to Gage, such as disorganization, unreliability, and restrained and severed social relationships. Despite these higher-order executive and social dysfunctions, EVR performed normally on neuropsychological testing. A group study conducted by Goel et al. (2004) compared persons with frontal lobe lesions to a control group, using the Wason Card Selection Task as a comparison measure. This task includes non-social and social reasoning tasks. There was no significant difference between control and experimental groups in the non-social reasoning task, however, a significant difference existed between groups in the social reasoning task, with left- frontal-damaged patients having the lowest scores. Furthermore, IQ and memory tests were not confounding factors to this finding. These researchers also found that frontal asymmetry increased with levels of social knowledge presented in normal controls but was limited in the experimental group. Tranel et al. (2002) also demonstrated asymmetric differences between PFC areas. They compared persons with vmPFC lesions based on right or left hemisphere location, and found that a greater social behavioral, decision- making, and emotional impairment resulted from right hemispheric vmPFC lesions.
Several adult studies have shown deficits in correct interpretation of social cues, understanding another’s perspective, and normal social responses following frontal lobe damage (Prigatano 1991; Channon and Crawford 2000). For example, specific deficits in
22 story comprehension and ToM tasks following left anterior frontal damage have been observed (Channon and Crawford 2000).
Several PFC regions are involved in social cognition and emotions and the complexity of these regions and their interconnections is evident in that different social tasks selectively recruit relevant neural substrates. Hornack et al. (2003) demonstrated this notion in showing that patients with OFC and ACC damage had significantly lower scores on a social and emotional behavior questionnaire than patients with damage to the
DLPFC and mPFC. Another research group, Bechera et al. (1994) created the Iowa
Gambling Task to evaluate higher-order cognitive and motivational mechanisms by simulating real-life decision-making. During this task, participants have decks placed in front of them and choose cards, with each card having a monetary reward or loss. After several selections, normal participants will see trends in decks that have more ‘loss’ cards and will refrain from those decks and will show a heightened galvanic skin response when hovering over a ‘bad’ deck. Patients with vmPFC (including OFC in this study) damage have a significant reduction in their ability to modify their behavior to avoid these losses or ‘punishments’ and also do not exhibit the heightened galvanic skin response. Other researchers have also found dorsomedial and DLPFC lesions to result in poor performance in this task (Manes, Sahakian et al. 2002). In support of the importance of the vmPFC in guiding decision-making, Koenigs et al. (2007) showed that patients with vmPFC damage increased their utilitarian responses in a moral judgment task. Whereas normal and patient groups responded the same on low-conflict scenarios (clearly right or wrong moral action to judge), patient groups responded differently on high-conflict dilemmas (e.g. pushing stranger on trolley tracks to save five lives while stranger would be killed) in that
23 they chose saving the greater number of people despite the emotional moral violation experienced by normal controls. Rolls (1999) discussed the role of ventral PFC neurons in rapid stimulus-reinforcer associative learning based on environmental contexts and how this is the basis of reversal and extinction learning. He showed that patients with damage to the OFC in particular exhibited impairments in the extinction and response-reversal tasks (Rolls, Hornak et al. 1994). Another related observation of this area is by Damasio in what he coins the ‘somatic marker hypothesis.’ In this hypothesis, Damasio claims the ventral PFC is essential for making appropriate decisions in the midst of rapid changes associated with the social environment. He posits that patients with ventral PFC damage have adequate social knowledge but have difficulties accessing or utilizing this knowledge when decisions are to be made in real-life situations (Damasio, Tranel et al. 1990).
Lastly, Shamay-Tsoory & Aharon-Perez (2007) conducted a study that investigated both cognitive and affective in various PFC sectors. They focused on these components within the domain of ToM with patients separated into four groups: vmPFC lesions, DLPFC lesions, posterior lesions, and a healthy control group, and found the vmPFC group to have significant impairments in the affective ToM condition. Across subjects, the more extensive PFC damage resulted in more cognitive ToM impairments. Shamay-Tsoory et al. concluded that partially dissociable cognitive and affective components of ToM exist in the PFC. The presented adult PFC lesion data highlight the multi-faceted integrative roles of various sectors of the PFC and how the intactness and proper functioning of this unit is able to engage in higher-order executive control functions that facilitate decision- making and behavior in a dynamic social environment.
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It is important to note that the PFC altercations can result in changes in its interconnected cortical and subcortical regions, such as changes in cellular connectivity, brain weight, dendritic arborization, and spine density (Goldman and Galkin 1978; Kolb,
Petrie et al. 1996; Kolb, Gibb et al. 2000). On the same note, lesions to several other areas associated with this frontal region, such as the amygdala, are known to influence social and emotional behavior. One such case, S.M., investigated by Adolphs et al.
(1995a; Adolphs and Tranel 1999), demonstrates this point. S.M. suffered from selective bilateral amygdala damage. Although she could draw facial expressions for most emotions, she had a difficult time drawing a facial expression for fear. She also could rate the valence of negative emotions, but could not rate the arousal of these emotions.
Although, perhaps not as devastating to social functioning as PFC damage, impairments could be problematic or even life-threatening depending on the context of the situation.
A study conducted by Kling (1972) supports this claim. He performed bilateral amagdalectomies on monkeys before releasing them to their natural habitat and found that most of the amagdalectomized monkeys estranged themselves from their social groups and eventually died as a result, suggesting the social implications of the amygdala. Kling
& Steklis (1976) conducted a similar study but with temporal pole ablations. Similar to the amygdalecomized monkeys, social impairments were detrimental; temporal pole ablations in monkeys resulted in the loss of normal emotional attachments to infant and peer monkeys. Resection surgery of the temporal pole in humans has resulted in impairments in retrieving face-name associations when left surgeries were performed
(Tsukiura, Namiki et al. 2003) and in impairments in recognizing personally familiar and famous faces when surgeries were on the right (Tippett 2000). Although only amygdala
25 and temporal areas are discussed as additional areas needed for social and emotional processing, there are many more that cover diffuse areas of the brain, and are supported by brain lesion studies. These regions include the insula, basal ganglia, precuneus, posterior cingulate, STS, and TPJ, and will be discussed in further detail later in this discussion.
The lesion data presented thus far reviewed adult studies. Although much smaller in number, lesion studies in children and the developmental effects exist and are pertinent to the interests of this dissertation. Eslinger et al. (2004) reviewed ten patient cases with early prefrontal cortex damage, in areas such as the DLPFC, mPFC, and
OFC/polar regions, and the detrimental effects of those injuries, with the majority having overwhelming social, moral, and behavioral deficits. For instance, one of the cases, JP, suffered from bilateral PFC damage (Ackerly and Benton 1948) and had a long history of interpersonal difficulties and grossly abnormal social behaviors due to impairments in executive functions, such as inhibition, attention, and working memory. Another case reviewed, DT, (Grattan and Eslinger 1992), had left PFC damage and was reported to have an arrest in social, emotional, and moral development, and impairments in cognitive flexibility, planning, and decision-making. Anderson et al. (2007) reported a case study of a 14 month old child, ‘PF1’, who, upon only 3 days old, underwent resection surgery of a vascular malformation in the right inferior DLPFC. Although his neurological exam and his mother’s ratings of social communication, motor skills, and living skills were normal, he had severe impairments in emotional regulation and engaged attention. PF1’s impairments were particularly noticeable in unstructured situations. Other studies by
Bechera et al. (1999) and Pennington & Bennetto (1993) show that early PFC lesions acquired within the first 16 months and 10 years of life, respectively, result in subsequent
26 impulsive, antisocial behavior. Bechera et al.’s study followed the patients (an individual with bilateral polar and vmPFC damage, and an individual with polar medial dorsal PFC damage) into adolescent and adulthood and noted persistent delinquent and criminal behavior. A significant finding highlighted by researchers and evident by the children lesion literature, is that not only locality, but when the brain damage occurred along the developmental trajectory, is of key importance to the aspects of impaired moral, social, and emotional behavior (Price, Daffner et al. 1990; Eslinger, Grattan et al. 1992;
Anderson, Bechara et al. 1999; Eslinger, Flaherty-Craig et al. 2004).
The few cases of the adult and children brain lesion reviewed are only representative of the copious volume of others studies demonstrating moral, social, and emotional impairments as a result of localized brain damage. PFC lesions seem to be the most directly correlated with these social impairments as they specifically interfere with planning, decision-making, attention, self-control, emotional regulation, working memory, memory for spatial and temporal patterns, and the mismatch between intent and execution
(Casebeer 2003). However, damage to more widespread brain areas in the subcortical, temporal and parietal areas, which may be more involved in the bottom-up stage of processing in that they perceive, recognize, and represent relevant stimuli, and motivate behavior are also known to produce gross deficits in moral, social, and emotional processing. The lesion data provide clear supportive evidence that there is a dedicated large scale neural network represented across different areas of the brain that function to process social information and regulate social behavior.
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4) Frontal Temporal Dementia (FTD)
FTD, which is classified by the degeneration of the frontal lobes and may extend to the anterior temporal lobes, typically occurs in years 40-50. There are three variants of FTD which include a Behavioral, Semantic Dementia, and Progressive
Nonfluent Aphasia (UCSF Memory and Aging Center). For the purpose of this discussion, we will focus on the so-called “Behavioral” variant of FTD (bvFTD), because of the associated social cognitive and emotional changes. The major characterizations of bvFTD are personality, behavioral and EF dysfunctions, all of which lead to a noted decline in social moral behavioral processing (Snowden, Neary et al. 2002; Miller, Diehl et al. 2003), and sometimes disruptive antisocial behavior (Miller, Darby et al. 1997).
Eslinger et al. (2007) conducted a study on persons with bvFTD, otherwise known as
‘social and executive function disorder’, compared to persons with language disorders.
Participants were administered tests and ratings that evaluated social judgments, ToM, and empathic sensitivity. BvFTD patients were impaired in all measures compared to the control group. Additionally, in the same study, Eslinger et al. showed, via MRI voxel based morphometry, that cortical atrophy in the right OFC, superior temporal, visual association and posterior cingulate regions correlated to the identified social impairments.
Other research also supports the link between bvFTD and these social impairments in EF,
ToM, empathy, and behavior (Kipps and Hodges 2006; Viskontas, Possin et al. 2007).
Viskontas et al., (2007) focused particularly on the OFC deficit in bvFTD and presented research on the resulting impairments in behavioral regulation, complex stimulus-reward reverse learning, and inappropriate social judgments. They also note the vulnerability of
28 the ‘large-spindle shaped’ neurons (noted previously as specialized for complex social systems) to this disorder in that FTD patients have a 74% reduction of these neurons in comparison to healthy controls (Seeley, Carlin et al. 2006). Moreover, neighboring pyramidal cell reduction was not significant, suggesting that social processes are selectively targeted in this disease. Another example of this selectivity is that physiological and negative emotional reactivity are reportedly normal but there is a reduction in self-conscious emotions, such as empathy (Sturm, Rosen et al. 2006). The presented data provide substantial evidence that the differentiated regional and functional components of the ‘social brain’ are affected by FTD pathology.
Note on the Discussed Dysfunctions
It is important to note that not every antisocial or abnormal social act is committed by someone who has a disease, disorder, or damage to the brain. All of us most likely have committed what would be classified as an antisocial act at one time or another. This is the nature of countless decisions every day that are highly influenced by external circumstances and interoceptive cues. However, when this antisocial or atypical behavior persists, or reaches a certain magnitide, concern should be noted. In particular, when these behaviors are goal-directed and pre-mediated as observed in psychopaths, concern should not only be noted for the health, well-being, and safety of the individual, but for other individuals in society.
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It is also important to note that interindividual differences exist in humans and that external circumstances contribute to these differences (these external factors will be discussed later in this introduction). Despite interindividual differences, it is important to recognize our sense of self, and the control we are able to exert over behavior (although the degree of this control is controversial). It is generally assumed that we are able to play the role of “judge” over much of our overt behaviors. As we develop a moral identity, our hierarchies of right and wrong are established. An apparent problem is when our experiences or innate biology create distorted beliefs or perceptions of right and wrong.
An example to illustrate this distortion could be an individual who believes he/she
“deserves” something and rises above rules or hurts someone to retrieve it. Another illustration is a classic moral dilemma of a doctor who lied to protect his friend from a malpractice issue. A final illustration is reported of delinquents who often justify their actions and do not view those actions as immoral but as “business” and often consider themselves as respectful and good people (Guerra 1994). It is evident that the confounding factors involved are numerous and extremely complicated, especially when considering one’s own perception may be distorted to believe he/she is being benevolent when in reality, others are being harmed or mistreated. The healthy development and establishment of perception and a moral framework is vital for social behavior.
In summary, diminished social richness, well-being, and health benefits experienced by those suffering with social impairments, whether developmental or acquired, and the protection sought from aggressive and violent acts exercised by individuals with specific antisocial disorders, such as psychopathy, are chief motivators for the present research. The presented research will provide a template of developmental
30 social moral processing in the brain for understanding and future training, prevention, and rehabilitation programs aimed at relieving persons burdened with social disorders, at the individual and societal levels.
Investigating Morality
Good and right moral judgments are paramount to civilized life (Casebeer 2003;
Gibbs 2003). Our moral nature, in its optimally functioning state, would yield a society free of antisocial behaviors, such as violence and crime. Knowing this, it is astonishing that only recently, social neuroscience has seriously investigated human moral cognition.
It is becoming increasingly apparent that we are in great need of an understanding of the neurophysiology and circuitry underlying moral cognition and behavior for the identification of social/moral pathologies, prevention and treatment, guidance of moral education and training, social and economic policy, and practice and enforcement of law
(Moll, de Oliveira-Souza et al. 2005; Blakemore and Choudhury 2006).
The neuropsychological, as well as the neurobiological underpinnings of moral judgment and moral behavior, both static and developmentally, are minimally understood.
Fortunately, as of late, great interest in these processes has provided the initial foundation of understanding the regions involved. Animal model experiments have shed light on several aspects of basic/primary emotions and classic and operant conditioned behaviors.
However, the behavioral complexity and flexibility, and more secondary cognitive social emotions observed in the social moral behavior of humans, for the most part, can only be
31 investigated by using human models for research. Lesion, event-related potentials (ERP), positron emission tomography (PET), functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) studies have been especially helpful in their contributions to understanding localization and function of the brain networks involved in processing social moral information.
A small number of adult studies have been conducted on the neural substrates underlying cognition and emotion involved in moral emotions, but to our knowledge, no studies have directly investigated these substrates in children. Even related studies to our current research, such as empathy to others in pain and the mirror system in watching another’s motor movements, are very limited in their study in children (Ohnishi,
Moriguchi et al. 2004; Decety, Michalska et al. 2008). The adult studies will provide a foundation for child moral development studies in that they will most likely be indicative to the neural systems involved in moral cognition, emotion, and motivation. Adult imaging studies and brain lesion data indicate that the neural substrates/systems involved in morality are 1) anterior and posterior temporal cortices, including the STS and TPJ, that generally function in social perception, 2) prefrontal cortices, including the OFC, mPFC, and DLPFC, which generally function to represent event sequence knowledge, and 3) limbic and paralimbic systems for motivation and emotion induction (Farrow, Zheng et al.
2001; Moll, Eslinger et al. 2001; Moll, de Oliveira-Souza et al. 2002; Heekeren,
Wartenburger et al. 2003; Greene, Nystrom et al. 2004; Harenski and Hamann 2006;
Schaich Borg, Hynes et al. 2006; Moll, de Oliveira-Souza et al. 2007; Young, Cushman et al. 2007; Eslinger, Robinson-Long et al. 2009).
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Due to the lack of study on children and development in this research domain and the prevalence of social disorders and associated social concerns, the current research is of utmost importance and of great need for its future applications to all of society. I propose specifically to investigate moral judgment and social emotional development in children, because of its key role in moral-decision making and moral behavior (Nucci 1997). Using fMRI, I propose to investigate the interplay of cognitive and affective components subserving these developments in children and adolescents, focusing on systems/networks identified in adults.
Behavioral Development
This complex integrated processing, yielding social moral behavior, is not fully established upon birth, or even during childhood. Morality is a developmental process that has recently been theorized to parallel maturation of brain systems, the social information that is represented in these systems, and the efficient processing of these systems. In the next several paragraphs, I will describe these developments, first the behavioral manifestations of these developments, and then the neural correlates theorized to generate these behaviors.
In humans, the first signs of social cognitive development is apparent around one year of age for humans, such that infants can attribute agency to different entities (Spelke
1995; Johnson 2003) and by one and a half years, demonstrate a realization that these agents have intentions. For example, infants begin to follow the gaze of an adult towards
33 a goal (Carpenter, Nagell et al. 1998). Additionally, children, unlike other primates, understand triadic reasoning, which can be thought of three destination points/relationships among people or object (i.e. I see that you are pointing to the box and telling me there is food inside). In comparison, primates are limited to dyadic reasoning
(Tomasello, Carpenter et al. 2005). Young children begin to label basic emotions in self and other (Oatley and Jenkins 1992). These few examples, no doubt, are precursors to more sophisticated social constructs seen in humans, such as ToM/ mentalizing which are typically observed when children successfully complete false-belief tasks (around 4-6 yrs.) (Flavell 1999), working memory, and social/moral emotions. The brain structures that underlie these phenomena are the antecedents of a social brain “network” that continues to develop well beyond early childhood.
Kohlberg (1964), like his predecessor Jean Piaget (1968), focused on cognitive development but narrowed his scope to the moral domain. Kohlberg spoke of moral development in terms of “cold” cognitive stages. Similar to previous theorists, such as
Immanuel Kant and John Stuart Mills, Kholberg stressed cognitive and rationale control as key to moral development and socialization.
In contrast to Piaget and Kohlberg’s cognitive development approach, Martin
Hoffman (Hoffman 2000), like philosopher David Hume, focused more on the ‘hot’ affective component involved in moral development. Hoffman primarily researched empathy and its role in moral maturity and claimed that empathy is the “spark of human concern for others, the glue that makes social life possible.” Empathy has been defined by other researchers ‘as sharing the emotional state of others and understanding it in relation
34 to oneself’ (Eisenberg 2005; Decety and Lamm 2007). According to Hoffman, taking others concerns and perspectives into consideration is key to moral development.
A theory of moral development constructed by John Gibbs (2003) incorporates the
‘hot’ affective and “cold” cognitive components of both theories and categorizes stages into immature and mature categories that can continue to develop into adulthood. He agrees with the general theme underlying both theories, which is moral development beginning with a superficial, self-centered, hedonic mentality and developing into a reflective, empathetic, other-centered mentality, while coinciding with increased socialization (Gibbs 2003). Gibbs coins this process as ‘decentration.’
Neuroscientist and neuropsychologist, Paul Eslinger, discusses this transition in light of the relevant literature and of the Concrete Operations Stage of Piaget’s Theory of
Cognitive Development period as introducing new abilities that allow for ‘other’ processing that is crucial for normal social interactions (Flavell and Botkin 1968; Selman
1971; Flavell, Miller et al. 1993; Eslinger, Flaherty-Craig et al. 2004). Eslinger discusses how the Concrete Operations stage is where the child begins to make ‘mental representations’ that are then elaborated upon to become ‘representational knowledge’ and again elaborated upon to become ‘working knowledge’ as the representations become malleable so as to be able to interact with a dynamic environment. This process requires, for example, each social situation to be processed differently due to different persons, intentions, actions, and contexts. The constituents that are represented and manipulated in the ‘working knowledge’ state are the foundation for social cognition and abilities, such as attributing beliefs, values, desires, and intentions to others (ToM), social response
35 reversals, and prioritizing goals, and are essential for the dynamic flexible social environment experienced by humans.
In conjunction with the development of different forms of knowledge, Piaget
(1968) explains how children begin to organize and group objects and events into sensible categories and sequences, which can be modified into new grouping or sequences based on future experiences. Language, unique to humans, is thought to be the bridge to how we can use these symbols and extensively categorize them for later representations
(Nusbaum 2006). This cognitive organization is pivotal for the acquisition of social and moral rules, event sequences, causality, and behavioral regulation. In this respect, children in this stage tend to be particularly rule-based and rely on external rules and regulations to guide their behavior. This childhood trend was also highlighted by
Erickson (1950) in his theory of psychosocial development. The transition between the eight stages of his theory includes the transition from a rule-based frame of thinking and behaviors that are mostly determined from outside sources or pressures from authority figures to a more abstract frame of thinking and the development of internal standards and goals in a kind of moral identity. As individuals develop and continue to interact with the dynamic social environment, they become less rule-based, are more sensitive/aware/in tune to the context of the situation (Flavell, Miller et al. 1993) and more concerned with the intention rather than the outcome of the behavior (Schultz 1986; Yuill 1988; Zelazo,
Burack et al. 1996). Additionally, children also have a tendency to extend their personal rule and intention analysis to others behavior, due to social constructs such as ToM
(Flavell, Miller et al. 1993).
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In parallel with Gibb’s notion of ‘decentration,’ Nucci (1997) extends this representation from self to one’s cultural group within society. He suggests that one transition that occurs during early and late adolescence is the differentiation between social conventions and their relevance to one’s particular social group and a second-order morality that is held supreme over these social conventions. Erickson (1950) acknowledges a similar more global frame of thinking in his stage Learning Identity vs.
Identity Diffusion in which the adolescent comes to the full realization of his/her membership and attempts to discover the ‘self’ and the role of self within society. A shift in social thinking is observed as adolescents become more self-aware and self-reflective
(Steinberg 2005) and as one’s moral identity begins to develop upon moving beyond purely salient external stimuli and guides for behavior to more internally guided, ‘other’ focused behavior, such as perspective-taking and empathy (Eisenberg and Miller 1987;
Eisenberg 1995; Eisenberg, Carlo et al. 1995; Eisenberg 2005).
In adolescence, and even more so, young adulthood, one observes the complete establishment of the social brain and the enablement of the highest levels of morality it permits. Abstract thought, complex moral reasoning, and intimate reciprocal relationships, are examples of human behavior, that are frequently partaken of due to the sophisticated capabilities resulting from the integrated and efficient processing of the underlying neural networks (Rest 1979; Colby 1983; Rest 1983; Eisenberg 1998;
Eisenberg 2005). This fits in nicely with Erickson’s stage of Intimacy vs. Isolation that emerges during early adulthood. In essence, all of the tools necessary for this highly complex reciprocal relationship have finally been established.
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In summary, although there are slight differences between the developmental theories discussed above, a common theme is that development entails transitioning from the superficial to the more profound (Gibbs 2003). In conjunction with this transition are four parallel streams of development taking place: 1) internalization of rules 2) language development and acquisition of social knowledge 3) self to other focus (entailing ToM, empathy, perspective-taking) and 4) social group/culture scope extending to all of society.
Why Children and Adolescent Focus?
In this next section, the discussion will be primarily concentrated on the children and adolescent development in contrast to the entire scope of development from birth to adulthood covered in the prior section.
As touched on throughout the last section, I am interested in studying this neural bases of moral cognition in children and adolescents for three reasons: 1) this age group experiences the highest degree of socialization 2) the research on this age group is minimal and 3) neural correlates of interest are known to continue to develop into adulthood. Below I will discuss this age group, what we know of their neural and behavioral development, and the need to study social/moral cognition within this group.
Although the terms adolescents, children, and juveniles are often used interchangeably and the distinctions are often unclear, puberty is thought to be the event that separates childhood from adolescence. Postnatally, it is considered the most profound and extensive period of change in one’s life (Petersen 1988). The commencement of
38 puberty is marked by physiological changes such as sex-specific pubertal hormones, and the physical changes that result. These neuroendocrine changes are thought to be coupled with changes in brain organization, glucose utilization, cerebral metabolism (Halpern
2000; Spear 2000), and behaviors such as self-identity, self-consciousness, and cognitive flexibility (Rutter and Rutter 1993). In summary, immense physical, hormonal, and neural changes inevitably influence social behavior and cognition in profound ways
(Blakemore and Choudhury 2006).
In the past decade, due to the technology explosion, the level of social interactions has increased exponentially (Adolphs 2001). E-mail, cell phones, text messaging, web-cams, i-phones, Face Book, and My Space are several examples of the reality of being social during the majority of ones day. The age group that is growing up with this lifestyle as the “norm” is the current children and adolescents, who are perhaps, the most social persons on the planet. Persons in this age range spend more time socializing than in any other time of development and experience the most rapid level of socialization (Harris 1995; Varlinskaya and Spear 2008). The large amount of time spent interacting with peers during this age range is a crucial for normal social development
(van den Berg, Hol et al. 1999). A significant increase in size and complexity of one’s peer group as well as the exchange of personal thoughts and feelings via chosen friendships is noted as one enters adolescence (Crockett 1984; Csikszentmihalyi and
Larson 1984; Youniss 1985). During heightened socialization, social communication, both verbally and non-verbally, is refined as one learns how to express and understand self and other and the integrated relationship of the two. Undoubtedly, the unprecedented
39 capacity humans have for language, learning, belief and intention inferences, and complex diversified social emotions undermine these processes.
It is also thought that adolescence differs from prior life stages because of the increased number of social, relational, emotional and physiological challenges presented to the adolescent and the pressure to, somewhat independently, effectively deal with these challenges (Petersen 1988). Adolescents are able to deal with these challenges because of their increased ability to engage in abstract thought, organize, plan, increase focused attention to salient stimuli, self-regulate behavior in a goal-directed fashion, interpret emotional and social cues, and appreciate and have a greater dependence on interpersonal relationships (Thomas, King et al. 1999; Luna, Thulborn et al. 2001; Herba and Phillips 2004; Yurgelun-Todd 2007). This stage of life is comprised of emotional and cognitive maturation that provides the capabilities to function independently as an adult
(Spear 2000). Petersen (1988) claims that this may be the first stage of life that delineates
“mature patterns of functioning” that will be utilized in adulthood. If this claim is true, the importance of this stage of life as a foundation for adult patterns of thinking and confronting and resolving problems is of utmost importance for further research.
The term adolescence was not even coined until the beginning on this century
(Hall 1904). Even more surprising is that the first paper to be published focusing solely on adolescence was in 1988 (Petersen). There is an extensive amount of research on early experience and development in infancy and early childhood but relatively little on development after this period. The idea that the brain continues to develop after childhood is rather new and is largely due to the fact that much of the research has been carried out on animal brain tissue of species that do not have the extended period of adolescent
40 development seen in humans (Yurgelun-Todd 2007; Blakmore & Choudhury 2006). In the 1960’s and 70’s, research on post-mortem brains showed that some brain areas, such as the PFC, continue to develop well beyond childhood. In the 70’s and 80’s research revealed the anatomical/structural changes that occurred during adolescence (Clarke and
Clarke 1976; Huttenlocher 1979; Brim and Kagan 1980). Brain imaging further confirmed these findings and helped to study human adolescent development and found that several areas of the brain continue to develop post-early childhood. More evidence for continued neural development in adolescence stems from the disorders that are known to develop at the end of adolescence, such as schizophrenia (Pauly, Seiferth et al. 2008).
Whereas it has been known for decades that sensitive periods of brain development occur in early childhood, only recently has attention been drawn to
“sensitive” periods of development in adolescents and more particular, sensitivities to the social environment. For example, there seems to be varying degrees of successful face recognition depending on age wherein it increased from 6-10 years of age and then decreased around puberty and then increased after this period (Herba and Phillips 2004).
Another study supporting the sensitivity of this stage found a correlation between the known “risky” behaviors of adolescents and brain activation differences in the mesolimbic circuitry between adolescents and adults (Bjork, Knutson et al. 2004). Reduced activation of the right ventral striatum and the right amygdala was identified while anticipating gains in adolescents which was interpreted as adolescents need to engage in more outrageous behavior for more of a greater reward effect. Another study asking adults and adolescents to respond to scenarios as either a ‘good idea’ or a ‘bad idea’ showed that adolescents took much longer to respond to the bad scenarios as ‘bad idea’
41 and during these activations activated more the DLPFC, which plays a role in cognitive control, to a higher degree than the adult group (Baird 2005). The explanation given for this was that adolescents rely more on reasoning whereas as adults rely more on a visceral response when predicting future outcomes (Blakemore and Choudhury 2006).
In addition to these studies, lesion studies have been instrumental in demonstrating that childhood and adolescence is a sensitive period of development. For example, as mentioned in the previous section, Eslinger et al. (2004) discussed ten patients with early prefrontal cortex damage, in areas such as the DLPFC, MPFC, and OFC/polar regions, and the detrimental effects of those injuries, with the majority having overwhelming social, moral, and behavioral deficits. A significant finding in Eslinger’s research was that not only locality, but when the brain damage occurred along the developmental trajectory, was of key importance. For example, it has been shown that adults that acquire vmPFC damage may have behavioral social impairments but perform normally on moral reasoning tasks. Children that have damage to this same area seem to have an arrest in the development of functions related to this area resulting in severe behavioral and moral reasoning impairments (Eslinger, Grattan et al. 1992; Anderson, Bechara et al. 1999).
Behavioral impairments in both are similar to impairments observed in psychopaths (Hare
1970). The PFC and the numerous areas directly and indirectly connected to it, such as limbic, paralimbic, anterior and posterior temporal cortices, TPJ, and posterior cingulate, have recently been acknowledged as regions involved in social moral information processing (Farrow, Zheng et al. 2001; Moll, Eslinger et al. 2001; Moll, de Oliveira-Souza et al. 2002; Heekeren, Wartenburger et al. 2003; Greene, Nystrom et al. 2004; Harenski and Hamann 2006; Schaich Borg, Hynes et al. 2006; Moll, de Oliveira-Souza et al. 2007;
42
Young, Cushman et al. 2007; Eslinger, Robinson-Long et al. 2009). Some of these areas, such as the PFC and TPJ, have been studied developmentally and have been shown to play key roles in executive function and theory of mind development, respectively
(Thatcher 1991; Case 1992; Saxe and Kanwisher 2003; Eslinger, Flaherty-Craig et al.
2004; Saxe and Wexler 2005). Executive functions are thought to continue to develop and be elaborated upon throughout childhood and into adulthood as individuals are interwoven into society and gain independence (Denckla 1996). This development allows for individuals to confront the challenges of planning, prioritizing goals, and being able to modify these plans and goals within different contexts (Grafman 1995; Miller and Cohen
2001). Damage to the frontal lobes associated to executive functions and corresponding developing systems involved in social moral cognition has detrimental effects on the acquisition of moral knowledge and the execution of appropriate social moral behavior
(Eslinger, Grattan et al. 1992; Anderson, Bechara et al. 1999).
The marked improvement in executive functions in normal children partially results from the reorganization of the PFC (Anderson, Anderson et al. 2001). Compared to sensory and motor systems, PFC neuronal myelination and synaptogenesis occur much later in development (Casebeer and Churchland, 2003; Fuster 1997). The developments coincide with behavioral and emotional maturity in children and adolescents as you see an increase in impulse-control, self-regulation, and ToM capabilities. Additionally, the PFC has a central role in the internalization of moral values and norms throughout development as cultural and contextual information is integrated (Grattan and Eslinger 1992; Anderson,
Bechara et al. 1999; Eslinger, Flaherty-Craig et al. 2004). The volume of PFC has been associated with greater abilities of adolescents to inhibit behavioral response or self-
43 regulation (Brocki and Bohlin 2004). Not surprisingly, it has also been shown that the
PFC does not reach its full volume until the early twenties (Sowell, Peterson et al. 2003;
Gogtay, Giedd et al. 2004). While the PFC undergoes the most pronounced course of development in the human brain, another structure contributing to executive-related functions, the STS, undergoes similar development but is more delayed than the PFC
(Giedd 2004). There is an increase in gray matter in the PFC up until puberty and a subsequent decrease into early adulthood. In conjunction with this decline, after puberty, there is an incline of white matter density extending into adulthood. Sowell et al. (1999) suggest that these changes are the largest in the dorsal, medial, and lateral regions of the frontal lobes in comparison to the parietal and the occipital lobes. Moreover, the decrease in gray matter and increase in white matter is an experience-dependent pruning process
(Blakemore et al., 2006). Research conducted by Bunge et al. (2002) suggests that faster reaction times (RT) and more focal activation in the frontal cortex in adults compared to children in tasks, such as GoNoGo, reinforce the idea of pruning and efficiency of neural networks. In conclusion, the two developments occuring during adolescents 1) synaptogenesis followed by synaptic pruning (Cragg 1975; Goldman-Rakic 1987; Rakic
1995), and 2) axon myelination are species and brain-region dependent (Reiss, Abrams et al. 1996; Giedd, Blumenthal et al. 1999; Barnea-Goraly, Menon et al. 2005), and have been proposed to potentiate significant connections while eliminating inefficient seldomly used connections for increased efficiency. Since the PFC and STS markedly mature during adolescence, it is thought that the functions associated with these regions also mature during this time (Casey, Trainor et al. 1997; Sowell, Thompson et al. 2002).
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Factors Influencing Development
Social behavior, whether inhibited or executed, is a result of a complicated interplay of neural systems that is generally similar for all persons, but due to unique life experiences and differing perceptions is specific to each individual. Unique life experience and the subsequent differing perceptions are the result of a myriad of effectors, such as genetics, culture, quality of parental care, family structure, stress, and socioeconomic status (SES) (Meaney, Diorio et al. 1996; Crabbe, Wahlsten et al. 1999;
McCrae, Costa et al. 2000). Although as humans we experience similar stages of development, it is clear that the developmental trajectory is influenced by these factors.
An example of external influence has been demonstrated in a study showing that the visual cortex of rats who were raised in what would be comparable to a human in a very low SES, showed reduced dendritic arborization and synaptic density than rats who had been raised in an environment similar to a human from a higher SES (Turner and
Greenough 1985). Human research has shown that education level, SES, and moral judgments are positively correlated (Rest 1979; Triandis 1990; Mason 1993). However, the interpretation of these results must be cautioned because other components, besides moral judgments, constitute moral behavior, such as empathy. With that said, lower level
SES children may have been exposed to more distressing social situations and may have experienced more sympathy or empathy, which are both components for prosocial behavior, which is a sign of moral maturity (Hoffman 1993; Eisenberg, Zhou et al. 2001).
Another factor to consider is familiarity or security. Research has demonstrated that
45 socialization has been thwarted when older adolescent (as well as adult) rats are placed in an unfamiliar setting (anxiogenic condition) (File and Hyde 1978; Varlinskaya and Spear
2002). Varlinskaya & Spear (2008) demonstrated that young adolescents are particularly sensitive to isolate housing. Yet other factors include maternal and paternal care, which has been shown to permanently effect synaptic density in the limbic system in such a way that predicts reactivity to stress (Meaney, Diorio et al. 1996). At the neurochemical level, external factors during development, such as stress or social deprivation can affect the various levels of neurotransmitters which, similar to the change that is known to occur in the hypothalamic-pituitary-adrenal axis, can alter emotional responses (Sullivan and
Dufresne 2006). Basically, hoards of research provide evidence that the developmental trajectory of a human, from pre-natal stages through adulthood, is influenced by external factors and that the nature and timing of these factors impacts adult mental health. The external input into the brain, and most importantly, emotional experiences have the ability to permanently alter brain systems to provide an efficient system for coping with one’s environment. The impact of emotional experiences on neonates and young children has been well documented, which has not been the case for older children and adolescence. It is necessary to study the impacts of social and emotional experience on the neural circuitry of this age group by first investigating the relevant vulnerable social moral circuitry in normal controls. In future attempts to correct for non-optimal social functioning, it is important to understand the impact that contextual influences have on development.
46
Social Constructs and Neural Correlates of Interest
To explore moral behavior, I wanted to investigate three essential components utilized by humans during social moral behavior, which have been mentioned sporadically throughout the introduction. These components are 1) Agency 2) Social/Moral Emotions
(SE) and 3) Moral judgments (MJ). In summary of the development discussed previously, agency is the precursor to ToM and is an early developed feature (around 1 yr) that allows humans to distinguish between self and other; it allows us to understand
‘intentions’ and thus makes us capable of holding ourselves and others responsible for their behavior. SE’s, central motive states often combined with cognition, are crucial for guiding moral behavior. MJ’s, which can be implicit or explicit/subconscious or conscious, are judgments regarding self and other’s behavior and how those behaviors align to one’s own goals/values. In relation to adult studies, these correlates of social moral behavior account for the main processes involved in the ‘social brain’ and hence, their development is most worthy of investigation.
A distributed cortico-limbic network that involves these social constructs is recruited regardless of stimuli presented (pictures, statements, narratives), or task requirements (passive viewing, active judgments) (Moll, de Oliveira-Souza et al. 2005).
The DLPFC, the OFC, posterior STS, anterior temporal lobes, insula, precuneus, ACC, and limbic regions are involved in moral cognition (Greene, Nystrom et al. 2004; Moll, de
Oliveira-Souza et al. 2005; Schaich Borg, Hynes et al. 2006). Prominent neuroscientist,
Jorge Moll (2005), describes the social moral emotion network as the OFC-STS network and that it is part of an event-feature-emotion complex (EFEC) framework (Figure 1-1).
47
Moll coined the EFEC framework because of the limitations of other non-integrative
theories. The EFEC framework is not restricted to the PFC, limbic regions, or any other
particular region, but highlights the integrative nature of diffuse areas of the brain
recruited for social moral processing. He proposes that this processing and behavior
depends on content- and context-dependent representations within this diffuse network.
With that said, Moll posits that social moral processing emerges from 1) contextual social
knowledge/event knowledge represented in the PFC (‘Event’), 2) social semantic
knowledge and social perception processed in the anterior and posterior temporal cortex
(‘Feature’), and 3) motivational (approach/avoidance) and basic emotional states
(‘Emotion’), which depend on cortical-limbic circuits. (Figures 1-1, 1-2).
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Similar and in support of Moll’s theory, Casebeer & Churchland (2003) posit that social
behavior seems to be rooted in the PFC and brainstem/limbic axis, with input from sensory and
48 multi-modal cortices. Derived from this network, he posits that the best functioning moral brain seems to be one that uses 1) multi-modal signals, 2) is conjoined with appropriately cued EF systems 3) shares rich connections with affective and cognitive brain structures 4) draws upon conditioned memories 5) and gains insight into the minds of others as to think about and actually behave in a manner enabling function as best it can.
To incorporate a general sequence of events in the adult frameworks outlined above, I included a social behavioral competence model formulated by Dodge (1986).
Dodge’s model consists of sequential steps that are executed when one makes a decision in a social situation. Other models, developed by neuroscientists, such as Moll (2005) and
Adolphs (2003) are in agreement with this model. For the most part, initially, there is an encoding process in which one selectively attends to and perceives stimuli. Next the value of the stimuli is interpreted as information concerning social cues (Agency processing would begin here), and previous associations and memories (SE processing would begin here) and rules and goals of the individual are computed and integrated (MJ would begin here). The individual then generates possible responses and event sequences, conducts a cost-benefit analysis, selects a response appropriate for the context, and executes that response. (For clarification of Dodge’s outlined steps relative to the current research, please see Figure 1-3 below). Considering the many steps that are involved in the social- decision making process, it is not surprising that it can be difficult to find a deficit responsible for an impairment in social-decision making. Although we have discussed an overall hierarchy of events above, it is to provide a basic understanding of the flow of events. One must be careful not to undermine the realization that the structures involved in these processes may have various functions, may participate in the overall process at
49 more than one time, and that these processes are multidirectional and recursive (Adolphs
2003).
Figure 1-3. Dodge’s sequential step model of social decision-making represented in an organizational chart with the social and emotional moral behaviors to be studied in the current research.
50
In summary, a cortico-limbic network integrates cultural and context-dependent knowledge, semantic social knowledge, and basic motivational states, encompassing the components of interest, agency, social emotions, and moral judgment. The following four chapters will describe the research I have conducted while investigating these constructs and their role in the processing of social/moral information and how this processing changes during the development of children and adolescents- the stage of life where the brain may be particularly sensitive to social experiences and provides the template for adult patterns of thinking*.
* The following research studies were conducted on the same developmental sample of children and adolescents. fMRI tests were first administered (Agency and Moral judgment tasks, followed by the Social Emotion task) followed by ‘out-of-magnet’ cognitive and emotion tests. ‘Out-of-magnet’ test scores for the sample are included in the Appendix.
51
Chapter 2
Agency
Humans are unique among species in the ability to transcend physical and biological constituents and developmentally embrace universal themes such as morality
(Haidt 2003; Sugarman 2005). In addition to judging our own and other’s behavior in various ways such as ‘right’ or ‘wrong’, humans possess the ability to judge our own as well as other’s intentions along similar dimensions that are related to norms, principles, and laws at both individual and societal levels. These cognitively-based attributions provide the basis for various social emotions such as praise and condemnation that significantly influence social behavior and interactions. An important dimension of such social cognition and social emotion is agency. Agency involves the way we come to understand ourselves as causes of actions and consequences that affect ourselves and others (Taylor 1985a; Roessler and Eilan 2003; Moll, de Oliveira-Souza et al. 2007).
Agency applies not only to the self but also to other persons within social networks, and develops from the realization that our actions and their consequences are a result of our will or intentions that affect and are affected by others and the recognition that others also possess this phenomenon. Considering its social implications, it is of no surprise that agency is a key construct in the development of morality (Moll, de Oliveira-Souza et al.
2007).
From a developmental perspective, agency is considered essential for the emergence of self, social knowledge, and adaptive social behavior and the first expressions are thought to emerge in humans at approximately one year of age (Spelke
1995; Johnson 2003). Children gradually elaborate their knowledge structures to
52 incorporate more abstract representations in self and interpersonal domains, focusing on the self and then extending the focus to others (Neisser 1991; Perner 1991; Flavell 1999;
Wellman 2001; Woodward 2001). In other words, as Piaget postulated, children start to distinguish between physical and mental, or concrete and abstract, and in relation to these distinctions, a shift from egocentrism, to ‘decentration’ begins to occur (Gibbs 2003).
One’s emotional life is also subject to this shift. At the age of two, children begin to talk about basic emotions, such as happiness, sadness, anger, and fear (Oatley and Jenkins
1992). Around this age, children begin to recognize their own basic feelings and thereafter begin to develop subcategories in which emotions become more complex. Parallel to this self-awareness, which is most sophisticated in human beings (Povinelli and Cant 1995), is the understanding that other persons also experience and display such emotions
(Humphrey 1990). The realization of other agents coincides with self-awareness and is based on subjective cognitive and affective experience (Frith and Frith 2003). The beginning of realizing others entities outside of the self, or the elaboration of agency, is the precursor for ToM, which is defined as the ability to attribute mental states to other people in order to predict their behavior (Frith and Frith 2003; Sodian and Thoermer
2008).
Coinciding with agency and of equal importance is another process pivotal to social and moral development known as causal knowledge. Without this knowledge, there would be no predictions of future outcomes, explanations of past events, acting in accordance to the present situation, and learning and categorizing novel events (Sobel and
Kushnir 2006). As experience with the dynamic external world continues, contextual knowledge increases, self and other interventions are understood, and conditional
53 probability emerges, all of which provide a powerful foundation for social learning (Pearl
2000; Meltzoff and Prinz 2002; Woodward 2003). This emergence allows for the rapid learning that is needed for persons to enforce or suppress responses in a dynamic context, and then to alter these responses accordingly for future interactions (Rolls 1999).
Conditional probability is essential to the social domain, because, unlike objects, self and others entail a vast repertoire of thoughts, emotions, attitudes, desires, beliefs, and intentions that require a convergent, flexible type of processing in order to distill and assimilate working concepts and knowledge of self and others.
By five or six years of age, ToM is typically established, as children are able to mentally represent other’s emotions and even predict the emotion that may occur in another (Oatley and Jenkins 1992). As these cognitive and emotional systems continue to develop, both toward self and others, there is increasingly shared representations that provide a basis for empathy, and particularly the self in relationship to others’ cognition and emotions (Eslinger 1998; Preston and de Waal 2002; Decety and Jackson 2004). The integration and distinction of self within social contexts gives rise not only to agency in a direct sense but also moral agency in relationship to the welfare of others or society as a whole (Decety and Chaminade 2003; Moll, de Oliveira-Souza et al. 2007). As the integration of self and other representation develops in young children, it occurs within a moral system that is primarily based on safety and harm to oneself and others (Nucci
1997). At approximately age ten, most children surpass the more basic safety/harm moral system influencing agency, and are developing an understanding of fairness as reciprocity.
When making moral judgments, this pre-adolescent age group typically views fairness in a way that is governed by the prevailing social rules and regulations dictated by surrounding
54 authority figures (Nucci 1997). Further development of the sense of fairness often includes empathy and compassion within broadening social circles and transition from a more external rule-based system to a more internally guided system, and from a more personal-focus to a more societal-focus. Not surprisingly, across cultural and ethnic groups, adolescents and young adults agree that prosocial or other-oriented thinking is an important indicator of moral maturity (Arnett 2003; Galambos, Barker et al. 2003;
Mayseless and Scharf 2003). Other-oriented thinking has been positively correlated with perspective-taking and empathy which have been shown behaviorally to continue to develop throughout adolescence (Selman 1980; Eisenberg and Miller 1987)(Eisenberg
1986; Kohlberg 1981, 1984, Selman 1980). This maturation is contingent on the development of understanding self and other as independent agents.
In summary, it is evident that a spectrum of self and other representations exists during the course of development. Agency seems to first originate as infants understand the self as its own entity and begin to experience subjective feelings. The self and other distinction becomes more clear and through social processes observed in humans, such as imitation (Tomasello and Call 1997). Children begin to understand that others have similar emotions and mental states to that of their own. Causal knowledge and conditional probability continues to reinforce this social learning. As agency of self and other is represented, intentionality is taken into account. ToM stems from agency and intentionality, and allows for empathy and perspective-taking, which continue to become more refined and sophisticated into adulthood. This development, beginning in infancy and continuing into adulthood, is essential for the highest forms of morality observed in humans, such as prosocial altruistic behaviors.
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The brain lesion and cognitive and affective neuroscience literature suggest that such shared representations and integration involves several brain systems that are recruited for aspects of social functioning, such as shared attention, perception of socially relevant actions, moral judgment, affective responses, recollection of social event knowledge, goal prioritization, and prediction of future events (Moll, de Oliveira-Souza et al. 2005). Based on brain lesion studies, development of social agency is most profoundly impaired when damage involves the prefrontal cortex (Eslinger, Flaherty-Craig et al.
2004). For example, the OFC is reported to be essential for the conditional probability and contingency-based learning that is necessary for the dynamics nature of social exchange
(Kringelbach and Rolls 2003). Cognitive neuroscience research suggests that specific neural regions are associated with moral judgment and social agency, including the PFC,
STS, and TPJ (Frith and Frith 2003; Moll, de Oliveira-Souza et al. 2007). The structures activated in adult research in what is termed the ‘theory of mind network’ as well as adult agency studies, include the mPFC, STS, TPJ, posterior cingulate cortex and anterior temporal poles (Abell, Krams et al. 1999; Gobbini, Koralek et al. 2007; Young, Cushman et al. 2007). However, these studies have been undertaken primarily in healthy adults and to our knowledge have not been directly investigated children. Furthermore, only two studies have indirectly investigated moral agency (Abell, Krams et al. 1999; Ohnishi,
Moriguchi et al. 2004; Decety, Michalska et al. 2008). These fMRI studies observed neural activations underlying empathy to physical pain and mentalizing, respectively.
Neither study explicitly investigated moral phenomena nor did they study developmental effects. Therefore, we sought to examine the typical neural systems that underlie the development and maturation of moral agency. Using fMRI, we designed the present study
56 to investigate this development in healthy children and adolescents 9-17 years of age.
Participants read and judged the actions in brief social-moral scripts as ‘right’ or ‘wrong’ while undergoing high field imaging. One-half of the scripts presented the actions as those of the participant (Moral Self-Agency) while the other half were the actions of others
(Moral Other-Agency). As mentioned, the child developmental behavioral data provides evidence that agency and related constructs, such as ToM, are established in early childhood and continue to be refined throughout adulthood. The adult neuroimaging literature indicates the neural substrates underlying these constructs are fully established and are heavily recruited for processing in social moral behaviors. The neural developmental process of these substrates throughout childhood and adolescents is not well understood. Based on the developmental brain lesion and adult cognitive neuroscience literature, we hypothesized that as children mature, dynamic neural activation patterns pertaining to the role of moral agency (self and other) would be observed. Furthermore, we hypothesized that the recruited structures comprising these patterns would include regions of the PFC, anterior temporal lobe and TPJ, all of which have been implicated as having a role in moral agency in adult lesion and neuroimaging studies (Green 2001; Bird, Castelli et al. 2004; Saxe, Carey et al. 2004; Fogassi, Ferrari et al. 2005).
Methods
Study Participants
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The fMRI protocol was conducted on 19 volunteer participants between the ages of 9-17 years (11 male, 8 female) who had no history of medical, neurological, or psychiatric illness, learning disability, or current medication usage. Along with fMRI scanning, participants were administered standardized tests of general intellect, academic achievement, executive functions, emotional and social intelligence in order to characterize several aspects of cognitive, emotional, and social development relevant to the experimental protocol (Wide Range Achievement Test 3 Oral Word Reading, Ravens
Colored Progressive Matrices (AB), Oldfield Handedness Questionnaire, Wechsler
Intelligence Scale for Children III Vocabulary and Block Design subtests, Controlled Oral
Word Association task, Wechsler Individual Achievement Test II Reading
Comprehension subtest, Chapman-Cook Speed of Reading test, the Home and
Community Social Behavior Scale, and Baron Emotional Intelligence Inventory: Youth
Version). All scores of participants demonstrated achievement within the normal range, with one exception on the Home and Community Social Behavior Scale, where this subject was at risk for social incompetence and antisocial behavior.
fMRI Study Procedures
Preparation and Positioning. The fMRI studies were carried out on a 3.0
Tesla MRI scanner. Stimuli were presented to participants through VisuaStim Digital
Glasses (Resonance Technology Inc., Northridge, CA) and responses were recorded through a handheld device. All subjects were first introduced to the tasks and response device in out-of-magnet training that included introduction and instruction slides as well
58 as sample trials of baseline and experimental stimuli on a laptop computer. Questions about the tasks and procedures were clarified with subjects until they fully understood the tasks for the fMRI session inside the magnet. Training was geared at alleviating any anxiety during the actual fMRI study and thoroughly familiarizing participants with the modes of stimulus presentation, task requirements, and response options. Instruction slides were repeated in-magnet and task readiness cues were presented through the 2-way intercom.
Participants laid supine in a head restrainer that minimized motion and provided precise positioning and comfort. A boxcar fMRI paradigm was used, which consisted of interleaved time intervals of baseline and cognitive activation. During fMRI scanning, participants were instructed to respond to visual stimulation by pressing either the left or right button with their respective thumb on a 2-button handheld device.
Image Acquisition. Functional MRI images were acquired on a whole-body 3 tesla imaging spectrometer (MedSpec S300, Bruker BioSpin Corporation, Ettlingen, Germany) with a TEM head coil for RF transmission and reception. A fast spin-echo sequence (TR /
TE = 4000 ms / 58.5 ms, flip angle = 90º, FOV = 23 " 23 cm2, 20 5-mm-thick axial slices with 1 mm distance between slices, acquisition matrix = 256 " 192, number of average =
1) and 3D gradient-echo sequence (TR / TE = 25 ms / 5 ms, flip angle = 15º, FOV = 23 "
23 " 13.5 cm3, acquisition matrix = 256 " 192 " 50, number of average = 1) were used to scan the whole brain, to exclude subjects with any potential neuroanatomic abnormalities.
Functional images were acquired with an echo planar imaging sequence (TR / TE = 3000 ms / 35 ms, flip angle = 90º, FOV = 23 " 23 cm2, 24 5-mm-thick axial slices with no gap
59 between slices, acquisition matrix = 64 " 64, number of average = 1). For the present study, 204 images were acquired during the alternating blocks of stimulation and baseline.
Cognitive Activation Task – Self and Other Agency. The boxcar design used for this task comprised of alternating experimental and baseline blocks (Please see
Figure 2-1 below for a representation of the paradigm design). There were 12 experimental blocks, 12 baseline blocks, and 4 rest periods. Experimental blocks were divided into 2 conditions: Moral Self-Agency and Moral Other-Agency, with six blocks representing each condition. Experimental block lasted 27 seconds, consisting of 3 statements, each presented for 6 seconds, with an additional 3 seconds per statement for the subject to respond using the two-button handheld device. Participants read the brief scripts and judged whether they believed the actions were right or wrong by pressing the right or left key, respectively (Please see Table 2-1 for stimuli examples). Scripts contained moral social situations that were formulated to be clearly “right” or “wrong” and validated on a small sample who were not recruited for fMRI study. The moral action in social situation was performed either by the participant (Self-Agency) or by another person and not at all involving the participant (Other-Agency). Baseline blocks each lasted 18 seconds and consisted of 2 statements each presented for 6 seconds with an additional 3 seconds for a right or wrong response. Baseline blocks were neutral statements that lacked a moral component but were either right or wrong and did not include persons. The rest periods were evenly dispersed throughout the paradigm and each lasted 18 seconds, allowing the blood-oxygen-level-dependent (BOLD) response to return to baseline after a series of stimulation blocks. Subjects viewed reminder
60 instructions windows before each task. The stimuli were all controlled for word length
(11-15), names used (short common female and male names), sentence structure, as well as presentation on screen (font, size, location). The timing and switching of visual stimuli were automatically controlled by transistor-to-transistor logic (TTL) signals incorporated in the pulse-timing program. The total in-magnet time for this paradigm was 10 minutes and 12 seconds.
Figure 2-1. The presented schematic is only to aid in understanding the block design used for the current experiment. All blocks are not presented here. The experimental blocks
(Moral Self-Agency and Moral Other-Agency) are interleaved with Baseline/Non-Moral blocks. Rest periods are evenly dispersed throughout the paradigm. Timings for all
Experimental blocks, all Non-Moral/Baseline blocks, and all Rest blocks are the same
(27s, 18s, and 18s, respectively).
61 Moral Category Example of Stimuli in fMRI Session Moral Right Moral Self-Agency I noticed that a classmate didn't have a lunch, so I offered him mine. Moral Other-Agency When Beth saw her classmate fall, she went over to help her up. Moral Wrong Moral Self-Agency Everyone else was picking on Toby, so I started picking on him, too. Moral Other-Agency Jill saw a handicapped person and made a joke about him. Baseline/Neutral Neutral Right On a clear and sunny day, the color of the sky is blue. Neutral Wrong In the game of basketball, a soccer ball is kicked back and forth.
Table 2-1. Examples of the Moral Self-Agency, Moral Other-Agency, and Baseline stimuli used for this study. The experimental tasks are listed on the left and one example of each corresponding stimulus presented on the right.
Data Analysis. The fMRI image data were processed with SPM2 software
(Wellcome Department of Cognitive Neurology, London, UK) implemented in Matlab
(Mathworks, Inc.). The first 4 images of each fMRI data set were discarded to remove the initial transit signal fluctuations and subsequent images were re-aligned within the session to remove any minor movements. The T1-weighted high-resolution anatomical images were co-registered with fMRI images and spatially normalized according to the Montreal
Neurological Institute brain template. The time-course images were normalized using the same normalization parameters and then smoothed with a 5 " 5 " 12.5 mm3 (full width at half maximum) Gaussian smoothing kernel. A statistic parametric map (SPM) was generated for each subject under each condition by fitting the stimulation paradigm to the functional data, convolved with a hemodynamic response function. The pixels representing the active regions were overlaid on the 3-D T1-weighted anatomic image in
Talairach coordinates. In this process, brain activation associated with nonmoral
62 judgments (baseline) task was contrasted to activation generated by the moral judgment
(experimental) task, isolating cognitive processes of moral judgment and agency within social moral contexts.
Group analysis was undertaken to generate average activation maps for the
Self-Agency and Other Agency conditions. In addition, these conditions were contrasted to identify unique activation components. Simple regressions between age and SPM2- derived z-scores were also computed in order to identify activation clusters that were positively and negatively correlated with age.
Results
Behavioral Results
Participants performed with a 98% agreement for both the moral (including the Moral Self-Agency and Moral Other-Agency conditions) and non-moral (Baseline condition) statements with no significant difference from the non-fMRI validation sample.
Hence, their judgments appeared typical. Mean average reaction/response times were
3820.92ms and 3786.48ms for Moral Right and Moral Wrong conditions, respectively, which did not differ significantly. However, mean average reaction/response time for
Other Agency judgments was slightly longer than for Self-Agency judgments (4037.25ms and 3570.15ms, respectively) (two-tailed t-test, p< 3.0 X 10-5).
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fMRI Results
Moral Self-Agency. When averaging across the Moral Right and Moral
Wrong statements that included the role of self-agency and removing baseline (Non-moral judgments) activation in a one-sample t-test (p<0.005, v>10), large medial and lateral clusters were identified. These regions included: mPFC, ACC, bilateral TPJ, right (R) anterior temporal pole, and medial precuneus/posterior cingulate (Please refer to Figure 2-
2 in which these activations are overlayed on axial slices and a 3D-rendered template image; Please refer to Table 2-2 for anatomical labeling, locality, and cluster size information). The activation cluster in the medial precuneus/posterior cingulate region was particularly prominent, closely followed by the mPFC.
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Figure 2-2. When averaging across the Moral Right and Moral Wrong statements that included the role of self-agency and subtracting out the baseline (Non-moral judgments) in a one-sample t-test (p<0.005, v>10), the following regions of activation were observed: medial frontal polar cortex (mPFC), anterior cingulate cortex (ACC), superior temporal sulcus (STS), bilateral temporal parietal junction (TPJ), Right anterior temporal pole (at pole), and medial precuneus/posterior cingulated (m precun/PCC). The activation cluster in the m precun/PCC region was particularly prominent, closely followed by the mPFC, areas involved in self-referential thinking and episodic memory
65 retrieval. The activated regions are commonly reported in adult studies investigating agency and mentalizing/ToM. A. Activations overlayed on a 3D-rendered template image. B. Activations overlayed on axial slices.
Moral Other-Agency. The average activation map (one-sample t-test
(p<0.005, v>10) for the Other-Agency condition statements in comparison to baseline revealed activation in the superior medial polar frontal cortex, bilateral anterior temporal poles, medial precuneus, and left (L) TPJ (Please refer to Figure 2-3 in which these activations are overlayed on axial slices and a 3D-rendered template image; Please refer to
Table 2-2 for anatomical labeling, locality, and cluster size information). Similar to the
Moral Self-Agency condition, there were prominent activation clusters in the medial precuneus and the mPFC.
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Figure 2-3. The average activation map (one-sample t-test, p<0.005, v>10), for the Other-Agency condition statements in comparison to baseline revealed activation in the superior medial polar frontal cortex (mPFC), bilateral anterior temporal poles (at pole), medial precuneus (m precun), and L temporal parietal junction (TPJ). Similar to the
Moral Self-Agency condition, there were prominent activation clusters in the m precun and the medial prefrontal cortex. As in the Moral Self-Agency task, these areas of activation have been demonstrated by adult studies to be recruited for agency and related constructs, such as mentalizing/ToM. A. Activations overlayed on a 3D-rendered template image. B. Activations overlayed on axial slices.
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Moral Self- and Other-Agency. The average activation maps of Self- and
Other-Agency mentioned described above are overlayed on a single 3D-rendered template image (Figure 2-4). The Moral Self-Agency activation map is presented in red, the Moral
Other-Agency in green, and areas common to both in yellow. Areas shared between tasks are the medial precuneus, L TPJ, R anterior temporal pole, and mPFC.
Figure 2-4. The average activation map of the Self-Agency (red) (one-sample t- test, p<0.005, v>10) and Other-Agency (green) (p<0.005, v>10) are overlayed on a 3D- rendered template image. Similar areas of activation between Self and Other Agency are represented in yellow. Shared activations include the L temporal parietal junction (TPJ), medial precuneus (m precun), and medial prefrontal cortex (mPFC). The R TPJ activation
68 is specific to the Moral Self-Agency condition. The mPFC and medial precuneus ativations are larger in the Moral Self-Agency condition and include the anterior cingulated and posterior cingulated, respectively. The L temporal pole (at pole) is activated in the Moral Other-Agency condition and not in the Moral Self-Agency condition. These activations suggest that although underlying neural networks are similar for self and other processing, distinctions exist.
Moral Self-Agency vs. Moral Other-Agency. Activations associated with
Moral Self-Agency and Moral Other-Agency were more specifically contrasted in a paired t-test (p<0.01, v >10). In this analysis, the Self-agency condition was found to recruit significantly greater activity in the R DLPFC (Please refer to Figure 2-5 in which the paired t-test results are overlayed on a 3D-rendered image and are colored red; Please refer to Table 2-2 for anatomical labeling, locality, and cluster size information).
Moral Other-Agency vs. Moral Self-Agency. The contrast of Moral Other-
Agency to Moral Self-Agency (p<0.01, v >10) revealed small activations in the L cerebellum, and parieto-occipital junction.(Please refer to Figure 2-5 in which the results of the paired t-test are overlayed on a 3D-rendered template image and are colored green;
Please refer to Table 2-2 for anatomical labeling, locality, and cluster size information).
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Figure 2-5. Activations associated with Moral Self-Agency and Moral Other-
Agency were more specifically contrasted in a paired t-test (p<0.01, v >10). In this analysis, the self-agency condition was found to recruit significantly greater activity in the
R dorsal lateral prefrontal cortex (DLPFC). The contrast of Moral Other-Agency to Moral
Self-Agency (p<0.01, v >10) revealed small activations in the L cerebellum, and parietal- occipital junction (POJ).
Age Regression Analyses. After conducting positive and negative age regression analyses (p<0.05, v >10), we found no areas of significant increasing activity in Moral Self-Agency and Moral Other-Agency conditions as children and adolescents age. However, several significant negative correlations (i.e., decreasing
70 activity with age) were evident in the Moral Self and Other Agency condition. These areas of decreasing activity with age included diffuse areas in the inferior parietal, insula, medial cerebellum, limbic and paralimbic, and inferior temporal. At a more stringent p- value (p<0.01), medial precuneus/cuneus and parieto-occipital junction activations were observed in the Self-Agency condition, and ventral tegmental area (VTA)/midbrain (MB) activation was observed in the Other-Agency condition (Please refer to Table 2-2 for anatomical labeling, locality, and cluster size information).
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Table 2-2. Average activation map, paired t-tests, and Age Regression Analyses localizations for the Self-Agency and Other-Agency conditions are displayed. MNI coordinates, voxel sizes (k), t-values, and Brodmann areas (BA) are reported. P-values are for each condition are specified and listed to the right of the respective condition.
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Temporal parietal junction (TPJ), superior temporal sulcus (STS), medial prefrontal cortex
(mPFC), dorsal lateral prefrontal cortex (DLPFC), midbrain (MB), ventral tegmental area
(VTA).
Discussion
The objective of this study was to investigate the neural substrates associated with agency in the moral judgments of children and adolescents and how these neural substrates were influenced by age in our 9-17 year old healthy sample. The main hypothesis was that regions of the PFC, anterior temporal pole, and TPJ activation would be observed in the average activation maps in Moral Self-Agency and Moral Other-
Agency and that these activations would be dynamic with maturation. To test these hypotheses, we specifically contrasted Moral Self-Agency and Moral Other-Agency in scripts that were balanced for right vs. wrong moral actions, placing participants’ intentions and causal actions of self towards others in comparison with the intentions and causal actions of others towards others and analyzed how these contrasts were correlated with increasing age. The results yielded neural activation patterns that not only were clearly identifiable, but also consistent with several regions that have been reported in healthy adult samples.
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Moral Self-Agency and Moral Other-Agency in Children and Adolescents
Children and adolescents activated a similar network to what has been reported in adult studies, including the mPFC, anterior temporal poles, TPJ, and the medial precuneus while undertaking moral judgments with self- and other-agency influences. Association of the mPFC and the medial parietal areas in moral agency (self vs. other) has been well documented in adult fMRI and lesion studies (Craik 1999;
Kircher, Senior et al. 2000; Kircher, Senior et al. 2001; Johnson 2002; Kelley, Macrae et al. 2002; Decety and Chaminade 2003; Decety and Jackson 2004; Greene, Nystrom et al.
2004; Seger, Stone et al. 2004; Jackson 2005). Several of the regions jointly activated in the Self and Other-Agency conditions are proposed by Damasio (1999) to be involved in higher order cognitive processing of self and others. He suggested that self-awareness or self-consciousness encompasses three dimensions (protoself, core self, and autobiographical self) that provide the agent with information to interact with the external environment and to simulate mental and intentional states of others (Seger, Stone et al.
2004). This simulation has become known as ‘simulation theory’, referred to by some as
‘simulation ToM’, and posits that individuals understand others by simulating how another would feel and/or act (Gallup 1982; Harris 1989; Taylor, Esbensen et al. 1994).
Within this framework of ToM, the similar activation patterns observed between the
Moral Self and Other-Agency conditions can be explained (Meltzoff 2001; Decety and
Chaminade 2003; Seger, Stone et al. 2004). The protoself represents the current state of the agent and is supported by non-conscious neural systems such as the medial parietal
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(precuneus) and somatosensory areas. The core self is the conscious representation of what is currently involving the agent, which includes mental representations of self and others, subserved by the medial prefrontal cortices (Frith and Frith 1999). Lastly, the autobiographical self is associated with the temporal areas for the purpose of retrieving past experiences of the agent to represent in the core self. The cohesion of these dimensions of self that is purportedly needed for normal social interaction is supported by the finding that the medial prefrontal cortex, along with lateral temporal, including the
TPJ, and medial parietal regions, have been linked to episodic memory and event sequence knowledge (Calabrese 1996; Breen, Caine et al. 2001). (Event sequence knowledge is defined as the representation(s) comprised of memories, causalities, and rules that are in temporal order and are needed for advantageous social decision-making and interpersonal exchanges (Moll, de Oliveira-Souza et al. 2005)). The self-dimensions, as proposed by Damasio, are essential for the simulation of others. Although ‘simulation theory’ is the most discussed explanation for ToM in the current literature, ‘theory theory’ is an alternative explanation that is given by many researchers (Churchland 1991).
‘Theory theory’, better known as ‘folk psychology,’ posits that humans develop a framework of rules and laws that they use to successfully navigate through every day life
(Kraml 2002). This framework, or theory, is acquired as one interacts with the external world, placing a strong emphasis on contextual, conditional, and contingency-based learning. Via this experience-based learning, humans can understand, predict, and explain the world and ‘other’ behavior. Based on the theories explaining ToM discussed here, it seems that two important themes are highlighted in ToM- an empathic element, highlighted more so in the ‘simulation theory’, and a cognitive element, highlighted more
75 in the ‘theory theory’. In relation to the social moral literature, and the highly agreed upon contributing roles of affective and cognitive processing to social moral networks, it would be plausible that both theories are involved and together constitute ToM, indicated by the current research. In social moral processing, moral agency involves perceiving and evaluating socially meaningful stimuli and the associated intentions for the purpose of predicting the following actions and responses of both you and the other person involved.
Doing this requires knowledge concerning conditional probabilities and memories of past experience, both which require a framework of concepts based on the outside world and personal relevance and experience in which to understand. Underlying activations observed in the current research indicate that these processes are ongoing. In addition to these theoretical accounts, previous research demonstrates that intentional/mental causality vs. physical causality, similar to the abstract vs. concrete dichotomy outlined by
Piaget (1968), activates the majority of the regions recruited in the present study (Fletcher,
Happe et al. 1995). In summary, the regions discussed are consistently active in mentalizing/ToM tasks (Brunet, Sarfati et al. 2000; Saxe and Kanwisher 2003; Saxe and
Wexler 2005; Gobbini, Koralek et al. 2007), and involve a self-based simulation and an externally-based conceptual framework. These regions will be given a further functional description below.
The mPFC region has been associated with moral judgment and social agency impairments in child and adult frontal lesion studies (Eslinger and Damasio 1985;
Dimitrov 1999; Eslinger, Flaherty-Craig et al. 2004), social and moral judgments in functional brain imaging studies of healthy adults (Bird, Castelli et al. 2004; Greene,
Nystrom et al. 2004; Ochsner, Knierim et al. 2004; Moll, de Oliveira-Souza et al. 2007),
76 and agency-related constructs, such as ToM, empathy, and self-regulation of behavior
(Damasio 1994; Farrow, Zheng et al. 2001; Moll, de Oliveira-Souza et al. 2002; Decety and Jackson 2004; Ruby and Decety 2004; Seitz, Nickel et al. 2006). For example,
Shamay-Tsoory et al. (2005) demonstrated in a PET study that higher metabolic values in the mPFC were positively correlated with empathy scores as evaluated by neuropsychologists. The TPJ is recruited for several of the functions designated to the mPFC, most likely because of its computational role in converging social information, attention to salient stimuli, and social perception of self and others (Decety and Lamm
2007). When taking into account the various functions of the TPJ and the integrative role of this region, it is not surprising that its involvement has been demonstrated in belief attributions associated with ToM tasks (Goel, Grafman et al. 1995; Saxe 2006). Research also supports temporal pole function in ToM tasks (Gallagher and Frith 2003) and in other functions such as semantic feature knowledge representation (Zahn, Moll et al. 2007) and in the convergence of interceptive and exteroceptive processing streams (Moran, Mufson et al. 1987; Gloor 1997)(Gloor 1997; Moran et al., 1987). Moreover, temporal pole damage has been shown to result in severe changes in social behavior (Miller 1999). For example, Kling & Steklis (1967) demonstrated that temporal pole lesions in monkeys caused social isolation and a significant reduction in affiliative behaviors that was so debilitating that when the monkeys were released to their natural habitat, they died. In essence, the overlapping activated regions across the Moral Self and Moral Other-Agency conditions have also been found to be involved in agency, self-awareness, ToM and related constructs, such as detecting and representing intentionality and goal-directed behaviors, and belief attribution needed for social moral judgments and decision-making.
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For the most part, similar activation patterns were observed between the
Moral Self and Other-Agency conditions. However, there were some minor differences that should be highlighted. Although, both conditions recruited the mPFC, the Moral Self
Agency condition recruited a significantly larger cluster that included more polar PFC and a portion of the ACC. This extended activation may be due to a higher degree of reflection and representation of mental states both of self and other due to the more personal direct element of the Moral Self-Agency condition (Lane, Fink et al. 1997;
Gallagher, Happe et al. 2000; Gusnard, Akbudak et al. 2001; McCabe, Houser et al. 2001;
Frith and Frith 2003; Mitchell, Banaji et al. 2005). This increase in personal salience most likely includes an affective component. Research conducted by Greene et al. (2004) support this explanation as they have found the mPFC to be significantly involved in attending to subjective emotional states and recruited more robustly in more personal, compared to impersonal, social moral situations. Additionally, the Moral Self-Agency condition recruited R TPJ and posterior cingulate which was not observed in the Other-
Agency average activation map. Like the mPFC, these areas, have been indicated to be involved in ToM tasks. In particular, the R TPJ, has been reported to be the most significantly activated region in belief attribution, when compared to other areas consistently activated in ToM tasks (Saxe 2006). Several studies have demonstrated the right parietal cortex to be predominantly involved in egocentric reference frames (Vogeley and Fink 2003). In further support of these studies, anosognosia, a neurogical disorder characterized by lack of awareness or denial of an illness or paralysis on one side of the body, is thought to follow right parietal lobe lesions (Ramachandran 1995). The STS, adjacent to the TPJ, was included in the large R TPJ activation. Although similar
78 functions have been assigned to the region involving the TPJ and STS, there seems to be functional specializations, such that the TPJ specializes in belief attribution, and the STS specializes in representing goal-directed action (Saxe, Carey et al. 2004). These activations can be attributed to the higher degree of engagement, in what can be assumed to be related to self-awareness and ToM related constructs, required for the individual in the Self-Agency task. The additional activation observed in the Self-Agency condition can not be attributed to a more difficult decision-making process, but as proposed, greater engagement, emotional involvement, and possibly simulation with others during judgment. The reason for this claim is that there was a significantly longer response time for the “other” statements in the Other-Agency condition, suggesting if anything, a more automatic or ‘easier’ decision was made in the Self-Agency condition. One must remember that although these individuals were directly involved in that they were the agent, it was in the context of a social interaction where ToM would most likely be utilized to understand the belief and/or intentions of the interacting “other,” explaining the more robust recruitment of these regions. The only additional activation recruited by the
Other Agency task was the L anterior temporal pole, which may account for the greater reliance on social concepts and rules (Zahn, Moll et al. 2007) when judging others, whereas decisions concerning the self may include more circumstantial, external considerations when judging behavior (Pronin 2008).
When we specifically contrasted Moral Self-Agency with the Moral Other-
Agency condition, we discovered that Moral Self-Agency recruited significantly greater R
DLPFC activity. In adults, activity in this region has been associated with both self- awareness and social cognition and has been shown to be more activated when attention is
79 directed at the self rather than at others (Schmitz, Kawahara-Baccus et al. 2004).
Moreover, the higher demand for self engagement in the Self Agency task and the more robust activation in self-awareness and ToM related regions compared to the Other-
Agency condition possibly indicates a greater working memory load as more social concepts and features are represented as they are needed for decision-making. This additional recruitment may be due to a higher degree of attention or salience involved when the agent is directly engaged in the scenario, or as mentioned in the previous paragraph, more components are considered when judging the self whereas others judging others may be a more rule-based approach. When comparing Moral Other-Agency to
Moral Self-Agency, L parietal-occipital and L cerebellum activations were identified. The
L parietal-occipital region is an associative area important for integrating perceptual knowledge, suggesting that this region may be involved in observing/imagining external social interaction needed for downstream decision-making. Although, Ohnishi et al.
(2004) found left cerebellar activity in a mentalizing task in children, it is unclear as to why it was significantly more activated in the Moral Other-Agency compared to the Moral
Self-Agency condition. Perhaps, there are partially separate networks subserving mentalizing for self and other. An interesting explanation for these differences, is that
‘theory theory’ and ‘simulation theory’ could be associated with partially dissociable networks, with each theory differing in its internal and external bases and make-up of cognitive and affective components. Further investigations will have to be conducted to further analyze these differences.
80
Moral Agency Development
In light of the findings and their consistency with neural activation patterns observed in adults, the present study showed no areas of increasing activity with age.
There were minor decreases in activation as children aged in the medial precuneus and parietal-occipital cortices in the Self-Agency condition and the VTA in the Other-Agency condition. These reductions might indicate more focal and consolidated activation patterns, and possibly less affective input to guide decision-making, as rules are internalized and relied upon more heavily, and as children and adolescents age. For the most part, results suggest that the necessary neural systems for distinguishing self and others and for incorporating these distinctions into simple rule-based moral judgments are established by nine years of age, the youngest age in this study, and continue to be recruited throughout childhood and adolescence.
Although the findings are in agreement with the behavioral literature that indicate children five to six years of age can recognize, mentally represent, predict, and empathize with the emotions and behaviors of others (Oatley and Jenkins 1992), studies indicate a spectrum of agency-related developments, such as perspective-taking, socialization, empathy, and compassion that continue to develop into adulthood. Due to the simple nature of the stimuli used for the present tasks, the agency-related developments in the childhood and adolescent years may not have been fully observed.
Future studies are needed to investigate additional agency-related neural developments
81 that were not identified in the present study. Furthermore, as suggested, the separate theories explaining ToM, ‘simulation theory’ and ‘theory theory’, may not be in conflict, but may work synergistically to represent and predict the beliefs and intentions of other.
The underlying activations of these theories may be partially dissociable and may have different developmental trajectories. Future studies will need to be conducted to further investigate these claims.
Summary and Conclusion
In summary, fMRI analysis indicated that in the course of typical childhood to adolescent development, the neural networks subserving agency in moral judgments of self and other are strikingly similar and are in agreement with previous self- awareness and ToM research. The primary brain regions belonging to these networks are the medial prefrontal cortex and medial parietal cortices, anterior temporal lobes, and temporo-parietal junction regions. In agreement with previous research, our findings indicate that this neural network is reliably recruited for self and other social processing and decision-making, including intentional causality, reading intentions and mental states, attributing beliefs, and retrieving task-relevant information that remains robust and stable throughout childhood and adolescent development and extends into adulthood. Most importantly, it is a critical neural foundation for adaptive social maturity.
82
Chapter 3
Moral Judgments
Moral judgments (MJ), are defined as the capacity to make decisions and judgments based on internal principles and to act in accordance with such judgments
(Kholberg 1964). From a developmental perspective, these MJ’s form a basis for what psychologist and developmentalist Lawrence Kohlberg declares as ‘MJ competence’
(Kholberg 1964). This competence encompasses the rules, concepts, and values that are acquired and internalized throughout maturation. MJ’s are of great interest because of their utility in guiding decisions and subsequent actions. As humans transcend the immature states of development in early childhood, these moral judgments are not only purposeful in guiding self behavior but are influenced by social consensus (Newburg
2006) and extend to others and society as a whole (Flavell, Miller et al. 1993). Because of the societal and cultural value of MJ’s, they have been of interest to humans for thousands of years and provide the foundation for complex social structures and systems such as economics, culture, law, and government (Eslinger, Robinson-Long et al. 2009).
Capabilities that are especially developed in humans, such as ToM, mental imagery, affective and cognitive communication, abstract beliefs and values, expectations, and attribution, have likely contributed to the complex uniquely human processes, such as
MJ’s. MJ is an essential prelude to moral behavior and plays a key role in guiding those behaviors (Nucci 1997). When one is involved in a social moral situation, and many times when one is an observer, a moral behavior, whether it be overt, inert, or
83 abandoned, is the aftermath of MJ (s) that are made in regards to the myriad of situational, personal, and interpersonal factors that face the judge.
Social moral interactions and behavior encapsulates the majority of our lives as humans and is the cause of the greater amount of our joys and sufferings endured as individuals and as a society (Haidt 2003). A major component of social cognition and behavior among humans is our incessant judging of social behavior, whether of the self or others (Brothers 2002). We most likely engage these MJ’s several times if not hundreds of times each day whether these judgments are made in real-time or in an imagined scenario, or towards people we know well, do not know well, or perhaps, will never meet. We are able to do this because of the complex interplay of cognitive and affective systems and the highly processed social and emotional information that is shared between them (Eisenberg 1995; Fletcher, Happe et al. 1995; Frith and Frith 1999;
Damasio, Grabowski et al. 2000). When these systems do not work properly, whether from traumatic brain injury, neurotransmitter imbalances, congenital malformation, disease, or experimental manipulations, social and moral behaviors are known to dramatically change, and in some cases, can be harmful to the individual and/or others.
Interestingly, several of the key structures that demonstrate abnormal activation in these systems are often found to be abnormal in individuals who fail to comply with moral guidelines and engage in antisocial and rule-breaking behavior, activities that are central to criminal, violent and psychopathic individuals (Raine and Yang 2006).
Although researchers are aware of the behavioral manifestations of cognitive and affective systems involved in moral development, minimal research has been conducted on the underlying neural substrates subserving this development. Only in the past
84 decade, have adult studies been conducted on the neural substrates underlying cognition and emotion involved in moral judgments (Moll, Eslinger et al. 2001; Moll, de Oliveira-
Souza et al. 2002; Greene, Nystrom et al. 2004; Moll, de Oliveira-Souza et al. 2005;
Moll, de Oliveira-Souza et al. 2007; Zahn, Moll et al. 2007). To our knowledge, no studies have directly investigated these substrates in children. Thus, the adult studies may provide an important foundation for investigating child moral development in that they will most likely be indicative of the neural systems involved in moral cognition, emotion, and motivation.
Moral development consists of a number of components and processes, including the accumulation of event sequence knowledge and motivational and emotional systems and the development of perception of social situations (Moll, de Oliveira-Souza et al.
2005). It is these systems that integrate information from external and internal sources to allow for moral perceptions, judgments, emotions, and behaviors. Event sequence knowledge can be described as representation(s) comprised of memories, causalities, and rules that are in temporal order and are needed for advantageous social decision-making and interpersonal exchanges (Moll, de Oliveira-Souza et al. 2005). Adult neuroimaging studies and brain lesion data indicate that this sequential knowledge essential for dynamic social contexts is represented in prefrontal and lateral temporal regions, such as the anterior temporal poles, OFC, mPFC, and the DLPFC (Moll, de Oliveira-Souza et al.
2002; Moll, de Oliveira-Souza et al. 2005; Zahn, Moll et al. 2007). Other studies demonstrate that the posterior temporal and parietal areas, such as the STS and TPJ, are involved in social perception. These areas are commonly recruited for belief attribution and goal-oriented and intentional actions during interpersonal situations (Saxe 2006). In
85 addition to event sequence knowledge and social perception, motivational and emotional processing are often highly involved in social moral processing. Limbic and paralimbic regions, such as the amygdala, hippocampus, insula, and ACC are frequently observed to subserve this processing (Davidson, Jackson et al. 2000; Greene, Nystrom et al. 2004).
In summary, the integrative neural substrates/systems involved in morality, often referred to as the ‘social brain,’ are posterior temporal and parietal cortices (implicated in perception), PFC and anterior temporal cortices (implicated in event sequence knowledge), and limbic and paralimbic systems (implicated in motivation and emotions)
(Moll, de Oliveira-Souza et al. 2005). It is these systems that are of high interest as we investigate moral development in children.
The PFC is of particular interest in this investigation because of its prolonged development throughout adolescence (Sowell, Peterson et al. 2003; Gogtay, Giedd et al.
2004). This region is known to undergo extensive reorganization during this period of life and works to establish neuronal networks that are capable of mediating increasingly complex adult level social interactions (Anderson, Anderson et al. 2001). This association cortex is crucial for the executive functions which direct attention to significant stimuli, select context-appropriate responses, and execute behavior. Several fMRI and lesion data provide evidence that social behaviors subserving moral judgments and behavior, such as cooperation, reciprocity, ToM, goal-directed behavior, understanding others, and prospective thinking are functions involving the PFC (Ackerly and Benton 1948; Eslinger and Damasio 1985; Price, Daffner et al. 1990; Mateer 1991;
Eslinger, Grattan et al. 1992; Grattan and Eslinger 1992; Marlowe 1992; Baron-Cohen,
86 Tager-Flusberg et al. 1993; Anderson, Bechara et al. 1999; Eslinger, Flaherty-Craig et al.
2004; Anderson, Barrash et al. 2006).
To date, the PFC lesion data has provided us with the majority of what we know about the PFC. Numerous cases provide compelling evidence that deficits emerge from the altercations in the acquisition and elaboration of social and moral conceptual knowledge and the ability to manipulate this knowledge to coincide with dynamic social- moral contexts. Practically speaking, these deficits typically yield behaviors and mental states observed in more primitive social species and human infants, such as impulsivity, inability to efficiently adapt to new or changing contexts, difficulty in interpersonal relationships, reduction in experiencing selective emotions, such as empathy, and primarily engaging in a hedonic, self-centered frame of thinking. Although these lesion studies are foundational to the current research and provide validity for structure location and function, they have their limitations. These limitations include a lack of a holistic approach to the brain, few children and adolescent lesion cases, and minimal developmental implications. The current research will give a window into neural maturation in children and adolescents, and will yield neural patterns of activations indicative of holistic brain function underlying moral judgment processing.
Our aim is to investigate moral judgment development in children, because of its key role in moral-decision making and guiding moral behavior (Nucci 1997). Using fMRI, we are interested in investigating the interplay of cognitive and affective components involved in this development in healthy children and adolescents 9-17 years of age. While undertaking fMRI study, participants will view multiple sentence vignettes designed to recruit neural underpinnings of moral certainty (sentences that are clearly
87 ‘right’ or ‘wrong’)* and moral ambiguous (sentences that are not clearly ‘right’ or
‘wrong’) judgments. Due to the behavioral developmental data indicating that moral judgments and reasoning mature with age as do the multiple components contributing to these developments, such as empathy, perspective-taking, and social knowledge, we suspected underlying neural substrates to parallel these developments. Structural evidence of PFC development in addition to the adult neuroimaging data supporting the pivotal role of the PFC in the processing and integration of cognitive and affective streams essential for moral behavior led us to our first hypothesis. We hypothesized regions of the PFC to become more active as children and adolescents mature in their acquisition, internalization, and representation of social and moral rules and values. As mentioned, the PFC is able to integrate and represent multiple processing streams, which is a capability crucial for moral behavior. During PFC development, innervations to this region and the establishment and refinement of involved networks yield the most mature behaviors observed in adults, such as moral maturity. Because of these networks associated with the PFC, we also hypothesized, based on child and adult lesion studies and adult neuroimaging data, that the anterior temporal, temporal-parietal junction, and amygdala would also display dynamic activation patterns as a function of age.
Methods
Study Participants
88 The sample was comprised of 19 volunteers between the ages of 9-17 years (8 male, 11 female) who had no history of medical, neurological or psychiatric illness, learning disability, or current medication usage. Participants were administered standardized tests of general intellect, academic achievement and executive functions, and completed inventories of emotional intelligence and social behavior in order to characterize several aspects of cognitive, emotional, and social development relevant to the experimental protocol. Administered tests were as follows: Wide Range Achievement
Test 3 Oral Word Reading, Ravens Colored Progressive Matrices (AB), Oldfield
Handedness Questionnaire, Wechsler Intelligence Scale for Children III Vocabulary and
Block Design subtests, Controlled Oral Word Association task, Wechsler Individual
Achievement Test II Reading Comprehension subtest, Chapman-Cook Speed of Reading test, the Home and Community Social Behavior Scale, and Baron Emotional Intelligence
Inventory: Youth Version. All measures indicated development and achievement within the normal range, with one exception on the Home and Community social behavior scale, where a subject was scored “at risk” for social incompetence and antisocial behavior.
fMRI Study Procedures
Preparation and Positioning. The fMRI studies were conducted on a 3.0
T MRI scanner. Stimuli were presented to participants through VisuaStim Digital
Glasses (Resonance Technology Inc., Northridge, CA) and responses were recorded through a handheld device. All subjects were first introduced to the tasks and response device in out-of-magnet training that included introduction and instruction slides as well
89 as sample trials of baseline and experimental stimuli on a laptop computer. Questions about the tasks and procedures were clarified with subjects until they fully understood the tasks for the fMRI session. Training was geared at alleviating any anxiety during the actual fMRI study and thoroughly familiarizing participants with the modes of stimulus presentation, task requirements, and response options. Instruction slides were repeated in-magnet and task readiness cues were presented through the 2-way intercom.
Participants laid supine in a head restrainer that minimized motion and provided precise positioning and comfort. A boxcar fMRI paradigm was used, which consisted of interleaved time intervals of baseline and cognitive activation. During fMRI scanning, participants were instructed to respond to visual stimulation by pressing either the left or right button with their respective thumb on a 2-button handheld device.
Image Acquisition. Functional MRI images were acquired on a whole- body 3 tesla imaging spectrometer (MedSpec S300, Bruker BioSpin Corporation,
Ettlingen, Germany) with a TEM head coil for RF transmission and reception. A fast spin-echo sequence (TR / TE = 4000 ms / 58.5 ms, flip angle = 90º, FOV = 23 ! 23 cm2,
20 5-mm-thick axial slices with 1 mm distance between slices, acquisition matrix = 256 !
192, number of average = 1) and 3D gradient-echo sequence (TR / TE = 25 ms / 5 ms, flip angle = 15º, FOV = 23 ! 23 ! 13.5 cm3, acquisition matrix = 256 ! 192 ! 50, number of average = 1) were used to scan the whole brain, to exclude subjects with any potential neuroanatomic abnormalities. Functional images were acquired with an echo planar imaging sequence (TR / TE = 3000 ms / 35 ms, flip angle = 90º, FOV = 23 ! 23 cm2, 24
5-mm-thick axial slices with no gap between slices, acquisition matrix = 64 ! 64, number
90 of average = 1). Two study paradigms were administered in each participant session. For this paradigm, 259 images were acquired during the alternating blocks of stimulation and baseline.
Cognitive Activation Task – Moral Judgment. The boxcar design used for this task was comprised of alternating experimental and baseline blocks (See Figure 3-1).
There were 15 experimental blocks, 15 baseline blocks, and 5 rest periods. Experimental blocks were divided equally into 2 conditions: Moral Right and Wrong (12 blocks), and
Ambiguous (3 blocks). Each block lasted 27 seconds, consisting of 3 statements presented for 6 seconds with an additional 3 seconds per statement for the subject to respond using the two-button handheld device. The subject was asked to judge whether they believed the statement was right or wrong by pressing either the right or left key respectively. The experimental statements contained moral social situations. The moral right and wrong conditions contained statements that were rule-based, having a definite right or wrong response (See Table 3-1 for examples). In the ambiguous condition, the moral scenario was ambiguous and more difficult to decipher a clear right and wrong answer. The baseline blocks each lasted 18 seconds and consisted of 2 statements each presented for 6 seconds with an additional 3 seconds for a right or wrong response.
Baseline blocks were neutral statements that lacked a moral component but were either right or wrong. The rest periods were evenly dispersed throughout the paradigm and each lasted 18 seconds, allowing the BOLD response to return to baseline after a series of stimulation blocks. Subjects viewed reminder instruction windows before each task. The stimuli were all controlled for word length (11-15), names used (short common female
91 and male names), sentence structure, as well as presentation on screen (font, size, location). The timing and switching of visual stimuli were automatically controlled by
TTL signals incorporated in the pulse-timing program. The total in-magnet time for this paradigm was 12 minutes 57 seconds.
Figure 3-1. The presented schematic is only to aid in understanding the block design used for the current experiment. All blocks are not presented here. The experimental blocks (Rule-Based and Ambiguous) are interleaved with Baseline/Non-Moral blocks.
Rest periods are evenly dispersed throughout the paradigm.
92
Moral Category Example of Stimuli in fMRI Session
Moral Right At recess, I saw a classmate playing alone so I went to play with him.
Moral Wrong Everyone else was picking on Toby, so I started picking on him, too.
Ambiguous When my very overweight friend asked if she was fat I said “no.”
Neutral Right On a clear and sunny day, the color of the sky is blue.
Neutral Wrong In the game of basketball, a soccer ball is kicked back and forth.
Table 3-1. Examples of the moral stimuli used for this study. The experimental tasks are
listed on the left and one example of each corresponding stimulus is presented on the
right.
Data Analysis. The fMRI image data were processed with SPM2 software
(Wellcome Department of Cognitive Neurology, London, UK) implemented in Matlab
(Mathworks, Inc.). The first 4 images of each fMRI data set were discarded to remove
the initial transit signal fluctuations and subsequent images were re-aligned within the
session to remove any minor movements. The T1-weighted high-resolution anatomical
images were co-registered with fMRI images and spatially normalized according to the
Montreal Neurological Institute brain template. The time-course images were normalized
using the same normalization parameters and then smoothed with a 5 ! 5 ! 12.5 mm3
(full width at half maximum) Gaussian smoothing kernel. A SPM map was generated for
93 each subject under each condition by fitting the stimulation paradigm to the functional data, convolved with a hemodynamic response function. The pixels representing the active regions were overlaid on the 3-D T1-weighted anatomic image in Talairach coordinates. In this process, brain activations generated by the moral judgment
(experimental) task were contrasted with the nonmoral judgment (baseline) task, isolating cognitive processes of morality and the related judgments made in social moral contexts..
Group analysis was undertaken to generate average activation maps for the overall MJ as well as the Ambiguous and Rule-based conditions. Simple regressions between age and SPM2-derived z-scores were then computed in order to identify areas of positive and negative correlation with age. Although we aimed to set the p-value threshold at 0.001, we thought it necessary to adjust the p-value appropriately to observe significant activations. For this reason, more /less stringent thresholds were applied and are noted and labeled accordingly.
Results
Behavioral Results
Subjects performed similarly both in-magnet and on out-of-magnet ratings of the same stimuli, with an average accuracy (based on agreement with the way the stimuli were designed to be interpreted and a non-study control group) of 100% for
Nonmoral statements, 98% for Rule-Based statements, and 49% for Ambiguous
94 statements (this latter finding was expected due to the high degree of variability in responses to the Ambiguous moral statements). Out-of-magnet ratings included a 5-
Likert scale, requiring the participants to rate the moral content of each stimulus/statement. Moral content was rated significantly different for Moral
(Ambiguous and Rule-Based) and Nonmoral statements, with average ratings of 3.35 and
0.39 for Moral and Nonmoral stimuli/statements, respectively. The mean reaction/response times averaged across subjects were 4069.27ms, 4117.11ms, and
5380.01ms for Nonmoral/Baseline, Rule-Based, and Ambiguous stimuli, respectively.
As expected, the Ambiguous condition mean reaction/response time was significantly higher (p<3.26 ! 10-6, two-tailed t- test) than the Rule-Based mean reaction/response times, due to the ambiguity and moral reasoning involved. Also as expected, the All
Moral (Ambiguous and Rule-Based statements) responses were significantly longer than the Nonmoral/Baseline responses (p<0.005).
fMRI Results
All Moral Activation. When averaging across all of the moral activation tasks (Rule-Based, and Ambiguous) and comparing to baseline (Nonmoral judgments) in a one-sample t-test (Family-wise-error (FEW) p<0.05, v>10), the following regions of activation were observed: L Anterior Temporal Pole, L lateral OFC (LOFC),
Precuneus/Posterior Cingulate, L STS, L TPJ, mPFC, and superior mPFC. When relaxing the threshold to p<0.001 (uncorrected), bilateral activation occurs in the areas mentioned above as well as additional activation in the supplementary motor cortex, the
95 ACC, mid cingulate and bilateral inferior/occipital cortices. These average activation results are summarized in Figures 3-2; Table 3-2.
Figure 3-2. When averaging across the moral activation tasks (Rule-Based, and
Ambiguous) and subtracting out the baseline/nonmoral statements in a one-sample t-test
(FWE p<0.05, v>10), a medial frontal and parietal network with additional left- lateralized anterior temporal, lateral temporal, and inferior parietal activations, was recruited. The following regions of activation were observed: L anterior temporal pole
(at pole), lateral orbital frontal cortex (LOFC), precuneus/posterior cingulated (m precun/PCC), L superior temporal sulcus (STS), L temporo-parietal junction (TPJ), medial prefrontal cortex (mPFC), and superior medial prefrontal cortex. A. Activation overlayed on a 3-D rendered template image. B. Activations overlayed on axial slices.
96
Rule-Based Judgments. Analysis of rule-based judgments (clearly right or wrong social situation) irrespective of any agency considerations and comparing this activation to baseline/nonmoral statements in a one-sample test (p<0.001, v>10), revealed activations in the precuneus/posterior cingulate, L STS, bilateral TPJ, superior mPFC,
ACC, L superior PFC, and R middle temporal. Medial regions in the PFC and precuneus/posterior cingulate regions, as well as the L STS/TPJ were prominent clusters in this condition (Figure 3-3, 3-5; Table 3-2).
Figure 3-3. When comparing Rule-Based activation to baseline/nonmoral statement activation in a one-sample t-test (p<0.001, v>10), activations are observed in the precuneus/posterior cingulate, L superior temporal sulcus (STS), bilateral temporal- parietal junction (TPJ), superior medial prefrontal cortex (mPFC), anterior cingulate
97 cortex (ACC), L superior PFC, and R middle temporal. Medial regions in the PFC and precuneus/posterior cingulate (m precun/PCC) regions, as well as the L STS/TPJ were prominent clusters in this condition. Activations are overlayed on a 3D-rendered template image.
Ambiguous. A one-sample t-test (FWE p<0.05, v>10) comparing the
Ambiguous condition (not clearly right or wrong social situations) to the baseline/nonmoral statements resulted in activation patterns involving the superior mPFC, mPFC, ACC, supplementary motor cortex, L STS, L TPJ, medial precuneus/posterior cingulate, L anterior temporal pole, and L LOFC. When relaxing the threshold to an uncorrected p-value of 0.001, additional activation is observed in regions bilateral to the regions specified above as well as areas in the R middle temporal, L precentral, L insula, L ventral mPFC, medial cerebellar, R cerebellar/inferior occipital, R caudate cortex, and thalamus (Figure 3-4, 3-5; Table 3-2).
98
Figure 3-4. A one-sample t-test (FWE p<0.05, v>10) comparing the Ambiguous condition to the baseline/nonmoral statements resulted in activation patterns similar to the
Rule-Based condition but with more robust and additional activation in the ventral lateral
(LOFC) and superior prefrontal cortex (PFC), and temporal pole (at pole) regions.
Ambiguous activations included the superior medial PFC (mPFC), medial PFC, anterior cingulate cortex (ACC), supplementary motor cortex (SMA), L superior temporal sulcus
(STS), L temporal-parietal junction (TPJ), medial precuneus/posterior cingulate (m precun/PCC), L at pole, and L LOFC. Activations are overlayed on a 3D-rendered template image.
99
Figure 3-5. At a shared p<0.001, v>10, average activation maps of the
Ambiguous (green), Rule-based (red) and Nonmoral (blue) conditions are overlayed on a
3D-rendered template image.
Ambiguous vs. Rule-based. A paired t-test contrasting the Ambiguous task with the Rule-based condition (Moral Right and Moral Wrong) (FWE p<.005, v>10) displayed bilateral DLPFC, and superior mPFC/supplementary motor activation. At a more relaxed threshold (p<0.001, v>10), the Ambiguous, compared to the Rule-based condition activated regions in widespread areas of the brain such as the bilateral DLPFC, bilateral LOFC, R VLPFC, bilateral frontal operculum, medial cerebellum, bilateral
100 parieto-occipital junctions, caudate/thalamus, bilateral precentral, medial supplementary motor cortex, and superior medial frontal cortex (Table 3-2).
Nonmoral vs. Moral Judgments. A paired t-test (p<0.001, v>10) comparing Nonmoral judgments to Moral judgments yielded areas of activation in the bilateral insula, calcarine sulcus, bilateral DLPFC, R supramarginal, R occipito-parietal junction, and mid cingulate (Figure 3-5; Table 3-2).
All Moral Judgment Positive Age Regression. After conducting an age regression analysis (p<0.01, v>10) between age and the Moral Judgment condition activations, activation increased with age in the mid cingulum, and the frontal polar, cerebellum, angular gyrus, DLPFC, and supplementary motor cortices in the left hemisphere (Figure 5A). The most prominent cluster observed was in the L frontal polar cortex (Figure 3-6 A,B; Table 3-2).
101
Figure 3-6. A. After conducting an age regression analysis (simple regression, p<0.01, v>10) between age and the Moral Judgment condition activations, activation increased with age in the mid cingulate cortex, and the frontal polar (FP), cerebellum, angular gyrus, dorsal lateral prefrontal cortex (DLPFC), and supplementary motor cortices (SMA) in the left hemisphere. The most prominent cluster observed was in the L
FP. B. Linear Regression displaying the signal change percentage in the L FP (MNI -28,
56, 20) as children and adolescents age (p<0.01). Data point colors correspond to gender of participants (Female=Pink, Male=Blue).
102
Ambiguous Positive Age Regression . After conducting an age regression analysis (p<0.001, v>10) between age and the Ambiguous condition activations, activation increased with age in the L angular guys, ACC, R caudate, posterior insula/posterior temporal gyrus/sylvian fissure, superior medial frontal, R cerebellum, and supplementary motor cortex. The most prominent cluster was in the L angular gyrus, followed by the anterior cingulate (Figure 3-7; Table 3-2).
Figure 3-7. After conducting an age regression analysis (p<0.001, v>10) between age and the Ambiguous condition activations, activation increased with age in the L angular guys, anterior cingulate cortex (ACC), R caudate, posterior insula/posterior temporal gyrus/sylvian fissure, superior medial frontal (mPFC), R cerebellum, and
103 supplementary motor cortex (SMA). The most prominent cluster was in the L angular gyrus, followed by the ACC.
Rule-Based Negative Age Regression. An age regression analysis
(p<0.005, v>10) conducted between age and the Rule-Based activations revealed activation in the bilateral amygdala and parahippocampal regions, and the R precuneus
(Figure 3-8).
Figure 3-8. Linear regression (B) of the signal change percentage in the R amygdala (MNI 24, 4, -30) (A) as children and adolescents age (p<0.01). Data point colors correspond to gender of participants (Female=Pink, Male=Blue).
104 No activations (p >0.01) were observed in the All Moral Judgment and
Ambiguous negative and Rule-Based positive age regression analyses.
105
106
Table 3-2. Average activation maps, paired t-tests, and Age Regression Analyses localizations for the Moral Judgment, Ambiguous, and Rule-based conditions are displayed. MNI coordinates, voxel sizes (k), t-values, and Brodmann areas (BA) are reported. Prefrontal cortex (PFC), temporal parietal junction (TPJ), superior temporal
107 sulcus (STS), medial prefrontal cortex (mPFC), dorsal lateral prefrontal cortex (DLPFC), anterior temporal cortex (ACC).
Discussion
The objective of this study was to investigate the neural substrates subserving the moral judgments of children and adolescents and how these neural substrates are influenced by age in our 9-17 year old healthy sample. We were specifically interested in comparing the neural correlates of Rule-based moral judgments in which there was a clear right and wrong action to Ambiguous judgments in which the right and wrong action was not clear. The results yielded neural activation patterns that not only were clearly identifiable, but also consistent with several regions that have been reported in healthy adult samples. Overall, these activations revealed a common network comprising a core medial frontal and parietal base with additional regions in the ventral lateral PFC, lateral inferior parietal and posterior temporal regions. This network and the age-related changes will be described in detail below.
Polar PFC in Social Moral Processing
The polar mPFC was a prominent cluster of activation identified across the moral conditions in this study. Early frontal damage and adult-onset damage have been demonstrated to result in poor developmental outcomes and poor adaptation,
108 respectively, particularly in the social domain (Harlow 1868; Ackerly and Benton 1948;
Eslinger and Damasio 1985; Anderson, Bechara et al. 1999; Eslinger, Flaherty-Craig et al. 2004). Brain imaging and lesion data have repeatedly suggested that this region plays a key role in social moral processing, such as reflections on mental states of self and others (Castelli, Happe et al. 2000; Gallagher, Happe et al. 2000; Frith 2001; McCabe,
Houser et al. 2001; Frith and Frith 2003; Mitchell, Banaji et al. 2005), evaluative judgments (Zysset, Huber et al. 2002), decision-making (Damasio 1996), social emotional processing (Moll, de Oliveira-Souza et al. 2007), representing novel or multi- tasking event sequences, prospective evaluations, and moral calculus, which is the ability to represent multiple action-outcomes sequences and to compare their weights in a cost/benefit analysis (Moll, Eslinger et al. 2001; Moll, Zahn et al. 2005). Moreover, this region continues to be involved in this processing regardless of nature of stimuli
(personal, impersonal, viewing pictures, reading sentences, passive or making judgments)
(Farrow, Zheng et al. 2001; Greene, Sommerville et al. 2001; Moll, Eslinger et al. 2001;
Moll, de Oliveira-Souza et al. 2002; Greene, Nystrom et al. 2004). Indicative of these findings, it can be speculated that the frontal polar mPFC region is an executive region that is multi-functional in its ability, in a general sequential order, to integrate emotion into decision-making, represent sequences of action, perform a cost/benefit analysis, and select an appropriate response to be executed. Additionally, these functions of the polar mPFC are conducive to the present context of the individual. Badre & D’Esposito (2007) conducted an investigation of PFC hierarchical organization by manipulating different tasks, and found that the frontal polar cortex was most active when the subject’s response was required to be adaptive to dynamic contexts. In summary, the social moral nature of
109 the tasks in the present study significantly recruit the medial polar frontal region, which is a crucial neural construct that largely contributes to the apex of social information processing in that it ensues an executive role in the representation and selection of a behavioral response conducive to the external environment.
OFC in Social Moral Processing
OFC activation continued to be observed after a stringent threshold
(FWE p<0.05) in the MJ and Ambiguous conditions. This region, like the amygdala, is known to receive sensory information from all the sensory modalities (Bachevalier 2005).
The social implications of the OFC, including its medial and lateral subdivisions, in social events are well established (Kaczmarek 1984; Saver and Damasio 1991; Rolls,
Hornak et al. 1994; Zald and Kim 1996; Beer 2002; Beer, Heerey et al. 2003). In the present study, we found lateral OFC (LOFC) activation in the caudal section of the OFC in both the MJ and the Ambiguous conditions, but not in the Rule-based condition
(p<0.001). Roelefs et al. (2009) found that the LOFC plays a key role in social motivational behavior and specifically in the selection of rule-driven stimulus response associations. In relation to this finding, the OFC is thought to be associated with appraising social-emotional stimuli and guiding goal-directed behavior (Bechara,
Damasio et al. 2000; Damasio, Grabowski et al. 2000; Britton 2005). These findings could explain the recruitment of this region in the Ambiguous and MJ and not in the
Rule-based condition, with the latter condition requiring more automatic judgments, whereas the Ambiguous condition requires a higher degree of appraisal of the social
110 scenario and multiple representations of conflicting rules to help guide social decision- making. The OFC and the anterior temporal pole maintain extensive reciprocal interconnections via the uncinate fasciculus (Ghashghaei and Barbas 2002; Kondo,
Saleem et al. 2003). Both are structures involved in detection, representation, and regulation of emotional stimuli (Moran, Mufson et al. 1987; Gloor 1997; Lane, Reiman et al. 1998; Adolphs 2001; Ochsner 2001). The anterior temporal pole activation observed in the MJ and Ambiguous tasks has been suggested to represent social conceptual knowledge and be a convergence center of task-relevant internal and external stimuli
(Moran, Mufson et al. 1987; Gloor 1997) whereas the OFC is more involved in the integration of these representations with other factors involved in social-moral judgments, such as intentionality, consequences, and contextual elements (Zahn, Moll et al. 2007). The OFC also receives projections from the midline and intralaminar thalamic nuclei relaying relevant associative memories (Barbas 1995), useful for understanding and directing behavior appropriately matched to the present social context. The OFC sends projections to the lateral hypothalamus and motor centers, such as the head of the caudate and VTA for the hormonal modulation of hormones and the motor control of emotions, respectively (Selemon 1985). The Ambiguous condition (p<0.001), exhibited caudate activation, as well as motor-related structure activation such as the precentral gyrus and the supplementary motor area. The degree to which the Ambiguous demanded more attention, and cognitive and affective integration, could explain the increased activation indicating a potential physiological and behavioral response. The OFC also has extensive reciprocal connections to the amygdala (Baxter, Parker et al. 2000; Ongur and Price 2000). Unfortunately, amygdala activation did not supersede significant
111 thresholds as might be expected in the Ambiguous condition. When conducting a moral judgment study with adults, Moll et al. (2002), did not find amygdala activation either, even though subjects rated the experimental stimuli as significantly more emotional than baseline moral judgments. Moll explained this phenomenon as the mOFC, which is also known to be involved in social information processing, down regulating amygdala activity. Although LOFC was activated in the MJ and Ambiguous conditions, mOFC activation was not detected in our analyses. However, several structures connected/associated with the mOFC in social contexts were observed in these tasks.
The anterior cingulate cortex which is connected to this region was activated in all conditions (p< 0.001). Studies have suggested an attentional, conflict monitoring, motivation and behavior regulatory role for the ACC, which when malfunctioning, has severe deficiencies in reasoning and emotional expression (Devinsky, Morrell et al. 1995;
Posner 1998; Bush, Luu et al. 2000; Botvinick, Braver et al. 2001). The STS which projects to the mOFC (Moll, de Oliveira-Souza et al. 2002), was also activated in all conditions (p<0.001) as well as the FWE p<0.05 level in the MJ and Ambiguous conditions. This connection functions to integrate cues regarding the intentions and emotional states of others, relaying information such as facial expression, body posture, and voice inflexions (Adolphs and Tranel 1999; Hoffman 2000). There is also a connection between the mOFC and the retrosplenial/posterior cingulate cortex/medial precuneus, which is also activated in all conditions, and has also been implicated in social information processing (Bachevalier 2005). The adjacent medial precuneus, in particular, is thought to play a role in episodic memory retrieval and searching for task-relevant information (Lundstrom, Ingvar et al. 2005). In the MJ tasks, episodic memory retrieval
112 may be necessary as individuals retrieve relevant previously experienced events to be represented for decision-making in the present situation. Considering the social implications of the mOFC, and the connected structures we see activated, the lack of mOFC activation at a significant threshold could indicate the nature of the task and stimuli involved in both the experimental and baseline condition. The LOFC and the
MOFC thus are two distinct ventral PFC regions that differ in their connections and function yet are synergistic as the systems/networks in which they are engaged are convoluted and subserve processes needed for social moral-decision making such as directly attending to stimuli, representing meaningful, affective stimuli, and implementing effector and executive functions.
Developmental Findings
The MJ condition as a whole (combining Rule-based and Ambiguous
MJ’s) recruited frontal and parietal regions as a function of age. The most prominent cluster observed to increase with age is the L frontal polar cortex and was followed by other left hemispheric activations such as the cerebellum, angular gyrus, DLPFC, supplementary motor, and the mid cingulum. It is necessary to note here that the PFC is characterized by using explicit rules to govern behavior according to goals and motivations. Coinciding with the development of the PFC, is the ability to increase number of rules used, represent competing rules, and to be able to flexibly switch between them in present contexts (Zelazo, Muller et al. 2003). The PFC developments noted in the current research on moral statements, laden with rules and values, support
113 these claims. Evolutionarily speaking, the polar PFC is one of the latest brain structures to develop within humans, and hence, accounts for the highly complex and sophisticated social behaviors observed in humans (Casebeer 2003). In addition to the functions previously prescribed to this region in adult studies, such as MJ’s, moral calculus, emotion regulation, future goal-oriented planning and behavioral execution, it has also been suggested that this region is needed in weighting costly decisions in such that an altruistic decision prevails over self-interests (Moll, Krueger et al. 2006). In support of this notion, the behavioral literature suggests that as children and adolescents develop, their ‘centration’ on self transitions to more other-perspective taking and that this process includes empathy. It would seem plausible that the increase in activation observed in the polar PFC region contributes to this transition. Another region of the PFC that had increasing activation with age when making moral judgments was the DLPFC. The prototypical function of this region is working memory (Curtis, Zald et al. 2000; Petrides
2005). The increased activation in this region can be explained by the internalized rules and values that accumulate and are elaborated upon, the social features that are represented, and the ability to hold in mind future outcomes and consequences of decisions, aiding in decision-making processes as children and adolescents age
(Lieberman 2005). As these processes continue to develop, the areas responsible for the representations would naturally seem to parallel this development. In other words, as these frontal circuits become more ‘open’ to external stimuli, prospective thinking, and learned potential outcomes, working memory capacity must also increase. The angular gyrus, which also increased with age, is an integrative region, able to process higher- order information (Pauly, Seiferth et al. 2008) that is essential for bottom-up processing
114 necessary for social judgments. An example of higher-order processes of this structure is demonstrated by a deficiency in abstract representation in that patients with brain damage in this region are unable to understand metaphors (Ramachandran 2004). Responses to social moral stimuli are often automatic and draw upon metaphorical and holistic modes of thinking (Moll et al. 2003). In relations to behavioral data, abstract thought develops with age (Piaget 1968). Further social implications of the angular gyrus, have been demonstrated by abnormal patterns of activation in persons with ASD (Raine,
Buchsbaum et al. 1997) and persons with adolescent-onset schizophrenia (Pauly, Seiferth et al. 2008), disorders that are both characterized with severe social and emotional deficits. Yet another region’s activation observed to increase with age is the supplementary motor region which is known to be involved in the planning and execution of a behavioral response (Tanji 1994). In addition to these structures in the MJ condition, the ACC and caudate increased with age in the Ambiguous condition. As children and adolescents realize the flexible nature of rules based on context, and internalize values and beliefs, more contention will be observed when competing rules are represented as seen with the ambiguous judgments. Researchers describe this conflict monitoring as a kind of an ‘oddball effect’ or norm violation detection in which the ACC plays an important role (Botvinick, Braver et al. 2001; Hornak, Bramham et al. 2003; Moll and
Schulkin 2009) has found this region to be active during these processes. The ACC has also been shown to be involved in controlling emotional output and response selection
(Devinsky, Morrell et al. 1995). As mentioned, the caudate, which is also observed to have more robust activation with age and has been shown to play a role in the motor control of emotions (Selemon and Goldman-Rakic 1985). These latter two findings
115 suggest that emotional processing accompanies the increase in conflict monitoring in that the individual may rely more on somatic states to guide decision-making. In summary, from the behavioral data, we know that not only does decision-making and behavior become refined, but the planning and execution of behavioral responses also becomes more articulate, and moral sensitivity increases (Moll, de Oliveira-Souza et al. 2002;
Moll, de Oliveira-Souza et al. 2003) as the child becomes more socially engaged in the external world. Supporting these changes, the MJ and Ambiguous positive age regressions provide evidence that there is a left-lateralized frontal-parietal network consisting primarily of associative higher-order cortices that are essential for moral maturity. There were no negative age regressions in the MJ and Ambiguous tasks, but the R precuneus and the bilateral amygdala/parahippocampal region activation attenuated with age in the Rulebased condition. In support of the behavioral data, these finding suggests that neural networks continue to organize and are vulnerable to social processing during childhood and adolescence and that the attenuation in the activation of emotional regions in the Rule-based task indicates the reduced somatic representation needed for decision-making and perhaps, the increased cognition needed for learned rule representation and event sequences demanded by social contexts.
Social Moral Sub-Domain Differentiations
When contrasted to the Rule-based condition, bilateral DLPFC, supplementary motor, and superior PFC activation was observed in the Ambiguous condition. In general, the PFC is characterized by using explicit rules to control behavior
116 in current contexts, especially when these rules are novel (Bunge 2006). Based on this knowledge, it is not surprising that significant localized PFC activation is observed when contrasting ambiguous statements to automatic rule-based statements. As mentioned previously, a key role of the DLPFC is working memory, which would be expected to be a process recruited by the Ambiguous condition because of the increase of load processing evidenced by the longer reaction/response times given by the participants.
The increase in load processing most likely reflects representation of multiple, competing rules, and developing social processes such as empathy and ToM that factor into decision-making. Moll et al. (2005) also found that the DLPFC became more active in less predictable social situation compared to the mPFC, which supports the DLPFC activation observed in the present study as children and adolescents make judgments to morally ambiguous statements. One study investigated and compared three groups
(young children, adolescents, adults) on a response inhibition task and observed that the adolescents had the highest degree of activation in the DLPFC, suggesting this group’s greater reliance on the frontal executive network (Luna, Thulborn et al. 2001). As the children and adolescents recalled and represented competing learned rules in the DLPFC, a large cluster encompassing sectors of the superior mPFC and medial supplementary motor was similarly activated in comparison to the more automatic Rule-based condition.
As mentioned previously, these regions have been associated with ToM, including attribution of mental states, cognitive empathy, mental representations, decision-making, attention to subjective emotional states, and in planning and organizing behavioral plan of action. Not only does rule recall and representation increase in the Ambiguous compared to the Rule-based condition, but the attention to and processing in reading
117 mental states and intentions and incorporating additional somatic states to guide decision- making are also more engaged.
In addition to our hypothesis to observe greater cognitive activation in the
Ambiguous task compared to the Rule-based task, we also hypothesized to observe more affective structures, such as the vmPFC and amygdala (Bar-On, Tranel et al. 2003; Lane
2004) that would represent affective feeling states to guide decision-making to the more automatic rule-based judgments. At the highest significant threshold used in the current research (FWE p<0.05), we do not observe this affective activation. We also did not detect these activations when relaxing the threshold, but did observe many other
‘affective’ and basic motive state activations, such as the bilateral frontal operculum gyri, caudate, and thalamus. In conjunction with the cognitive activations observed in the
Ambiguous vs. Rule-based contrast, these findings suggest that various cognitive and affective subcortical and cortical activations are recruited when judgments are made that require greater attention, recall, multiple representations, and the appropriate response selection, with the most robust activation in the frontal medial and lateral regions.
Theory of Mind
In regards to the MJ introduction, as ToM and perspective-taking develop, the intentions of the individuals involved becomes comparable if not more important than the action. Focusing on intentionality is essential for moral judgments (Flavell, Miller et al. 1993). The STS/TPJ and mPFC have been demonstrated by several studies (Saxe,
Carey et al. 2004) to be active in belief attributions and intentionality, both which factor
118 into ToM. These regions are activated in all MJ conditions, which indicates that these
ToM processes are part of a network that subserves MJ’s. Furthermore, although we do not see the more posterior regions increase with age, superior mPFC increased with age in the Ambiguous condition. This can be explained as social featural perception and belief attribution being well established by middle childhood, but the emotional induction, cognitive empathy, and flexible processing known to increase with age, continues to enrich ToM as children and adolescents age.
Left Lateralization and Social Moral Implications
Collectively, the MJ tasks exhibited a left hemispheric dominance in frontal, temporal, and parietal regions of the brain. Although other studies have found left lateralized activation in social and moral decision making (Moll, de Oliveira-Souza et al.
2002; Heekeren, Wartenburger et al. 2003), this finding has not been the highlight of discussion. Indirectly social, select hemispheric studies have shown left hemispheric lateralization for expressive and receptive linguistic processing (Sperry 1974; Joseph
1982; Frost, Binder et al. 1999; Pujol, Deus et al. 1999; Cai, Lavidor et al. 2008). It has been suggested that this linguistic processing plays a key role in the development of sophisticated human social constructs, such as ToM which is a core element of social- moral processing and development (De Villiers 2000). Part of the developing frontal- parietal left lateralization observed in the MJ and Ambiguous conditions included the L angular gyrus, and in the Ambiguous condition only, the L Sylvian fissure region. Both regions are known to be involved in different aspects of linguistic functioning, such as
119 associating various stimuli, integrating these components and relaying this information to areas such as the PFC (Pugh, Mencl et al. 2000; Leonard, Eckert et al. 2001). Moreover, it has been speculated that there is linear increase in left hemispheric functioning with age
(Rubia, Overmeyer et al. 2000). As language and interpersonal communication increase, it is not surprising that we are observing predominantly left hemispheric lateralization throughout the sample, and that this left lateralization activation becomes more robust with age in select conditions. It is important to note that this activation is not due to language alone, evidenced by the contrast of the experimental condition with a baseline condition similar to that of the experimental but void of social moral content. It would seem then, that the lateralization observed may be the result of a specific network that involves social moral language specifically. Moreover, one language theory posits that while both hemispheres are involved in language, the left hemisphere is involved in egocentric speech, which is a more internally generated communication/language not solely based on outside stimuli and is though to be where ‘thought’ originates.
(Vygotskiæi 1962; Joseph 1982). The theory claims that this ability emerges around three years of age and is localized in the left hemisphere and that with age, it develops further by becoming more internalized and by organizing and making sequential sense of one’s experiences and behaviors with the stimuli of the external world. Eventually, these associations or symbolic representations will allow an individual to transcend perception- action reflexive behavior, be able to represent thought prior to action, and to a certain extent, regulate behavior (approximately around the age of seven). Although the theory does not elaborate on developments after this age, lesion studies to the left-hemisphere support the theory of egocentric speech being localized in the left hemisphere. For
120 example, neuroanatomist, Dr. Jill Bolte Taylor (2008) experienced an arterio-venous malformation in language regions of the left-hemisphere which she explained resulted in the loss of her ‘inner speech’ and her ability to communicate with the outside world.
The left lateralization which is known to continue to increase with age, may be in part, due to the progression of self and other awareness, acquisition and organization of rule and event sequences, and more generally, one’s experiences within the social environment.
Summary and Conclusion
In summary, the data in the present study are in agreement with cognitive, behavioral, and moral development theories describing developmental phases that continue into adulthood. For the most part, these theories claim that infants and pre- school aged children are concrete, inflexible thinkers and are superficial and self-centered
(Gibbs 2003; Hoffman 2000; Kohlberg 1964; Piaget 1968). They focus on the salient, tangible features of a present stimulus, and primarily have egotistical motives. It is thought that these childish tendencies are due to the early stage of cognitive development, including an under-developed working memory and ToM, as well as the lack of socialization or learned sequence knowledge. As children develop, these tendencies change, as does cognitive development and socialization. As children’s working memory and theory of mind develop, they develop the ability to hold in mind and coordinate several components of a situation, think more abstractly, and take others perspectives.
They begin to learn to represent and use multiple rules and to flexibly switch between
121 these rules in response to changing contexts, goals, and motivations (Bunge 2006). As children are further incorporated into society, their event sequence knowledge increases, broadening their scope of social knowledge and building social skills (Frederickson
2003). The behavioral tendencies observed throughout development are the result of interactions between cognitive and affective systems that govern moral development.
Our positive regression analyses demonstrated a frontal-parietal network that continues to develop into early adulthood. Particularly, PFC regions, such as the polar frontal and
DLPFC, that exhibit executive functions, and the angular gyrus, which plays a role in abstract higher-order thinking, continues to be vulnerable to social stimuli and influence social and moral decision-making. Our negative age regression demonstrated the internalization of social rules with age.
In the average activation maps of the present study, the ‘social brain’ network is clearly established in childhood. All of the structures indicated in this network were similar MJ activations in adult studies, such as the mPFC, polar frontal cortex, TPJ/STS, posterior cingulate and temporal poles (Greene, Nystrom et al. 2004;
Moll, de Oliveira-Souza et al. 2005). It seems as though the differences may occur in lateralization and activation robustness with age. The regions, although some may be at a more immature stage of processing, seem to be capable of integrating social information concerning intentionality, belief attribution, recall and representation of learned rules, moral calculus, and response selection necessary for moral judgments.
In conclusion, due to the importance and impact of sociality in our lives, whether direct or indirect, an understanding of MJ is of utmost importance. An understanding of MJ will allow for a better understanding of human social behavior and
122 will be innovative in promoting MJ’s that foster prosocial behavior and attenuate antisocial behavior, of which the latter is the root of numerous social disorders/diseases and their associated pain, diminished quality of life, and vulnerability to criminal behavior (Stams, Brugman et al. 2006).
123 Chapter 4
Social Emotion
Basic, or primary, emotions and their underlying neural mechanisms have been studied extensively in humans since the advent of fMRI. The typical basic emotions include fear, anger, disgust, sadness, and happiness and are thought to be cross-cultural
(Ekman 1992; Ekman 1999). To some degree, they are considered hard-wired, innate, primitive neural processes that are crucial for adaptation and survival. According to models such as MacLean’s Triune Brain (MacLean 1990), which describes the evolutionary perspective of brain complexity and development, basic emotional systems are conserved across mammals and are rather ‘closed’ allowing for minimal behavioral flexibility. Humans, who have the highest degree of brain complexity, primarily due to our possession of an expanded neocortex, particularly the PFC, have a high degree of behavioral flexibility to a variety of situational and cultural contexts. Humans have complex thoughts and representations, can plan possible future events, evaluate advantages and disadvantages of decisions, assess outcomes, attribute intentions, and detect and express a large repertoire of sophisticated emotions. The human neocortex, which allows for these higher-order phenomenon, is seamlessly integrated with
‘primitive,’ subcortical structures involved in instincts, motivations, and basic emotions
(Stellar 1954), enabling a refined mushrooming between ‘higher cognition’ and emotions
(Moll, de Oliveira-Souza et al. 2007). The interconnections between sucortical and cortical regions are so numerous that there is rarely an emotion without a thought and vice versa. Human subcortical systems, such as the basal ganglia, brain stem, and limbic
124 structures, provide the raw motivational, visceral-somatic, and automatic materials needed for more complex constructs, such as social emotions. In other words, basic emotions are the springboard for social emotions, which are more complicated emotions involving a great amount of cognition and stored prior knowledge and include emotions such as pity, compassion, guilt, gratitude, social disgust and anger.
Social emotions, or more precisely moral emotions, are defined as differing from basic emotions in that they are intrinsically linked to the interests or welfare either of society as a whole or of persons other than the agent (Moll, de Oliveira-Souza et al. 2002) and are represented across a wide range of cultures (Haidt 2003). Social emotions require extended representation of oneself within a society, function to regulate social behavior, and are often valuable for the long-term interests of the social group rather than the short-term interests of the individual person (Adolphs 2003). Social emotions play a pivotal role in the unique human phenomenon that has become known as morality in that humans have a “sense of righteousness and justice that permeates interindividual behavior” (Waal 1998; Moll, de Oliveira-Souza et al. 2003). Social or moral emotions are responses to social moral violations and/or motivate and guide moral behavior that strives for righteousness and justice for the establishment of group cohesion, conformity, and survival (Moll, de Oliveira-Souza et al. 2003). All social and moral emotions in their normal states are purposeful in motivating and guiding an individual to care, support, enforce, and improve the integrity of the human race, and more generally to uphold social order (Haidt 2003).
Papez (1995), followed by MacLean (1990), theorized that there was an emotional circuit responsible for emotional processing. More recently, neuroimaging
125 studies have supported this claim and have demonstrated that emotions, and social moral emotions alike, are rooted in the brain and involve cortical and subcortical loops. More specifically, subcortical structures, such as the amygdala, septal nuclei, ventral striatum,
VTA, and paralimbic cortex along with hypothalamus have a central role in undirected emotionality and motivation including hunger, aggression, sexual arousal, and social attachment. It is the coupling of the connected cognitive/cortical and subcortical motivational states that allow for what we know as social moral emotions. For example, in sequential order, we notice someone is hurt, have feelings of attachment and anxiety, and are motivated/encouraged to help (Moll, de Oliveira-Souza et al. 2005). Moreover, complex values, beliefs, and social rules accumulated through experience over time compel us to behave in a certain way in a given context. These convoluted systems enable processes necessary for social moral constructs such as attention, semantic and perceptual representation, event and action sequence knowledge, moral appraisals, decision-making, goal prioritization, affective states, and behavioral planning (Moll, de
Oliveira-Souza et al. 2002; Moll, de Oliveira-Souza et al. 2003). Phan et al. (2002) conducted a meta-analysis on basic human emotions and found the mPFC to be the most commonly activated structure (across various induction methods). Moreover, two primary structures indicated by lesion, electrophysiology, and imaging studies to be activated in social emotional processing are the amygdala and OFC (Barbas 1993; Barbas
1995; Bachevalier 1996; Barbas 2000; Ongur and Price 2000; Adolphs 2001; Emery,
Capitanio et al. 2001). Furthermore, the lesion data demonstrate that the laterality and extensiveness of the lesion influenced the particular deficit and to what degree it was manifested. For example, S.M. suffered from bilateral amygdala damage and reported
126 reduced recognition and experience of negative emotions, such as fear (Adolphs 1995a).
Others cases with amygdala damage have reported using fewer emotional words to describe emotional situations. Cases of early-onset damage have additionally demonstrated abnormal social behaviors (Adolphs 1995a; Tranel, Bechara et al. 2002).
Evidenced by epileptic cases, electrical stimulation, and brain lesion studies such as the famous Gage case, where entire personality shifts and emotional disorders result from frontal lobe damage (Harlow 1868), the frontal lobes play a crucial role in modulating emotional behavior (Eslinger and Damasio 1985; Price, Daffner et al. 1990; Davidson
1992; Eslinger, Grattan et al. 1992; Anderson, Bechara et al. 1999). Eslinger et al. (2004) reviewed 10 cases of early PFC damage, in areas such as the DLPFC, mPFC, and OFC, and described severe social-emotional deficits that drastically interfered with daily functioning and interpersonal interaction were related primarily to mPFC, frontal polar, and OFC regions. Many of these individuals suffering from OFC damage have trouble expressing emotions and reacting appropriately to dynamic social contexts (Bechara,
Damasio et al. 2000; Bechara 2002). For example, several cases have reported social regulation deficits such as inappropriate teasing, not prioritizing according to context, and a lack of self-monitoring in social situations (Beer 2002; Beer, Heerey et al. 2003).
Researchers speculate that a link exists between a lack of empathy, antisocial emotion processing, a conservation of social cognition, basic emotions and OFC damage (Eslinger and Damasio 1985; Saver and Damasio 1991; Eslinger, Grattan et al. 1992; Shamay-
Tsoory, Lester et al. 2005) indicating a specific social moral role for the OFC. These regions alone, however, are not sufficient to account for these emotions. Due to the cognitive and affective, and internal and external exchange of information at the
127 intrapersonal and interpersonal levels, respectively, several additional regions are implicated to be involved in social moral emotion processing. The regions suggest a large scale network of brain areas, such as the V/DLPFC, vmPFC, ACC, posterior STS,
TPJ, precuneus, posterior cingulate, anterior temporal lobes, insula, and limbic regions
(Damasio, Grabowski et al. 1994; Anderson, Bechara et al. 1999; Frith and Frith 2003;
Moll, de Oliveira-Souza et al. 2003; Greene, Nystrom et al. 2004; Saxe, Carey et al.
2004; Moll, Zahn et al. 2005; Cacioppo, Visser et al. 2006; Schaich Borg, Hynes et al.
2006). These regions and their interconnectivity account for the complex processes and interactions between systems. Features of emotional stimuli are thought to be processed notably in the amygdala but also in more posterior extrastriate regions, such as the fusiform gyrus. Imaging studies in adults reveal that biologically relevant motion detection, goal-oriented action and mental state attributions consistently activate the posterior STS and TPJ regions. Posterior cingulate and precuneus regions are thought to be involved in emotional processing and episodic memory. The anterior temporal poles are reported to play a role in episodic memory retrieval and as an integration center for interoceptive and exteroceptive cues and when severely damaged is known to severely impair social functioning. The ACC has been shown to play a role in emotional expression and conflict monitoring. These findings suggest that a stable cortico-limbic network is recruited for moral appraisals and emotional processing.
Social moral emotions include two factors- an elicitor and an action tendency.
The emotionally competent stimulus places the agent in a motivational and cognitive state that increases the likelihood of engaging in specific goal-directed behaviors (Haidt
2003). Social moral emotions are classified by these motivational and cognitive states
128 and by the intensity by which they are experienced. Typically, basic and other non-social emotions are measured on positivity/negativity, pleasantness/unpleasantness, approach/avoidance or low/high intensity scales. Social emotions have an added dimension of pro/anti sociality, which is similar to approach and avoidance for non-social emotions. Moral human behavior is supported by neurobiological and psychological processes that constitute an antisocial-prosocial spectrum (Moll, de Oliveira-Souza et al.
2003). Along this spectrum, the social emotions that are at the prosocial end of the social spectrum promote cooperation, helping, social attachment, and social conformity (Moll,
De Oliveira-Souza et al. 2008; Moll and Schulkin 2009) and have been shown in behavioral studies to be beneficial and essential for optimal human health and quality of life (Rilling, Gutman et al. 2002; Fredrickson 2004; Isen 2005). Antisocial emotions, on the other hand, are experienced when social norms are violated, promote aggression, punishment, group dissolution, and social reorganization (Allport 1954; Moll, Zahn et al.
2005) and have negative effects on health. They have been correlated with mental illnesses such as antisocial personality disorder, social phobias, and psycopathy.
Emotional dysregulation in general, which is known to affect social behavior, is a characterization of mental illness, according to the Diagnostic and Statistical Manual of
Mental Disorders (APA, 1994) and plagues 57. 7 million Americans, or 1 out of 4
(NMH, 2005). One of these mental illnesses, major depressive disorder is the leading cause of disability (WHO, 2004). Moreover, 90% of suicide cases exhibit a mental illness (Regier 1993). Considering most persons burdened with a mental illness are characterized by emotional dysfunction, which most likely interrupts normal social functioning and is typically coupled with a long history of these deficits that can often be
129 traced to childhood (Wilson and Norris 2003), developmental research on these underlying processes is essential.
In conjunction with the social emotional implications in the mental illnesses discussed, social emotional processing has been highly correlated to success and quality of life in that this processing encapsulates the emotional, personal, and social competencies that allow an individual to cope effectively with a dynamic social world on a moment to moment basis (Bar-On, Tranel et al. 2003). Bar-On (Bar-On 1997b; Bar-On
2000) developed a model of emotional intelligence that describes these competencies at the optimal levels that would be expected in adulthood or after the proper development of cognitive and affective systems. The components of this model include abilities such as emotional awareness and expression, the recognition of these emotions in others, establishing interpersonal relationships, regulating emotions in order to appropriately adjust to dynamic social contexts, and the ability to motivate the self to strive towards personal values and goals. Supported by brain lesion data demonstrating the conservation of one intelligence and loss of the other, Bar-On indicates that his model of emotional intelligence, which he posits is highly correlated with social intelligence, is vastly different from cognitive intelligence or IQ. Neuroimaging and brain lesion data support this claim (Duncan 2001; Bar-On, Tranel et al. 2003; Eslinger, Flaherty-Craig et al. 2004; Lane 2004), suggesting separate networks subserve these intelligences. The validity for distinct networks subserving social emotion processing and behavior has also been demonstrated. For instance, a dissociation has been demonstrated to exist between moral knowledge and behavior; this chasm is exacerbated in developmental sociopaths
(Blair 1995; Moll, de Oliveira-Souza et al. 2002)(Blair, 1995; Moll et al., 2002). Not
130 surprisingly, in these individuals, there seems to be an impairment in moral emotions guiding behavior. Another example is supported by individuals suffering from frontotemporal damage who experience emotion-induced epileptic seizures in response to unresolved moral issues (Cohen, River et al. 1999). These findings provide clear evidence that neural substrates function to generate moral emotions for the rapid implicit appraisal and/or guidance of social moral behaviors. Further research is needed to investigate these networks, how they integrate information needed for social interaction, and how they contribute to proper social emotional function, and more generally, optimal well-being and quality of life.
Although numerous studies have investigated basic emotions, only few exist that have investigated social or moral emotions. Furthermore, the latter studies have investigated these emotions in adults. To our knowledge, no studies have investigated social moral emotions in children, even though studies suggest that emotional processing continues to develop during childhood and adolescence (Monk et al., 2003). We would like to investigate the neural patterns subserving social emotions, collectively, pro and antisocial emotions, and how these patterns are influenced by age in a healthy sample of developing children and adolescents. Behavioral data and neuroimaging data of children and basic emotion components support dynamic changes in emotion recognition and expression during childhood and adolescents. The adult neuroimaging data provides evidence of established activation in PFC and limbic areas particularly. These regions and the related progressive and regressive neural developments are of utmost interest in the current investigation. In conjunction with this study, future studies will provide the foundation for the early identification of social emotion dysfunction for the purpose of
131 treatment and prevention. Additionally, these investigations will have implications for understanding disorders with marked social deficits, such as autism, Asperger’s,
Williams Syndrome, FTD, and neuropsychiatric conditions that are known to cause significant social emotional deficiencies. The study was designed to test the hypotheses that 1) the collective social emotions would recruit neural regions involved in ToM, such as the medial PFC, medial parietal, and lateral temporal areas, and prototypical affective regions, such as the amygdala and vmPFC 2) that antisocial and prosocial emotions would be differentiated based on their approach and avoidance tendencies, and 3) that the affective regions and select frontal areas would become increasingly active as a function of age as children and adolescents become more sensitive to social moral stimuli.
Methods
Study Participants
The fMRI protocol was conducted on 17 volunteer participants between the ages of 9-17 years (7 male, 10 female) who had no history of medical, neurological, or psychiatric illness, learning disability, or current medication usage (17 subjects’ data instead of 19 subjects’ data was used in this sub-study due to excessive head movement in two subjects during fMRI data acquisition). Along with fMRI scanning, participants were administered standardized tests of general intellect, academic achievement, executive functions, emotional and social intelligence in order to characterize several
132 aspects of cognitive, emotional, and social development relevant to the experimental protocol. Administered tests were as follows: Wide Range Achievement Test 3 Oral
Word Reading, Ravens Colored Progressive Matrices (AB), Oldfield Handedness
Questionnaire, Wechsler Intelligence Scale for Children III Vocabulary and Block
Design subtests, Controlled Oral Word Association task, Wechsler Individual
Achievement Test II Reading Comprehension subtest, Chapman-Cook Speed of Reading test, the Home and Community Social Behavior Scale, and Baron Emotional Intelligence
Inventory: Youth Version. All scores on the various neurocognitive tests demonstrated achievement within the normal range, with one exception on the Home and Community
Social Behavior Scale, where this subject was at risk for social incompetence and antisocial behavior.
fMRI Study Procedures
Preparation and Positioning. The fMRI studies were carried out on a 3.0
T MRI scanner. Stimuli were presented to participants through VisuaStim Digital
Glasses (Resonance Technology Inc., Northridge, CA) and responses were recorded through a handheld device. All subjects were first introduced to the tasks and response device in out-of-magnet training that included introduction and instruction slides as well as sample trials of baseline and experimental stimuli on a laptop computer. Questions about the tasks and procedures were clarified with subjects until they fully understood the tasks for the fMRI session inside the magnet. Training was geared at alleviating any anxiety during the actual fMRI study and thoroughly familiarizing participants with the
133 modes of stimulus presentation, task requirements, and response options. Instruction slides were repeated in-magnet and task readiness cues were presented through the 2-way intercom.
Participants laid supine in a head restrainer that minimized motion and provided precise positioning and comfort. A boxcar fMRI paradigm was used, which consisted of interleaved time intervals of baseline and cognitive activation. During fMRI scanning, participants were instructed to respond to visual stimulation by pressing either the left or right button with their respective thumb on a 2-button handheld device.
Image Acquisition. Functional MRI images were acquired on a whole- body 3 tesla imaging spectrometer (MedSpec S300, Bruker BioSpin Corporation,
Ettlingen, Germany) with a TEM head coil for RF transmission and reception. A fast spin-echo sequence (TR / TE = 4000 ms / 58.5 ms, flip angle = 90º, FOV = 23 ! 23 cm2,
20 5-mm-thick axial slices with 1 mm distance between slices, acquisition matrix = 256 !
192, number of average = 1) and 3D gradient-echo sequence (TR / TE = 25 ms / 5 ms, flip angle = 15º, FOV = 23 ! 23 ! 13.5 cm3, acquisition matrix = 256 ! 192 ! 50, number of average = 1) were used to scan the whole brain, to exclude subjects with any potential neuroanatomic abnormalities. Functional images were acquired with an echo planar imaging sequence (TR / TE = 3000 ms / 35 ms, flip angle = 90º, FOV = 23 ! 23 cm2, 24
5-mm-thick axial slices with no gap between slices, acquisition matrix = 64 ! 64, number of average = 1). For the present study, 316 images were acquired during the alternating blocks of stimulation and baseline.
134 Cognitive Activation Task – Social Emotions. The boxcar design used for this task comprised of alternating experimental and baseline blocks (Figure 4-1). There were 12 experimental blocks, 12 baseline blocks, and 4 rest periods. Experimental blocks were divided into six conditions: Guilt, Pity, Gratitude, Anger, Fear, and Disgust. Two blocks were presented for condition. Each experimental block lasted 48 seconds, containing 4 stimuli, each consisting of two sentences presented for 6 seconds. Baseline blocks lasted 24 seconds, containing 2 stimuli, each consisting of 2 sentences presented for 6 seconds. To ensure the subject was reading the written stimuli, either the right or left button on a hand-held device was to be pressed after reading completion of each sentence. Experimental stimuli were in the form of written sentences designed to evoke the emotion pertaining to the particular block in which it belonged (See Table 4-1 for examples). The sentences were to be read by the subject and subsequent neural social emotional reaction was to be captured by fMRI. Baseline stimuli were similar to the
Experimental Block stimuli in that they consisted of two sentences, but differed in that they were not social-emotional in nature. In other words, the Baseline stimuli were not designed to evoke a social-emotional response, or any emotional response, for that matter. The Rest periods were evenly dispersed throughout the paradigm and each lasting 18 seconds, allowing the BOLD response to return to baseline after a series of stimulation blocks. Subjects viewed reminder instruction windows before each task. The stimuli were all controlled for length (two sentences), point of view (all sentences were in the 1st –person), sentence structure, as well as presentation on screen (font, size, location).
The timing and switching of visual stimuli were automatically controlled by TTL signals
135 incorporated in the pulse-timing program. The total in-magnet time for this paradigm was 15 minutes 48 seconds.
Figure 4-1. The presented schematic is only to aid in understanding the block design used for the current experiment. All blocks are not presented here. The experimental blocks (Gratitude, Pity, Guilt, Anger, Fear, Disgust) are interleaved with Baseline/Non-
Moral blocks. Rest periods are evenly dispersed throughout the paradigm.
136
Table 4-1. Below are example statements representing each of the six different
Social Emotion conditions as well as an example of a Neutral/Baseline statement.
Data Analysis. The fMRI image data were processed with SPM2 software
(Wellcome Department of Cognitive Neurology, London, UK) implemented in Matlab
(Mathworks, Inc.). The first 4 images of each fMRI data set were discarded to remove the initial transit signal fluctuations and subsequent images were re-aligned within the session to remove any minor movements. The T1-weighted high-resolution anatomical images were co-registered with fMRI images and spatially normalized according to the
Montreal Neurological Institute brain template. The time-course images were normalized using the same normalization parameters and then smoothed with a 5 ! 5 ! 12.5 mm3
(full width at half maximum) Gaussian smoothing kernel. A statistic parametric map was
137 generated for each subject under each condition by fitting the stimulation paradigm to the functional data, convolved with a hemodynamic response function. The voxels representing the active regions were overlaid on the 3-D T1-weighted anatomic image in
Talairach coordinates. In this process, brain activation associated with the neutral
(baseline) task was contrasted to the activation generated by the social emotion
(experimental) task, isolating cognitive and emotional processes of socio-moral happenings.
Group analysis was undertaken to generate average activation map of the social emotion conditions: Guilt, Pity, Gratitude, Anger, Fear, and Disgust.
Additionally, these social emotion conditions were grouped into an All Social Emotion
Group which included all social emotion conditions, a Pro-social group (Guilt, Pity, and
Gratitude) and an Antisocial group (Anger, Fear, and Disgust). Below, respective figures and tables of activated regions regarding each condition and group can be found. Simple regressions between age and SPM2-derived z-scores were then computed in order to identify areas of positive and negative correlation with age.
Results
Behavioral Results
Out-of-magnet, participants rated stimuli read in the scanner. Stimuli were rated in the form of a 5-point Likert scale, in terms of how much the participant agreed that the stimulus (sentences) evoked the predicted social emotion. Likewise, the
138 baseline neutral statements were rated on the same scale in terms of how ‘neutral’ the participants thought the stimuli (sentences) were. Participants were in 87.45% agreement with how the designed social emotional stimuli were intended to be interpreted. They were in 74.11% agreement with the intended neutral/baseline stimuli. In a non-study adult control group, persons were in agreement with the intended design of the stimuli,
91.10% and 90.75%, respectively.
fMRI Results
Moral Emotions. Averaging across all emotions investigated in the present study (guilt, pity, gratitude, fear, anger, and disgust) compared to the baseline condition of neutral statements in an one-sample t-test (p<0.005, v>10) yielded activations in the L STS, bilateral TPJ, frontal polar, bilateral middle temporal, bilateral anterior temporal poles, R lingual, medial precuneus, L fusiform, L DLPFC. The most prominent clusters were observed in the L STS/TPJ and the frontal polar cortex, followed by the R TPJ and the bilateral anterior temporal poles (Figure 4-2; Table 4-2).
139
Figure 4-2. Averaging across all emotions investigated in the present study (guilt, pity, gratitude, fear, anger, and disgust) compared to the baseline condition of neutral statements in a one-sample t-test (p<0.005, v>10) yielded activations in the L superior temporal sulcus (STS), bilateral temporal parietal junction (TPJ), frontal polar (FP), bilateral middle temporal, bilateral anterior temporal poles (at pole), R lingual (ling), medial precuneus (m precun), L fusiform (fusi), L dorsal lateral prefrontal cortex
(DLPFC). The most prominent clusters were observed in the L STS/TPJ and the FP cortex, followed by the R TPJ and the bilateral at poles. A. Activation overlayed on a 3-
D rendered template image. B. Activations overlayed on axial slices.
140
Prosocial Emotions. After conducting a one-sample t-test (p<0.005, v>10) on the prosocial emotions (guilt, pity, and gratitude) contrasted to baseline, activation was observed in the bilateral STS/TPJ, L VLPFC, R anterior temporal pole, mPFC, and medial precuneus. The most prominent clusters in this condition were the bilateral
STS/TPJ regions, followed by the L VLPFC (Figure 4-3; Table 4-2).
Antisocial Emotions. After conducting a one-sample t-test (p<0.005, v>10) on the antisocial emotions (fear, anger, disgust) contrasted to baseline, activation was observed in the L inferior occipital, L STS/TPJ, DPFC, VPFC, dmPFC, and R lingual gyrus, with the most prominent cluster in the L inferior occipital cortex, followed by the L STS/TPJ
(Figure 4-3; Table 4-2).
141
Figure 4-3. After conducting a one-sample t-test (p<0.005, v>10) on the prosocial emotions (green) (guilt, pity, and gratitude) contrasted to baseline, activation was observed in the bilateral superior temporal sulcus/temporal parietal junction (STS/TPJ), L ventral lateral prefrontal cortex (VLPFC), R anterior temporal pole (at pole), medial PFC
(mPFC), and medial precuneus (m precun). The most prominent clusters in this condition were the bilateral STS/TPJ region, followed by the L VLPFC. After conducting a one-sample t-test (p<0.005, v>10) on the antisocial emotions (red) (fear, anger, disgust) contrasted to baseline, activation was observed in the L inferior occipital
(inf occ), L STS/TPJ, dorsal LPFC, VLPFC, dorsal mPFC, and R lingual gyrus, with the most prominent cluster in the L inf occ cortex, followed by the L STS/TPJ. Activations are overlayed on a 3D-rendered template image. Common areas of activation between the Prosocial and Antisocial conditions are represented in yellow.
142
Selected activations among social emotions. For each moral emotion, a one-sample t-test was conducted. In this paragraph, the most significant findings are highlighted. For each of the prosocial emotions of guilt (p<0.001), pity (0.005), and gratitude (0.001), significant activations were observed. Guilt recruited regions in the R middle temporal, R TPJ, and frontal polar cortices. Pity recruited the R inferior occipital and the L VPFC and DPFC. Gratitude recruited more posterior activations in the medial precuneus, medial cerebellum, and R lingual. Anger was the only emotion from the
Antisocial emotion condition where significant activation was observed (p<0.001); this activation was observed in the medial regions on the brain such as the occipital pole, thalamic and brainstem regions, dmPFC, superior medial frontal, precuneus/posterior cingulate, and supplementary motor, and in the L cerebellum (Table 4-2).
Prosocial vs. Antisocial. After conducting a paired t-test (p<0.01, v>10), contrasting Prosocial and Antisocial conditions, activation was observed in the Prosocial condition as follows: R precuneus, putamen/lenticular nucleus, pre and postcentral gyri, and the paracentral lobule (Figure 4-4; Table 4-2). There was no significant activation identified in the Antisocial vs. Prosocial contrast.
143
Figure 4-4. After conducting a paired t-test (p<0.01, v>10), contrasting Prosocial and Antisocial conditions, activation in premotor, motor associative, and motor and emotional regulative areas was observed. These activations were as follows: R precuneus (precun), putamen/lenticular (put/lenticular) nucleus, pre and postcentral gyri
(pre/post central), and the paracentral lobule (para lobule). Activations are overlayed on axial slices.
SE Age Regression. SE activation patterns pertaining to increasing and decreasing age were generated after conducting age regression analyses (p<0.01, p<0.005, respectively). Activation that increased with age was observed in localized subcortical areas, such as the R hippocampus/amygdala region. Activations that decreased with age were observed in the mid cingulate and convergent areas such as the
144 R parietal-occipital junction and the L temporal-occipital junction (Figure 4-5; Table 4-
2).
Figure 4-5. A. A linear regression analysis was conducted between contrast
(indicative of signal change between baseline and the experimental task) in the R amygdala (MNI 24, -4, -15) and age for each subject. Data point colors correspond to gender of participants (Female=Pink, Male=Blue). B. A positive age regression analysis
(p<0.01) yielded activations in the R amygdala. Activation is overlayed on a template image displayed in three planes.
145
Prosocial and Antisocial Emotion Age Regressions. In the Prosocical conditions, activations were observed to increase and decrease with age. The R cerebellum and R hippocampus/amygdala regions were found to increase in activation as a function of age (simple regression, p<0.005, v>10), whereas R middle temporal gyrus activation decreased with age (p<0.005). Activation was not found to increase in the
Antisocial condition as a function of age, but was found to increase in the L precentral gyrus and the medial cuneus and precuneus (simple regression, p<0.005, v>10).
Emotional Intelligence and SE Activation Regression Analysis. After conducting a regression analysis (simple regression, p<0.01, v>10) between emotional intelligence scores from the Baron Emotional Intelligence Inventory: Youth Version and
SE fMRI activation, prominent activation in the rostral brainstem and hippocampal/parahippocampal regions were more robust with increasing emotional intelligence (EQ) scores (Figure 4-6).
146
Figure 4-6. A. A linear regression analysis was conducted between contrast
(indicative of signal change between baseline and the experimental task) in the L hippocampus/parahippocampus region (MNI -28, -34, -7) and emotional intelligence
(EQ) for each subject. Data point colors correspond to gender of participants
(Female=Pink, Male=Blue). B. A positive regression analysis (p<0.01) yielded activations in the L hippocampus/parahippocampus region (MNI -28, -34, -7). Activation is overlayed on a template image displayed in three planes.
147
148
149
Table 4- 2. Average activation maps, paired t-tests, and Age Regression Analyses localizations for the Social Emotions, Prosocial, and Antisocial conditions are displayed.
MNI coordinates, voxel sizes (k), t-values, and Brodmann areas (BA) are reported.
Temporal parietal junction (TPJ), dorsal medial prefrontal cortex (dmPFC), hippocampus
(hippo), anterior cingulate cortex (ACC), midbrain (MB), ventral tegmental area (VTA).
Discussion
The objective of this study was to investigate the neural substrates associated with social emotions in children and adolescents and how these neural substrate were influenced by age in our 9-17 year old healthy sample. While our main concern was investigating social emotions, in developing children and adolescents, collectively, we were also interested in contrasting prosocial emotions (guilt, pity, gratitude) and antisocial emotions (anger, fear, disgust) within this group. The results yielded neural
150 activation patterns that were not only clearly identifiable, but also consistent with several regions that have been reported in healthy adult samples.
In accordance with adult studies, we found neural activations involved in childhood and adolescent social emotion processing, reflecting the numerous cognitive and affective components involved in emotional processing. As mentioned in the introduction, the most common areas found in the moral social emotion literature involve a cortical-limbic network. Within this network, we found superior medial PFC, frontal polar, DLPFC, anterior and middle temporal, TPJ, STS, lingual and fuisform activations in the All Social Emotion task (SE task p<0.005). The most robust activations observed in this task have been designated to play key roles in self-awareness and the ToM network, which include the superior medial PFC, STS, anterior temporal poles, and TPJ cortices. The superior mPFC has been shown in studies to be directly related to increased self-awareness, social cogntion (Goldberg, Harel et al. 2006), and moral judgments
(Moll, de Oliveira-Souza et al. 2002; Moll, de Oliveira-Souza et al. 2003). The STS has been consistently shown to be involved in social perception processing, such as representing goal-directed action (Jellema, Baker et al. 2000; Pelphrey, Singerman et al.
2003) belief attribution (Fletcher, Happe et al. 1995; Gallagher, Happe et al. 2000;
Narumoto, Okada et al. 2001; Gallagher, Jack et al. 2002) and emotion attribution
(Narumoto, Okada et al. 2001; Decety and Sommerville 2003)(Decety & Chaminade
2003, Narumoto et al. 2001). Multi-convergence regions such as the TPJ have been well documented for their involvement in social moral emotions because of the converging neural processing streams integrating social information and functions related to the STS and the ventral visual association cortices. Lastly, studies indicate an important role for
151 the anterior temporal poles in semantic feature knowledge and episodic memory processing (Nakamura, Kawashima et al. 2000; Zahn, Moll et al. 2007).
Lateralization of Social Emotions
The activation identified was bilateral for the most part, supporting other findings that suggest a complementary role by both hemispheres in the production of emotions (Gainotti 1972; Gage and Safer 1985; Wittling 1990)(Gage & Safer 1985,
Gainotti et al. 1993, Wittling, 1990). With the exception of the right lingual/cerebellum and medial activations, however, we did find a slight dominant left hemispheric activity
(in DLPFC, TPJ, STS, fusiform) in the All Social Emotion activation map. One of the oldest theories of emotion suggested that the left brain is specialized for cognition and the right for emotion. More recently, Gainotti (2005) explains that the right hemisphere is mainly involved with primary basic components of an emotional response that are involved more so with the limbic system and autonomic nervous system (ANS) activation, whereas the left hemisphere is involved in the regulation and conscious control of emotional expression, which might explain this slight lateralization considering the cognitive nature of these more sophisticated human social emotions. In opposition to theories supporting hemispheric lateralization for emotions, the majority of researchers now believe both hemispheres process emotions, and that lateralizations are only found between or within regions of the brain (Wager, Phan et al. 2003). In support of this theory, researchers have shown that positive and negative emotions, which have similarities to certain prosocial and antisocial emotions (although prosocial and antisocial
152 emotions are more complex and can include both postive and negative emotions; i.e. guilt) are processed by both hemispheres but with a hemispheric dominance in the PFC region (Ahern and Schwartz 1985; Davidson, Jackson et al. 2000). The right PFC is typically more activated for negative affect and withdrawal and the left is more pertinent for approach and positive affect. Lesion studies have also provided evidence that damage to the PFC in the left hemisphere will produce depressive symptoms (Gainotti 1972;
Sackeim, Greenberg et al. 1982; Robinson, Starr et al. 1984; Morris, Robinson et al.
1996). Davidson et al. (1990) showed that film-induced negative effect increased right
PFC and temporal pole activation, whereas positive effect activated left-hemisphere structures. Lastly, Urry et al. (2004) reported baseline PFC activation asymmetries predicted increased well-being. In the present study, the Prosocial condition supports
PFC lateralization by displaying significant left PFC activation compared to right PFC.
However, left PFC was also dominant in the Antisocial condition, although less robustly than in the Prosocial condition. Perhaps, the minor systematic differences between positive and prosocial emotions and negative and antisocial emotions overpower similarities, not allowing similar hemispheric trends to be applied. An alternative hypothesis is that non-social emotions, categorized into positive and negative, demonstrate lateralization between them, whereas social emotions are left lateralized and differ in robustness between prosocial and antisocial. Lastly, regional lateralization generalizations have been questioned by researchers suggesting differences may be influenced by the nature of the stimuli induction or study design (e.g. pictures vs. written scripts) and differences between moral and more basic emotions (Adolphs, Tranel et al.
1995; Farrow, Zheng et al. 2001; Moll, Eslinger et al. 2001; Moll, de Oliveira-Souza et
153 al. 2002; Moll, de Oliveira-Souza et al. 2005). For example, Takahashi et al. (2004) found a slight left hemispheric dominance for social emotions when using language/reading stimuli similar to the ones used in the present study. The language/reading load in the task could be responsible for the slight left lateralization we observed. However, our baseline was designed to counterbalance stimuli/reading effects, suggesting a slight left lateralization specific to social emotion processing. Furthermore,
Moll et al. (2001) used auditory moral statements as experimental stimuli opposed to written statements as used in the current study, and reported similar activations to the ones observed here. In relation to the current research, this suggests that the social moral processing and not the stimuli induction method explain the social emotion activation patterns. Further studies need to be conducted to better understand the causes for regional lateralization differences and if and how they differ between non-social and social emotions and within the social emotion domain, between prosocial and antisocial emotions.
Posterior Brain Activations
In addition to these activations, we saw a substantial amount of activation in posterior brain regions, including polar inferior occipital (Antisocial condition), lingual
(SE and Antisocial condition), fusiform (SE condition) and cerebellar activity (SE and
Prosocial Positive Age Regression). Several studies do show these areas to be activated in social emotional and cognitive constructs (Moll, de Oliveira-Souza et al. 2002; Gobbini,
154 Koralek et al. 2007), but they are typically not the focus of discussion. A meta-analysis conducted by Wager et al., (2003) on basic human emotions reported that the some posterior regions, such these areas, are activated in emotions and hint that these areas are most likely more complex than researchers once thought. Until recently, the cerebellum has been thought of as a motor-related structure. Scientists are now finding that it is also involved in cognition, learning, memory, and emotion (Anderson, Anderson et al. 2001;
Marien, Engelborghs et al. 2001; Turner, Paradiso et al. 2007). Select autistic cases report cerebellar abnormalities (Brambilla, Hardan et al. 2003). Lesion studies have shown that the right cerebellum in particular has connections to frontal areas involved in the present study, such as the left inferior and superior frontal PFC (Appollonio, Grafman et al. 1993; Marien 2000), suggesting that the cerebellum, through a cerebello-ponto- thalamic-cortical tract, is involved in social emotion processing (Sonmezoglu, Sperling et al. 1993). Additionally, the cerebellum was the most prominent activation in the
Prosocial positive age regression, suggesting that as the connectedness is established between cognitive and emotional networks, structures once though to be more primitive, remain important in higher order processing. Besides being known as the fusiform face area, the fusifrom gyrus has been implicated in emotion processing (Britton 2005) and
ToM tasks such that it represents visual stimuli that signify agency and intentionality
(Ohnishi, Moriguchi et al. 2004; Gobbini, Koralek et al. 2007). It seems to have a general role in the bottom-up-processing of perceiving, identifying and relaying social emotional stimuli for further analyses. Additionally, when subjects were involved in a dimension task where they had to discriminate between objects based on size, orientation, shape, texture, and a context task that required subjects to change responses based on
155 contextual cues, the fusiform was activated (Badre and D'Esposito 2007). This may imply that not only it is important for visual discrimination and higher-order visual processing, but also may be involved in a network that relays information useful for dynamic social environments. The lingual gyrus, adjacent to the fusiform gyrus, was not hypothesized to be activated because it has not been a region of interest in the adult social emotion literature. Due to its extrastriate visual processing role, proximity of this structure to the fusiform gyrus, and the role it plays in face processing (Robinson 2007), we suspect that this region plays a general role in the implicit processing of social emotion stimuli. The TPJ, also a more posterior region, but focused on in the social literature, was recruited in the SE tasks. This region also has extensive connections with the visual association cortices which is not surprising considering the role of the TPJ in integrating social featural information (Goel, Grafman et al. 1995; Wiggs, Weisberg et al.
1999; Saxe, Carey et al. 2004; Arzy, Thut et al. 2006; Saxe, Schulz et al. 2006; Decety and Lamm 2007). Due to the activation observed in the present study and the discussed connections important for social emotion processing, it is evident that the visual association cortices, cerebellum, and multimodal association cortices highlight salient features of stimuli to feed forward to executive control centers. Lastly, a question may arise as to whether the stimuli used in the present study were causing these activations and it was not as we are suggesting, playing a role in a social moral processing network.
We do not think this to be the case, because baseline statements were similar to experimental statements, differing only in social moral emotional content. Additionally,
156 Limbic Sensitivity
Considering the extensive connections between these visual cortices and amygdala nuclei, we expected to observe amygdala activation as the visual cortex fed emotional salient information forward to limbic areas. This activation was not present and we believe this to be due to top-down regulation of the by higher cognitive social structures, such as the PFC, which is known to play an important role in self-regulation and behavior reinforcement (Baxter, Parker et al. 2000) or to its shared activation in the baseline and experimental conditions. However, the R hippocampal/amygdala region activation was found to increase with age in social emotion processing (p<0.01) and more specifically in prosocial emotion processing (p<0.005). This finding suggests that as children and adolescents age, there is a more accurate degree of emotion identification, accumulation of personal experience recollection and a higher degree of emotional simulation with others or situations extended outside of the self. Additionally, Davidson et al. (2004) found that the hippocampus is involved in the context-regulation of emotions, which would be expected to be more pertinent as developing children continually acquire rules and associate these rules within certain contexts. Moreover, what has been labeled the ‘reinforcement learning circuitry’ has extensive connections between regions such as the hippocampus, amygdala, and the OFC (Casebeer and
Churchland 2003). The intense socialization process that takes place during the childhood and adolescent years is characterized by the intense learning and internalization of social moral rules and social conventions. These activations may contribute to that process as cognitive and affective systems are integrated. The greater
157 amygdala recruitment with age might be explained more generally as its integration with the developing cognitive systems, such as the PFC that are known to develop throughout adolescence. Several studies demonstrate the amygdala’s role in facial emotion recognition (Haxby, Hoffman et al. 2000; Gobbini and Haxby 2007; Kleinhans, Johnson et al. 2009). When this phenomenon is studied developmentally, research indicate that facial emotion recognition abilities are influenced by puberty and hence, increase during adolescence (Petersen 1988; Kolb, Wilson et al. 1992). Another study (Monk, McClure et al. 2003) showed a difference between adults and adolescents when asked to shift between emotional facial expressions and attending certain features of the face. These findings not only provide evidence that emotional processing occurs during this stage of development, but also support increasing emotionally-related limbic activity with age.
Moreover, emotional intelligence (EQ) scores of the participants in the current study were positively correlated with limbic and motivational system activations, supporting
Bar-On’s theory of overlapping social and emotional intelligences, and suggesting that individuals with a higher correlation have a higher moral sensitivity, including simulation of others feelings and empathy (Bar-On, Tranel et al. 2003).
Prosocial Emotions
The prosocial emotion neural patterns accounted for the majority of the activation in the All Social Emotion activation map in which substantial medial and bilateral activation were exhibited in the STS/TPJ, mPFC, and medial precuneus structures with additional R anterior temporal pole, L VLPFC, and R precuneus. Right
158 anterior pole activation, as mentioned previously, plays an important role in semantic feature knowledge and episodic memory processing (Nakamura, Kawashima et al. 2000;
Zahn, Moll et al. 2007). The ventral lateral PFC, also activated in the Antisocial condition but more robustly in the Prosocial condition, is known to be an affective structure because of its extensive connectivity to the limbic system and has been demonstrated to play a role in aversive emotions (Kringelbach and Rolls 2003) including social aversion and other-critical emotions (Moll, de Oliveira-Souza et al. 2007). The shared activation between the two indicate structures common for social emotion processing and that differences may not be as clear because the complex mix of positive and negative emotions included in social emotions, such as guilt and pity. The R precuneus activation has been implicated in ToM tasks and for the integration of emotion, imagery, and memory (Fletcher, Happe et al. 1995; Maddock 1999). In contrast to the
Antisocial condition (paired t-test p<0.01), the Prosocial condition recruited the basal ganglia, (putamen/lentiform nucleus), which has been shown in previous studies to be involved in the programming of emotionally induced behavior (Wager, Phan et al. 2003).
Perhaps, this recruitment is due to the “approach” nature related to prosocial emotion and behavior. Research supports this explanation by showing that prosocial behavior is involved in broadening one’s future thought and action repertoire, leading to exploratory behavior and skill-building (Frederickson 2004). Additionally, a meta-analysis of PET and fMRI emotion activation studies found 70% of happiness studies activate the basal ganglia (including mainly the VTA and putamen) (Phan, Wager et al. 2002). It is important to note here that the caudate of the basal ganglia was only one of two activations that survived the relaxed 0.05 threshold in the collective SE Pos Age
159 regression, suggesting a more “other” centered, prosocial framework of thinking that parallels moral maturation. The putamen/lentiform nucleus and caudate sectors of the basal ganglia activations support previous data in that they contribute to prosocial emotional processing and behavioral planning and as the present study findings suggest, are involved in social moral emotional development. Additionally, the Prosocial vs.
Antisocial condition recruited several other motor-related structures, such as the precentral gyrus and the paracentral lobule. In relation to this finding, a PET study showed increases in left-sided pre and post central gyri activation to positive affect
(Sutton 1997). Adjacent to the precentral gyrus, postcentral, or somatosensory cortex, was activated in the Proscial vs. Antisocial contrast. Representation of body signals or emotional states are thought to occur at level of the insula and somatosensory cortices
(Bechara 2006). ‘Conscious feelings’ which include social emotions are at the cortex level and are thought to map visceral states and bring them to conscious levels/self- awareness. The reported studies in conjunction with individuals suffering from disorders, such as anosognosia, suggest that insular-somatosensory cortices would be active in the all SE tasks. However, insula activation was not observed, and the somatosensory actvation was only observed when contrasted to the Antisocial condition. The present finding suggests that the Prosocial condition more robustly represents emotional body states of self and others, and perhaps induce a higher degree of self-awareness than the
Antisocial emotions.
Only humans have the cognitive abilities to make utilitarian decisions and behave in a way that is not in the best interest of the individual, and understand their complex role and relationships to others within a social environment. Prosocial emotions
160 and behavior often incorporate a higher degree of consequences and societal prioritization of goals. In other words, they are not typically immediately satisfying and the rewards are often delayed and may not even reward the person behaving pro-socially.
Humans have the ability to plan for the future, estimate consequences, control impulses, and behave according to priorities and goals which are behaviors often displayed when acting prosocially instead of selfishly. The highly developed language and cognitive capabilities stored in the temporal and frontal lobes, respectively, are especially active in these more unique human abilities, such as Pro-social emotions and behavior. In the Pro- social condition compared to the Anti-social condition, we see a higher degree of activation in these areas, suggesting as Moll did in a similar study conducted on adults that pro-social emotional activation patterns reflect a greater load of knowledge of social rules and moral values (Moll, de Oliveira-Souza et al. 2007). In particular, Moll highlights the greater PFC activation observed in prosocial emotions and attributes this to the reparative measures that may be taken in the future (Moll, Eslinger et al. 2001), such as helping- measures that require a more complicated, engaging, attentive future plan that will help guide goal-oriented behavior. An example of the additional resources needed for prosocial emotions is demonstrated in the Guilt condition. Self-conscious emotions such as guilt require the understanding of violation of social norms and negative evaluation of self which both require ToM (Takahashi, Yahata et al. 2004). Children with autism are known to have an impairment of ToM, and also exhibit impaired recognition of self-conscious emotions, such as guilt and embarrassment (Heerey, Keltner et al. 2003). We are seeing the ToM network activation superior in the guilt emotion compared to the other emotions tested (and in RTPJ which has been documented more
161 so to be involved in ToM) suggesting the greater demand for social processing needed for prosocial emotions, and more specifically, when reparative actions need to be made. In summary, when directly contrasting pro and anti social emotion conditions, significant activation in cognitive, emotion, and motor areas support the “higher processing” required for this processing. Furthermore, no activation was observed when contrasting
Antisocial vs. Prosocial conditions.
Antisocial Emotions
The Antisocial condition activated selective areas also activated by the
Prosocial condition such as the polar mPFC, and the left TPJ. Additional activation was observed in the DLPFC, inferior occipital, and R lingual regions. As mentioned, this activation was left-lateralized which goes against popular belief that “negative emotions” are right laterlized in the mPFC (Robinson and Starkstein 1989). Based on investigations on emotional facial expression of fear, disgust and anger, we expected to see amygdala
(Breiter, Etcoff et al. 1996; LeDoux 2000), putamen and insula (Sprengelmeyer, Rausch et al. 1998; Moll, de Oliveira-Souza et al. 2007), and ACC and OFC (Phan, Wager et al.
2002; Eisenberg, Lieberman et al. 2003; Moll, de Oliveira-Souza et al. 2007) activation in the antisocial conditions. Moll et al. (2002) found emotionally unpleasant stimuli, whether moral or nonmoral, to activate the amygdala, insula, thalamus and MB.
Although many of the regions we hypothesized to be active in the Antisocial activation were not observed, other activations, such as the thalamus and midbrain, were selectively observed in the anger condition but were not seen in the disgust and fear condition. The
162 OFC and ACC, hypothesized but also not activated in the collective antisocial condition or selectively in the separate conditions, are indicated in social aversive processing which
Blair et al. (1999) claims to be important for response reversals (changing current behavioral response). We expected to observe more ACC activation in the Antisocial condition compared to the Prosocial condition, because of the social pain and conflict monitoring roles associated with this region (Eisenberg, Lieberman et al. 2003; Greene,
Nystrom et al. 2004). We may not see this activation because negative emotions may be instrumental in the prosocial emotions such as pity and guilt. Selective activations in response to the anger stimuli could be due to these stimuli possibly being easier to imagine and experience. The large absence of the hypothesized activations to the antisocial stimuli could be attributed to the nature of the scanner (not true social interaction). Another explanation for these absences is that these activations were present in both experimental and baseline conditions and in both Antisocial and Prosocial condition.
Developmental Findings
One of the areas we were particularly interested in investigating was the PFC.
Several lesion studies have demonstrated that frontal lobe damage, and more specifically,
PFC damage, effects aspects of cognition, social behavior, and moral conduct (Eslinger,
Flaherty-Craig et al. 2004). These lesion studies along with the behavioral literature posit that as children and adolescents mature, cognitive flexibility becomes more apparent as
163 they are able to consider more variables into their decision-making, such as their role in intersocietal relations, others intentions, emotions, goals, as well as their own emotional and cognitive constructs. Graffman (1995) proposes that these constructs allow for numerous dynamic and extensive behavioral models that coincide with long-term complex goals. Moral sentiments and behavior is known to stem from these foundational systems. As social relationships and experiences mature, these moral sentiments, also, in turn become more complex and involve a greater degree of autonomy and moral reasoning (Eslinger, Flaherty-Craig et al. 2004), demonstrated by the differentiated social emotions activation patterns. Although we did not observe PFC activation increase with age in the present task, we did observe increased limbic activation, as mentioned previously, increasing as a function of age. Based on her reseach, Blakemore theorizes, that as an adolescent matures into adulthood, there is less PFC activation, and that an anterior to posterior activation shift occurs. We do not see PFC decreasing, nor posterior increasing in the SE, but the lack of PFC increasing with age is supported by her research. An alternative finding to this negative finding may be related to the nature of the stimuli. Perhaps, if more complex moral dilemmas were presented to subjects, increasing PFC activation would be observed as we hypothesized. Decision-making, in which the subjects had to make a judgment in response to the scenario, may recruit PFC activation with age (as seen in the MJ conditions).
For the most part, multi-convergence areas, such as the parietal-occipital and temporal-occipital regions became less active with age as seen in the SE negative age regression. This suggests that social emotional processing becomes more efficient and refined with increasing age as children and adolescents accumulate event sequence
164 knowledge, have more acute social perception, have more cognitive and affective constructs, such as ToM, from which to base judgments, and generally, the assimilation of the self with the external social environment. Reduced activation in these areas is most likely due to the establishment and efficiency of structures and networks specialized for social moral processing.
Summary and Conclusion
In conclusion, our results indicate that the establishment of these social moral processes begin in early childhood and involve attention directed to and perception of social processes, such as intentions processed by the visual association and TPJ, social value tagging and relaying processed by the cerebellar, limbic, and ventral PFC areas, and social planning, representation, and behavior processed by the dorsal PFC areas.
With a slight left hemispheric dominance, these structures work within a network to integrate and share the multiple and complex social moral constructs that guide social moral emotions and behavior. Limbic activation increases with age as higher cognitive social structures, such as the PFC, become more extensively connected with this region, and as children and adolescents emotional systems become more sensitive to social moral interpersonal situations. Prosocial emotions require significantly more resources for processing and recruit structures necessary for approach or motor-related behavior.
Differing activation maps observed amongst the moral emotions are in agreement with adult studies demonstrating distinct networks for various moral emotions. Future investigations are needed to further delineate the dedicated networks underlying each
165 prosocial and antisocial emotion. The present findings have significant future implications in that they provide foundational research for the early identification of social emotional dysfunction, treatment and intervention for the promotion of prosocial behavior, and increased quality of life and well-being.
166 Chapter 5
Final Discussion
The aim of the present studies was to investigate the neural underpinnings of social moral processing in typically developing children and adolescents using high field
MRI imaging while participants either executed an explicit judgments based on the
‘rightness’ or ‘wrongness’ of social moral actions or passively read social moral emotional scenarios. Based on the behavioral literature on children and adolescents, and lesion and neuroimaging findings of which the majority have been in adults, we concentrated on three critical social moral constructs that subserve social moral events: social moral agency, emotion, and judgments. Using the most revolutionary and safest neuroimaging technique, fMRI, we identified clear patterns of neural activity for each social moral construct. Many of our findings were hypothesized and nicely paralleled behavioral developmental theories and were in support of much of the neuroscience data.
Across the presented studies, we observed a complex interplay of overlapping activation patterns, as well as dissociable networks. Likewise, adult neuroimaging studies investigating positive and negative basic emotions (Ahern and Schwartz 1985;
Davidson, Ekman et al. 1990; Phan, Wager et al. 2002), various social emotions (Farrow,
Zheng et al. 2001; Takahashi, Yahata et al. 2004; Britton 2005; Moll, de Oliveira-Souza et al. 2007), and social moral judgments (Moll, Eslinger et al. 2001; Moll, de Oliveira-
Souza et al. 2002; Heekeren, Wartenburger et al. 2003; Greene, Nystrom et al. 2004;
Young, Cushman et al. 2007; Eslinger, Robinson-Long et al. 2009) have discovered the complexity of subserving neural networks in that there exists shared and differentiated
167 regional activations between each of these phenomena. Additional evidence supporting the present convoluted variations in related neural networks is that the ToM network seems to function perfectly normal in psychopaths, who typically are unable to experience specific vital social emotions, such as empathy and guilt (Richell, Mitchell et al. 2003). Autistics, on the other hand, have clear deficiencies in the ToM network which eradicates their ability to attribute belief and intentionality to others. This deficiency seems to have select overlap in other networks as well, as autiscs are known to have diminished emotional feelings of pride and embarrassment (Baron-Cohen 1992; Frith and
Frith 1999).
We observed intra-study as well as inter-study differentiated networks that suggest large-scale neural organization of social moral judgments and social emotions.
We observed variations between the selected social emotions of fear, disgust, pity, gratitude, anger, and disgust, and between prosocial and antisocial emotions in the Social
Emotions study. In the Agency study, we observed a slight difference between the Self-
Agency and Other-Agency activation patterns, mainly in robustness and lateralization of activation. In the MJ study, we observed marked differences between the moral and nonmoral and between Ambiguous and Rule-Based Judgments. Furthermore, clear differences were detected between the collective neural networks subserving each construct of agency, social moral emotions, and moral judgments. The variations within each study and between each study suggest a very intricate, complicated, set of neural structures that serve many roles and are selectively recruited for necessary processes.
Despite these differences, common activation patterns were pronounced among studies.
168 The following discussion will provide coverage of both the commonalities between studies as well as differences in the following sequence 1) Cross-Sectional Post-
Hoc Analyses 2) Cross-sectional results summarized 3) Developmental results summarized 4) Highlights 5) Models explaining summarized findings 6) Limitations in the presented studies 7) Importance of Research 8) Future questions and directions
1) Cross-Sectional Post-Hoc Analyses
Conjunction Analysis (CA) Across Studies
After conducting a conjunction analysis between the three social moral construct conditions, we found the L STS/TPJ, superior mPFC, L middle and anterior temporal gyri, and medial precuneus to be activated (p < 0.001) (Figure 5-1).
169
Figure 5-1. After conducting a conjunction analysis between the three social moral construct conditions, a left lateralized network was identified in structures reported by the adult literature to be vital for social moral processing. We found the L superior temporal sulcus/temporal parietal (STS/TPJ) junction, superior medial prefrontal cortex
(mPFC), middle and anterior temporal gyri (mid/at pole), and medial precuneus (m precun) to be activated (p < 0.001, v>10). Activations are overlayed on a 3D-rendered template image.
170
Paired t-tests between studies
MJ vs. SE. When contrasting the MJ and SE conditions in a paired t-test,
MJ activations are observed in the precuneus, posterior cingulate, bilateral occipito- parietal junction, R angular, ACC, L insula, L cerebellum, bilateralsuperior and anterior temporal gyri (p<0.005, v>10) (Figure 5-2).
Figure 5-2. When contrasting the Moral Judgment and Social Emotion conditions in a paired t-test, Moral Judgment activations were observed in the precuneus (precun), posterior cingulate (PCC), bilateral occipito-parietal junction (OPJ), R angular, anterior cingulate cortex (ACC), L insula, L cerebellum, bilateral superior (sup temp) and anterior temporal (at pole) gyri (p<0.005, v>10). This activation pattern highlights the heightened
171 activation needed for the integration of processing streams subserving explicit decision- making. Activations overlayed on a 3D-rendered template image.
SE vs. MJ. The Social emotion condition contrasted to the Moral
Judgment condition, recruited the L lateral dorsal/ventral prefrontal cortex (LD/VPFC), L temporo-parieto-occipital junction (TPOJ) (p < 0.01, v>10) (Figure 5-3).
Figure 5-3. The Social emotion condition contrasted to the Moral Judgment condition, recruited the L lateral dorsal/ventral prefrontal cortex, L temporo-parieto- occipital junction (p < 0.01). This contrast yielded much less robustness and activations than the opposite contrast, indicating reduced recruitment for social moral processing when passively viewing social moral stimuli. However, slight distinctions in key areas
172 are observed in the displayed contrast. Activations are overlayed on a 3D-rendered template image.
2) Cross-Sectional Results Summarized
Conjunction Analysis Findings and Average Activation Maps
Ohnishi et al. (2004) and Decety et al. (2008) are two of the known studies that have conducted fMRI studies on children (ages 7-13) regarding social constructs such as empathy and mentalizing. Both studies had similar findings to the present average activations maps, such as activations in the OFC, mPFC, STS, and TPJ regions.
We are in agreement with the authors in suggesting that these activations are indicative of
‘social brain’ mechanisms being established in early childhood.
Similar results are reported in the existing adult literature. Greene et al.
(2004) and Moll et al., (2002, 2007) had very similar studies to the studies presented here. Greene et al (2004) compared moral dilemmas on emotionality and the more personal emotional moral dilemmas recruited the mPFC, STS and posterior cingulate more readily than the less emotional, impersonal moral dilemmas. We also observed significant mPFC and STS activation in all the moral tasks presented, and posterior cingulate in the MJ and Agency conditions, suggesting an emotional element across studies. Within our results, though, we do see slight differences between tasks involving these regions suggesting the degree of emotional component recruitment may reflect the
173 slight differences between social moral tasks. For example, heightened mPFC and STS activation was observed for the Self-Agency condition in comparison to Other-Agency condition, which is more similar in theory to Greene’s more ‘personal’ moral condition.
Additionally, in a paired t-test (p< 0.01) between the Social Emotion and Moral judgment conditions, a small cluster in the left STS was found only in the Social Emotion task, supporting other studies suggesting that this region can be further differentiated by function (Saxe 2006), and perhaps serves an emotional attributional purpose. Moll et al.
(2002) conducted a very similar study to the MJ (Rule-based)/Agency studies in an adult sample in that he investigated judgments to simple moral statements compared to non- moral factual judgments. Our study differed in the further investigation of the division of agency, self and other, and the use of children and adolescent participants instead of adult participants. Despite these minor differences, a very similar network to Moll et al.’s study was found with the exclusion of mOFC, which was not detected in any of our studies. Moral judgments compared to non-moral factual judgments predominantly activated the frontal polar PFC and mPFC, which was found in all of the present studies.
Likewise, Moll et al. (2007) conducted a study similar to the SE study and found similar results not only to the SE study but to the MJ and Agency studies as well, such as activation in the mPFC, STS, LOFC, and anterior temporal cortex.
Regardless of adult or child study, or the particular social cognitive or social emotional construct investigated, polar PFC, mPFC, TPJ/STS, medial precuneus/posterior cingulate, and temporal polar regions are consistently recruited for processing, suggesting these regions are involved in a wide array of social processes.
The shared activations between the MJ, SE, and Agency studies are consistent with this
174 forthcoming social and/or moral research in outlining a dedicated neural basis for social moral processing. This dedicated neural basis observed in the CA, will be discussed throughout the remainder of the discussion.
MJ vs. SE and SE vs. MJ summary and analysis
In the MJ vs. SE paired-tests, several areas of the social brain were identified to be significantly more activated by the moral judgment statements and responses than by the passive reading/imagining of social moral emotional stimuli. Large associative and conceptual knowledge areas were recruited. The posterior cingulate was most robustly activated, followed by the ACC and angular gyrus. The PCC has been shown to function in episodic memory retrieval, and “feeling state” representations
(Calabrese 1996; Breen, Caine et al. 2001; Harenski and Hamann 2006). The ACC is known to be involved in conflict monitoring and induction of emotion in behavior
(Devinsky, Morrell et al. 1995; Botvinick, Braver et al. 2001). Lastly, one of the relevant functions of the angular gyrus is in abstract reasoning (Ramachandran 2004).
Collectively, these functions play crucial roles in decision-making and seem to be especially recruited for the social moral processing necessary for such explicit decisions.
The lack of frontal activation in the MJ vs. SE contrast may be due to areas of activation subserving both processes (MJ and SE) as indicated in the CA, such as the mPFC, that is recruited for social information processing in the ToM network. DLPFC and OFC activation were expected to survive significant thresholds in this MJ vs. SE contrast (OFC did survive p<0.01 threshold). Although these activations were not present in the paired
175 t-test, they were significantly activated in the MJ average activation map, but not in the
SE average activation map. Based on prior research, we suggest that these regions are especially important for affective working memory (Perlstein, Elbert et al. 2002; Mikels,
Reuter-Lorenz et al. 2008). Perhaps affective memory is used to catalogue and represent the social, moral, and/or emotional information along with associated rules for advantageous decision-making. Due to the MJ vs. SE contrast not yielding these activations, we can assume that the SE may use these regions, but to a lesser extent than explicit judgments. We suggest that implicit judgments may have been occurring in the
SE condition even though no response was required.
In the SE vs. MJ contrast, we expected to see significantly more subcortical/limbic activation, because of the function of these regions in emotional experience and visero-endocrine regulations that are essential for social-emotional related phenomenon such as social bonding, reward, depression, and altruistic decisions (Moll, de Oliveira-Souza et al. 2007). A PET study conducted by Lane et al. (1997) compared activations between pleasant and unpleasant emotional pictures from the IAPS
(International Affective Picture System) to neutral pictures, and found thalamus, hypothalamus, MB, PFC, and head of caudate activations. The lack of significant activation in these areas in the SE vs. MJ paired t-test as well as the average activation maps for the SE condition suggest one or more of the following: 1) that all the conditions in the present study equally recruit these more emotional regions (which most likely is not the case since the average activation maps did not show significant activation in these areas when compared to baseline conditions), 2) that these emotional regions were activated in the baseline conditions of each separate condition (which is more likely the
176 case due to the uncomfortable stimulating nature of the scanning environment), and/or 3) the fact that the situations are pseudo-social and imagining them does not substitute for real situations that may activate these regions. Although the collective SE did not show significant subcortical activation in average activation maps or when compared to the MJ conditions, activations were observed in sub-social emotion analyses, such as lenticular nucleus activation in the pro vs. antisocial condition, which is a subcortical structure demonstrated by other studies to be involved in moral judgments (Moll, Eslinger et al.
2001). The other various subcortical activations were all seen in the MJ conditions.
Significant caudate and thalamic activation were observed in the Ambiguous moral judgments. These regions and various pontine nuclei were also significantly active in the
Ambiguous vs. Rule-based condition. Because of the probable emotional components involved in moral stimuli of any kind, including moral judgments, and the nature of the ambiguous statements and associated activations, we posit that these judgments demand more emotional resources to guide-decision-making.
Now that the post-hoc analyses have been briefly summarized, it is necessary to expound on these findings in the broader scope of the cross-sectional activation maps. For clarity purposes, the next section is organized into anterior and posterior sections based on regional brain activations identified across subjects and conditions.
177 Anterior activations
As hypothesized, and supported by the results of the presented studies, the
PFC is foundational to social moral processing. In Eslinger et al.’s (2004) review of ten cases studies discussed throughout this dissertation, gross social and moral behavioral changes result from brain damage to this area. The most profound social deficits occurred in either unilateral or bilateral damage to the frontal pole, OFC, and the MPFC.
Eslinger also noted that the core deficits were in social cognition, social learning, and fluid intelligence. Interestingly, crystallized intelligence was often spared, an idea supported by Bar-On’s research on emotional and social intelligences (Bar-On, Tranel et al. 2003). Fluid intelligence, on the other hand is ‘malleable’ in a sense and can be adapted and modified by external sources. This intelligence and the associated flexible adaptive behavior is crucial to successfully interacting with the dynamic social world.
The diversified PFC regions enable and subserve these interactions. Cases, such as the ones presented in Eslinger’s review, demonstrate that these developing PFC regions enable the capability of transcending basic stages of social moral development, or concrete, egocentric, externally guided patterns of thinking, reasoning, and behavior.
As mentioned in the introduction, sophistication and higher order cognition involved in social moral behavior is speculated to be largely due to the human
FPC expansion in humans compared to other primates. This region was robustly activated in all studies as shown by the CA. Badre et al. (2007) investigated PFC hierarchical organization by manipulating different tasks and found that the frontal polar cortex was most active when the subjects response was contextually-based. This
178 prominent activation cluster provides further evidence that the PFC, and more specifically the polar medial PFC, plays a critical role in the interactions and decision- making involved in dynamic social contexts. Furthermore, this commonly activated region extended into and included the mPFC, which also plays a critical role in these contexts as it has been shown to be involved in the integration of emotion into decision- making and planning (Damasio 1994), ToM (Castelli, Happe et al. 2000; Saxe and
Kanwisher 2003), personal and impersonal moral judgments (Greene, Sommerville et al.
2001), passive viewing of moral pictures (Moll, de Oliveira-Souza et al. 2002), and making judgments based on empathy and forgiveness (Farrow, Zheng et al. 2001).
In the MJ vs. SE paired t-test discussion, the DLPFC was hypothesized because of the hypothesis that it would survive significant thresholds. As mentioned, it was activated in the MJ average activation map and because of its known working memory function, was speculated to be involved in affective working memory. Another important finding was the most robust activation of this region found in the Ambiguous average activation map. Moreover, the behavioral data showed that the longest reaction times were in response to the moral ambiguous statements in the Ambiguous condition, suggesting a correlation between task difficulty, ambiguity, and number of social moral rules and emotional components represented.
Although DLPFC activation has been observed in social moral related tasks, particularly when difficulty is high, OFC activation is more consistently observed in the social moral research literature. As mentioned previously, due to the observed activations in the MJ condition, we thought the OFC in conjunction with the DLPFC played a role in affective working memory. Other functions known to this region are in
179 appraising social-emotional stimuli, self-regulation, guiding socially appropriate and goal-directed behavior, and rapid-reversal learning (Bechara, Damasio et al. 2000;
Damasio, Grabowski et al. 2000; Kringelbach and Rolls 2003). Within the MJ condition, the Ambiguous had significantly more LOFC activation than the Rule-based condition suggesting the sensitivity of this region to the demand of resources necessary to guide decision-making. It is important to note that extensive reciprocal connections exist between the OFC and amygdala (Ghashghaei and Barbas 2002; Kondo, Saleem et al.
2003) and are critical for the linkage of sensory representations, value tagging, and subsequent social judgments of stimuli. In a sense, the OFC seems to be analogous to the vmPFC and its well-established role in representing affective social representations for the purpose of guiding decision-making, as discussed in Damasio’s somatic marker hypothesis (Damasio et al., 1990). As might be expected, both the OFC and vmPFC are robustly activated in the Ambiguous condition (p < 0.001). Not surprising, like the
DLPFC, greater OFC and vmPFC activation seems to be related to longer reaction times as more resources and affective input are recruited to guide decision-making.
Another interconnected network involving the OFC is between the OFC, anterior temporal poles, and the ACC (which all share connections with the amygdala)
(Kondo, Saleem et al. 2003). This network is thought to play an important rule in the recall of episodic memories and the generation of associated emotions. Bilateral anterior temporal pole activation was observed in the CA. The ACC is observed in the MJ condition and in the MJ vs. SE paired t-test, indicating that more recall, or episodic memory retrieval, is involved with the decision-making tasks, such as in the Ambiguous and Rule-Based conditions, and even more so when more resources have to be recruited
180 for difficult decision-making, as seen in the Ambiguous condition. Additionally, researchers speculate that as one evaluates the affective significance of the situation, the
ACC helps in directing attention and exploratory behavior towards salient stimuli and outlining a plan of action in response to an event (Devinsky, Morrell et al. 1995). Other studies have also shown a conflict-monitoring function of this region and a general involvement in social emotional regulation (Lane, Reiman et al. 1998; Berthoz, Artiges et al. 2002). The OFC, ACC, and temporal pole network seems to be activated selectively within each study and most robustly in tasks that require attention needed for goal- oriented behavior and memory recall needed for an explicit decision to be executed.
Fitting nicely with the present activation patterns, Bachevalier & Meunier
(2005) suggest that these activations (OFC, temporal poles, ACC), and the amygdala and the mPFC are part of a system important for maintaining intraspecific social bonding.
We are observing these convoluted networks and regions to be intricately and selectively involved as well as the degree of involvement depending on the variations of the social moral processing recruited for each condition.
Posterior Activations
For the most part, posterior activation was more prevalent in the SE tasks.
The first step of social moral processing is the perception of social signals by posterior structures such as the FFA and the TPJ/STS. The FFA and TPJ/STS process static faces to make a coherent picture for identification purposes and evaluate dynamic changes in faces such as expression and gaze shifting, respectively. The TPJ/STS region, a
181 convergent zone of perceptual information processing, is thought to integrate ventral and dorsal visual processing streams (shape/object and motion) of socially meaningful stimuli
(Adolphs 2003). These two regions as well as other higher-order associative occipital- temporal cortices are an interconnected system that together yield an initial representation of socially relevant information. Fusiform activation was present in the SE condition, but not in the MJ or Agency conditions. Additionally, the extrastriate cortex and the cerebellum were activated in the SE tasks and not the MJ and Agency tasks. The fusiform and cerebellar activations suggest that a higher degree of emotional intensity may require more discriminatory processing, and/or the nature of the task that requires emotional mental imagery may influence these activations. Reinforcing the validity of the study at hand, one of these convergent zones, the L STS was a robustly activated region in Agency, SE, and MJ average activation maps, and the most robust activation in the CA. On another note, Harenski & Hamman (2006) conducted a study showing that L
STS activation was present after contrasting moral social emotional stimuli to the non- moral social emotional stimuli, suggesting a strict moral role for this region.
Another activation common among all conditions as shown in the CA was the medial precuneus, which research has shown to be involved in empathy, episodic memory retrieval, mental imagery, and ToM (Farrow, Zheng et al. 2001; Gobbini,
Koralek et al. 2007). Although the precuneus and posterior cingulate are often activated together, as presented in select studies and in some conditions in the current research, there seems to be distinct functions. Some researchers have grouped this medial precuneus activation and related functions with the posterior cingulate activation (Greene and Haidt 2002; Gobbini, Koralek et al. 2007). In agreement with the notion of
182 differentiated functions pertaining to this region, we are seeing medial precuneus but not posterior cingulate activation in the SE condition. Moreover, posterior cingulate survived significant thresholds in MJ when compared to SE in a paired t-test. The Harenski et al.
(2006) study previously mentioned, found one structure to be strictly ‘moral’ when comparing moral and non-moral social emotional stimuli activation—the posterior cingulate. Research suggests that this region plays a role in representing a subjective
‘feeling state’ and episodic memory. We have already discussed the episodic memory retrieval network involving the OFC and how this was more activated in the MJ condition in comparison to the SE condition. The subjective ‘feeling state’ is a representational emotional pattern that is speculated to help guide decision-making as (Maddock 1999;
Damasio, Grabowski et al. 2000). Greene et al. (2004) found in comparing personal vs. impersonal moral dilemmas. In support of this more ‘subjective feeling state’ activation, the posterior cingulate was also activated in the Self-Agency condition and not in the
Other-Agency condition. It seems then that this region is involved in decision- making/explicit judgments, and more specifically, in more personal judgments that may possess a more affective component. On the contrary, other social moral studies have not identified this structure. Lastly, although we have demonstrated here that a functional differentiation exists in the medial precuneus/posterior cingulate region, further investigation needs to be conducted to identify these functions.
Although surprised at the lack of posterior cingulate in the SE condition considering its affective role, other structures, such as the insula and somatosensory gyri are also known to be involved in representing subjective ‘feeling states’ and were observed in the SE task. Bilateral somatosensory (postcentral gyrus), and paracentral
183 gyrus activation was observed in the Prosocial vs. Antisocial contrast. Furthermore, these structures have implications in empathy related-constructs such as ‘mirror system’ components and in the attribution of emotion and personality (Heberlein 2002). The
‘feeling state’ activation differentiations between and within the MJ and SE conditions suggest that states may be generated by partially distinguishable networks recruiting the cognitive or affective representations needed for the task at hand.
3) Developmental results summarized
PFC and other higher-order associative areas continue to develop in adolescence
(Gogtay, Giedd et al. 2004), evidenced by the social and behavioral changes and preferences observed in this age range. In support of this claim, we found PFC areas, such as the supplementary motor, DLPFC, and frontal polar cortex, and higher-order associative areas, such as the angular gyrus to increase with age in the MJ positive age regression analysis. Although none of these areas increased with age in the SE condition, higher-order cortices, such as convergent centers parieto-occipital and temporo-occipital, decreased with age. The Agency conditions had no detected significant development- related activations. These findings further highlight the differences between social moral processing networks, the establishment of networks subserving relevant functions, and the refinement that continues throughout childhood and adolescence.
As mentioned previously, one pivotal structure to human morality/sociality is the frontal polar PFC and we see this region activated across all tasks. We also see this
184 region become more activated as a function of age in the MJ task. We attribute this finding to the fact that in the MJ condition, a response/decision was required by the subjects, whereas a response was not required for the SE task. Additionally, a more involved interaction (explicit decision-making) with the external social environment demands the higher-order functions associated with this region. In essence, this finding implies that as decisions arise, and the underlying affective and cognitive networks become integrated and efficient throughout this age group, decisions rely more heavily on components derived from both systems, and thus are controlled by a fully informed executor.
Whereas we did not find robust limbic/subcortical activation in the SE average activation maps as hypothesized, activations in these regions were present in our developmental analysis. Amygdalar, hippocampal activations increased with age in the
Social Emotion condition (p<0.05), and the Prosocial condition (p<0.005). Interestingly, these activations decreased as a function of age in the Rule-based condition. Moreover, a structure important for the motor control of emotions, the caudate, increased with age in the SE condition. We posit that these findings are indicative of the increased moral sensitivity that is known to increase with age (Kohlberg 1964; Gibbs 2003; Hoffman
2000). Supporting this notion are the emotion-related activations, such as the ACC, caudate, and insula, that were activated in the Ambiguous positive age regression analysis. As children age and subsequently go through extensive periods of learning and socialization, children become more adept at recognizing when social rules and regulations are upheld and broken, and simulating the feelings of others during these events. In support of these processes, Eisenberg et al. (2005) found that personal distress,
185 helping, and perspective-taking increased with age. Also in support of these activations is a finding by Davidson (2004) showing that the hippocampus is involved in emotional regulation within specific contexts. Hippocampal activation increasing with age as observed in the present study, demonstrates the behavioral research-supported notion that the ability to regulate emotions within the social environment also increases with age.
On the contrary, as children become increasingly aware of the moral boundaries placed on themselves and others, these moral rules and regulations are internalized and become automatic to ones interaction with others. Due to the simplistic basic nature of the Rule- based statements, we suspect this internalization of rules in the form of an automatic appraisal process to have occurred, and were not surprised to see limbic activation decrease as a function of age. In summary, as children age and are more aware of social rules, and acquire appropriate contextual event knowledge, they recognize and become more sensitive to conflicting rules (Nucci 1991) and the social implications of these rules to self and others.
One last developmental highlight was found in the cerebellum. We see cerebellar activity in the MJ positive age regression. Ohnishi et al.’s (2004) study of mentalizing in children recruited the cerebellum. In agreement with other studies, they suggest the cerebellum plays an important role in mentalizing (Brunet, Sarfati et al. 2000;
Calarge, Andreasen et al. 2003). Other studies have reported an emotional role for this region. Both of these designated functions play a role in the development of social moral decision-making, and therefore may explain the cerebellar activation increasing with age.
It is important to note, however, that the cerebellum seems to be involved selectively in social moral processing. For example, it is recruited in the Other vs. Self Agency
186 contrast and in the SE average activation map, but is not age-dependent in these tasks as seen in the MJ task. Futhermore, L and R cerebellar regions were recruited selectively.
The findings in the current research suggest that the cerebellum is increasingly recruited with age in decision-making tasks that include a higher degree of emotion, and that it is steadily recruited for ‘other’ processing and emotional imagery. Future studies will need to be conducted to further delineate the precise roles played by regions of the cerebellum.
In summary, the developmental findings suggest that more engaging decision-making tasks, such as the MJ task, continue to benefit from the integration of cognitive and affective systems as children age, as structures important for long-term goals, planning, and plan execution become more recruited with age. Cognitive and affective integration is also beneficial in social emotional expression and social and emotional intelligence which motivate and guide moral behavior, as we see limbic and motor-emotional activations in regions such as the hippocampus/amygdala, and caudate increase with age.
4) Highlights
After collectively evaluating the cross-sectional analyses, two themes worthy of highlighting were evident, ToM and language, and will be discussed below.
187 Theory of Mind
The average activation maps of our conditions of Agency, Social
Emotions, and Moral Judgments, were subserved by a common neural network, as represented in the CA analysis. This pattern of activation, including the mPFC, temporal poles, TPJ/STS, and medial precuneus regions has recently been recognized as the ‘ToM network.’ Intense research is currently ongoing in the investigation of this network and its social implication (Frith and Frith 2003; Gallagher and Frith 2003; Saxe and
Kanwisher 2003; Saxe and Wexler 2005; Young, Cushman et al. 2007). The behavioral
ToM phenomena, or second order representation, was touched on in the introduction and sporadically assigned to certain structures throughout the preceding chapters, but further emphasis will now be placed on the underlying neural network because of its clear role in the presented studies, or more precisely, social moral processing.
The ToM network is thought to be established around the age of 5-
6 (Flavell 1999) as children begin to engage in certain behaviors such as lying, indicating they understand that others have beliefs different than their own. The ToM network allows for self-other simulation and shared representations for analogical reasoning that is pivotal in the understanding of others and largely contributes to healthy social interaction (Adolphs 2003; Decety and Sommerville 2003; Decety and Grezes 2006).
Although this network is established in early childhood, it continues to be refined as cognitive and affective systems become more intertwined and social rules and values are internalized.
188 Vicarious emotional arousal or distress at someone else’s distress, also classified as ‘simulation theory’, is thought to play a key role in the ToM network, which is the forerunner of empathy, sympathy, and perspective-taking. These processes are purposeful in promoting and motivating prosocial and altruistic behavior (Batson
1991; Eisenberg 1998; Hoffman 2000; Decety and Meyer 2008). Another proposed key player in ToM, ‘theory theory’, as outlined in previous chapters, is the ability to perceive and build a cognitive framework of the external world based on learning and to use this framework to understand the mental states of others. As stated previously, the cognitive and affective mechanisms comprising these theories explain how humans understand others mental and emotional states. These other- focused behaviors, which lead to prosocial behaviors such as empathy and perspective-taking, continue to develop over adolescence (Selman 1980; Eisenberg and Miller 1987) and are agreed upon across cultural and ethnic groups worldwide to be important markers for moral maturity (Arnett
2003; Galambos, Barker et al. 2003).
Although this isolated network appears in the CA, it is also almost exclusively activated in the Self-Agency and Other-Agency tasks. The ToM network is recruited to a much higher degree (FWE p<0.05) in the Ambiguous condition.
Additionally, the Ambiguous condition displayed other pivotal structures in social moral processing such as the ACC, supplementary motor, OFC and DLPFC. Likewise, the SE condition also activated the ToM network with additional activations in the bilateral middle temporal, lingual, cerebellar, and fusiform regions. As discussed, the foundational ToM network is activated in all conditions, however, the degree of the
189 recruitment of this network, and additional resources needed for social moral processing seems to depend on the cognitive and affective demands pertaining to the task.
Research comparing mental causality to physical causality (i.e. false belief task vs. rusting or melting process), and mental representation to physical representations (representing belief of another person vs. representing belief of physical characteristic), found the TPJ to be activated, demonstrating its preferable role in ToM abilities (Saxe and Kanwisher 2003). An adjacent region to the TPJ, the STS, has been shown to be activated by similar stimuli (Haxby, Hoffman et al. 2000; Pelphrey,
Singerman et al. 2003; Saxe, Xiao et al. 2004) that are purposeful in mental belief attribution, such as the presence, movement, and intentional actions of another person, reciprocal imitation, and reasoning about the physical and logical reasoning of another agent. However, Saxe et al., claim that the STS play more of a precursor role in ToM whereas the TPJ region is more at its core (Saxe 2006). Research demonstrates a kind of spectrum of recruitment indicating more robustness as the belief attribution becomes more complicated, as seen in false belief attribution compared to observing intentional actions (Saxe and Kanwisher 2003; Saxe and Wexler 2005). In support of this spectrum,
Ohnishi et al. (2004) suggests that ToM (as seen in humans) has its bases in the detection of agency and animacy and the inference of intentions from these perceptions, and that this information is processed by the fusiform and STS. Regardless of recruitment demand, these structures are crucial to ToM processing because the role they play in the convergence of dorsal and ventral processing streams that relay information not only of relative spatial location and visualization of animate body parts, but also the
190 identification of social cues concerning those movements, such as agency, intentionality, and belief attribution.
The functions of the mPFC have been discussed at length and include the representation of emotions needed for social decision making and planning
(Greene and Haidt 2002), goal-oriented behavior, prospective behavior, and more generally, social moral processing. Like the TPJ and STS, the mPFC is also activated in
ToM related tasks, such as mentalizing, empathy, and false belief attributions (Shamay-
Tsoory, Lester et al. 2005; Saxe, Schulz et al. 2006).
The temporal poles are not emphasized as much as the other more prominent ToM structures, but have been shown to be active in ToM tasks in several studies. Zahn et al. (2007) has shown that this region is involved in semantic-memory representation and processing, which possibly further processes the information fed forward by more posterior regions such as the STS/TPJ and PCC. It also functions to integrate internal and external information (Moran, Mufson et al. 1987; Gloor 1997) which similar in function to another ToM anterior structure, the mPFC.
Although all the ToM regions subserve behaviors related to ToM, such as mentalizing, false belief tasks, and intentional actions, specializations in function, as mentioned, exist within this network. For example, in a ‘paper, rock, scissor’ game played against a computer game or against another human were compared, the mPFC was robustly more activated than the TPJ when playing against the human. It is speculated that the mPFC has an affective and interactive/executive component whereas the TPJ is strictly cognitive in that it processes information to send downstream for interactive/executive purposes (McCabe, Houser et al. 2001; Gallagher, Jack et al. 2002).
191 Another example is demonstrated by Saxe again between the R and L LTPJ. R TPJ seems to more robustly recruited in higher-order ToM tasks than the L TPJ. In conjunction with this speculation, the L TPJ and PCC, compared to the other ToM regions, were activated when geographic-social background information was given about a protagonist. Saxe (2006) suggests that these regions may be activated in anticipation of needing to reason about mental states, in forming an impression of the personality, or in retrieving mental state candidates for this character from long-term memory. Although the ToM network was observed in the CA, the LTPJ was the most prominent activation, which fits nicely with the proposed function of this region. The stimuli used in the present studies required the subjects to retrieve long-term memories concerning previous situation and/or appropriate social rules and gather information about the situation as they mentally visualized the scenario and prepare to make an explicit or implicit judgment.
A final point regarding the ToM network is that the same structures, excluding the temporal poles, are posited to comprise what is known as the
‘default network’ of the brain (Shulman 1997; Buckner, Andrews-Hanna et al. 2008).
Although the two theories are separate, there seems to be extensive overlap. The default network is thought to subserve self-awareness or consciousness and is more active when having higher levels of self-focus or awareness as seen in studies where making judgments about one’s own or others mental or somatic state (Craik 1999; Fiset, Paus et al. 1999; Laureys, Lemaire et al. 1999; Kelley, Macrae et al. 2002; Mitchell, Banaji et al.
2005). One study showed that transcranial magnetic stimulation when applied to the medial parietal area interfered with accessing semantic knowledge about oneself (Lou,
Luber et al. 2004). Another study found that research participants showed increased
192 activation correlated to self-consciousness when they knew they were being watched by a camera (Gusnard, Akbudak et al. 2001). These studies suggest that this neural network provides an internal self-model that exhibits more activation when aspects of self are salient and less when they are irrelevant. These regions are also known to decrease with task difficulty and subject’s emotional state (Simpson 2001b; McKiernan, Kaufman et al.
2003). Not surprisingly, very similar trends are noted when ToM tasks are more relevant to a situation and when there are higher-order demands on this network. As demonstrated in the extensive overlap between the Self and Other Agency conditions, and previous research, self-awareness is the product of the realization of ‘other.’
Simulation becomes automatic with age as the underlying networks for self and other become indistinguishable.
Language
It is important to include a small section on language because of its key and often overlooked importance in social moral development. Although most of the activation across studies was bilateral, it was left hemisphere dominant. Each average activation map demonstrated this dominance, as did the CA. The SE vs. MJ paired t-test revealed only left activation in the PFC and STS. Likewise, the MJ positive age regression analysis revealed only left hemisphere activations. Lastly, areas particularly involved in language, such as the L Sylvian fissure and angular gyrus, increase with age in the MJ and Ambiguous conditions.
193 In adults, there is a left-hemispheric language-dependent predominance (Geschwind 1970), supported by fMRI studies investigating verbal fluency and semantic decision-making (Rueckert, Appollonio et al. 1994; Binder, Rao et al. 1995;
Demb, Desmond et al. 1995). The age in childhood in which hemispheric dominance in language is established is not well-understood but is thought to differ between children and adults because of continued physiologic development, particularly in the association cortices (Benson, Logan et al. 1996; Stapleton, Kiriakopoulos et al. 1997; Müller 1998).
As discussed at length in the introduction, association cortices, such as the PFC and STS undergo extensive myelination, synaptic reorganization, and pruning in the second decade of life as a result of maturation and learning. Researchers investigating language development posit that as the brain reorganization continues, brain activation for language becomes more localized. Language plays a major role in socialization, and hence morality. Because socialization, moral thinking, and moral behavior go through extensive development during childhood and adolescence, it is probable that language continues to develop throughout this age period as well (Mills 1994). An example related to this is a study conducted by Kleinhans et al. (2008) demonstrating atypical lateralization of language, a known characterization of autism, such as impaired language and social behavior.
Unlike ‘lower animals,’ primates, and to a much higher degree, human primates, do not have only perception-action behaviors, but are able to represent ideas and symbols in the form of language. For example, the basic response to food is approach, but people do not simply respond or react to their environment but bring standards and expectations (Carver 1990; Baumeister 1996; Beer, John et al. 2006).
194 Internal qualities need to be taken into account, which introduces an internal belief system, which includes standards and values that lend to an internal map or perception of world. More specifically, the perception-action transcendence of humans is essential in the social emotional and behavioral regulation that occurs when people exert control over their interpersonal behavior to match their internal standards and expectations instead of merely reacting to properties of environmental stimuli. Language symbolizes everything we experience and is able to integrate this information into our previously held world schema, modifying those schemas as necessary. These modifications play a key role in the extensive adaptive and flexible behavior observed in humans. It contributes to the developmental processes allowing us to interact in a dynamic socially complex world. In other words, language is pivotal for abstract thinking, both of which are essential for mature social moral behavior. Language is the highway for abstract thought, which is severely limited in autistics and deaf persons who are not fluent in sign language (Bailly,
Dechoulydelenclave et al. 2003; Leybaert and D'Hondt 2003). Not surprisingly, the angular gyrus, which plays a role in abstract thought, was activated in the MJ and
Ambiguous conditions.
As mentioned in the MJ discussion, egocentric speech is speculated to be left-hemisphere specific, as are complex emotional processing and expressions compared to basic emotion processing (Gainotti 2005). Lastly, it may be tempting to assume this hemispheric lateralization is the result of the written sentences/language and reading present in the current research. However, the baseline was similar to the experimental task but void of moral content. Furthermore, Moll et al. (2002) conducted a similar study fMRI study in adults comparing moral to factual statements. However, these statements
195 were presented audibly and continued to recruit stronger left hemisphere activation. In summary, this left-hemispheric dominance seems to be specific for social moral processing, allowing for self-awareness, introspection of goals, intentions, and values, and prospective memory to facilitate interactions with the external social world (Taylor
2008).
5) Models explaining summarized findings
The majority of social moral studies agree with Moll’s event feature emotion
(EFEC) framework outlined in the introduction, demonstrating that feature selection and perception, subserved by the anterior temporal lobe, and the STS/TPJ, event sequence knowledge, subserved by the OFC, DLPFC, and the frontal cortex, in the emotional motivation state, subserved by the amygdala, thalamus, ACC, and vmPFC (ventromedial prefrontal cortex) are essential for social moral behavior. The social moral emotional response and behavioral action or inhibition is the result of the dynamic integration of the affective and cognitive components of the EFEC framework (Damasio 1994; Rozin,
Lowery et al. 1999; Greene and Haidt 2002; Haidt 2003; Greene, Nystrom et al. 2004;
Young, Cushman et al. 2007; Zahn, Moll et al. 2007; Eslinger, Robinson-Long et al.
2009). Moll et al. (2005) describes binding mechanisms related to these processes, such as sequential, temporal and third-party binding linking various regions in the brain that represent different forms of knowledge in the PFC (Weingartner, Grafman et al. 1983), temporal binding among highly connected regions in the posterior cortex (Singer 2001),
196 and third party binding of anatomically loosely connected regions which results in formation of episodic memories (O'Reilly and Rudy 2000). This binding and integrating of social information to make a holistic coherent representation and/or expression is demonstrated by the diffuse activations spanning the brain, particularly in the frontal, parietal, and memory-related areas of the brain. These large-scale networks allow for powerful human capabilities such as symbolic language, syntax, future planning, episodic memory, and making complex inferences (Suddendorf 1999; Corballis 2003). Although each of these components is an important social construct, it is the integration and binding that makes for social moral emotions, judgments, and behavior (Yuill 1988;
Zelazo, Burack et al. 1996; Abell, Krams et al. 1999). As these systems bind information together, mature, and become more efficient in their processing during childhood and adolescence, higher-order behavioral manifestations are revealed, such as increased executive function in adolescence that instill a greater “top-down” modulation of activity on the more primitive subcortical regions (Yurgelun-Todd 2007). The binding and maturation that occurs over widespread areas of the brain is the culmination of cognitive and affective processing, evident in the complex social lives of humans.
Up to this point, the dedicated social moral network has been outlined and explained to exchange spatially distant information via binding mechanisms. The next step is to explain the way social moral information is processed. Eslinger et al. (2004) suggests two processing systems are involved: 1) an automatic or implicit processing system that involves the mPFC and OFC that feed forward an emotional response to the stimulus to more cognitive regions such as the DLPFC and polar cortex in a caudal- rostral fashion; the importance of the mPFC and OFC to social moral processing is
197 critical due to their role in the regulation of interpersonal relationships, social cooperation, moral behavior, and social aggression (Davidson, Jackson et al. 2000;
Greene and Haidt 2002) 2) this second system (DLPFC and polar cortex) is more slow and deliberate as it incorporates perspective-taking, judgments, sympathy/empathy, cost/benefit analyses between behavioral options, strategic planning, plan selection, and behavioral execution (Eslinger, Grattan et al. 1992; Grattan and Eslinger 1992; Eslinger
1996; Green 2001; Moll, de Oliveira-Souza et al. 2002; Moll, de Oliveira-Souza et al.
2003). Moll et al. (2002) support Eslinger’s theory of these streams of social moral processing in suggesting that OFC and mPFC with the STS and limbic-subcortical regions function to enable rapid and automatic appraisals of social moral emotional events which provide the foundation for the subsequent cognitive, motivational, and recursive social-emotional processing that is the bases for moral decision-making and behavior.
Thus far, we have demonstrated that feature selection, motivational state, and event sequence knowledge represent disparate regional and functional mechanisms and that these regions and functions are temporally bound and integrate information in social moral processing. Although recursive loops and reappraisals, as mentioned, frequently occur, the general flow of information is in a posterior to anterior direction and is purposeful in directing attention to and representing complex social stimuli involved and relaying episodic memories and associated emotional states to guide advantageous decision-making.
198 6) Limitations in the presented studies
The object of the study is to investigate social moral judgments and social moral emotions. Obviously, these happenings normally take place in a social environment where constant reading of intentions, goals, and other social cues are perceived, evaluated and subsequent contingent behavior is adjusted on a moment-to- moment basis. Due to the nature of the fMRI tasks, and the lack of real social interaction and reading of statements, our data could be a misrepresentation of actual neural networks responsible for Agency, MJ’s, and SE’s. Although, other imaging studies using different stimuli, different imaging methods, and more importantly, the brain lesion data are in agreement that the structures and activation patterns identified in the present study are valid.
One possible limitation was that the social emotion ‘fear’ was used in the
SE condition. Although, ‘fear’ was presented in a social situation, it is typically not included by the majority of researchers to be a ‘social emotion.’ To investigate if the inclusion of ‘fear’ had a negative influence on the SE average activation map, another one-sample t-test excluding fear and was conducted and similar results to the average activation map were found, suggesting it did not have a profound effect on the results generated.
A limitation that may have negatively influenced the Ambiguous activation was not having a ‘confusing’ or ambiguous baseline. The baseline used consisted of clearly right or wrong statements. The robustness of the DLPFC activation
199 in particular, because of its known role in the response to increased cognitive demand, may have been reduced if ambiguous baseline statements were included.
These relationships need to be further investigated and may not be comprehended completely unless investigated at multiple levels of analysis. fMRI is only one technique used for investigation, but neurorecording, neurostimulation, and genetic analyses are only a few of the other ways to provide a more complete understanding. In conjunction with this notion of gaining a more clear representation of the social brain, Saxe (2006) addresses the tendency for “error of reification”, which is the assumption that regions of interest refer to “chunks of cortex” in which all of the neurons in those regions are functionally homogenous. For the most part, current researchers have coarser-grain regions of interests. Typically, there is a finer grain of structure within these larger regions, which will be discovered with the use of stronger
MRI magnets and associated better technology which will be available in the near future.
An example of the current limitations of inaccuracy in the present study is the STS/TPJ region. Although commonly ‘lumped’ together as one region, there is no doubt that this region will be functionally differentiated (Saxe, Carey et al. 2004). Although we are progressing rapidly in our discoveries of the ‘social brain’, considering our technical limitations and often uni-level analyses, only the surface has been unveiled, leading to an exciting future in this area. The advancement of technology, the accessibility of these technologies, and increased collaboration, will inevitably lead to the elimination of partial representations of data.
200 7) Importance of the presented research
An extensive amount of literature demonstrates a directly proportional relationship between social interaction and psychological and physical functioning
(Bernston 2006). A longitudinal study nicely demonstrates this relationship by comparing an anxiolytic drug to a placebo. The researchers observed a significant increase in the effect of the placebo over time. It was suggested that this was the result of more human touch points and social interaction between the caregiver and the subject as a result of improvement in study regulations (Marci 2006). Related to this study, behavioral therapeutic interventions have proven successful at any age and highlight neural plasticity occurrence in the brain. Davidson et al. (2003) conducted a study that encapsulates these ideas. An eight week mindfulness meditation study was evaluated via
EEG and immune function measures. After the eight week period, a significant increase in left anterior activation, which has been posited in positive affect, was observed. After an influenza vaccine was administered, antibody titers were significantly higher than controls. Additionally, the most robust changes in brain activation correlated with highest level of antibody titers. Moreover, cognitive behavioral therapy changed regional activations similar to medicinal therapies. Clearly, physiological functioning, whether peripherally or centrally, can change due to degrees of sociality or applied cognitive strategies. Both of these observations, are important in the present research, because finding a template in earlier stages of social moral processing is only informative if it can be manipulated to produce optimal social functioning.
201 Bar-on et al. (2003) showed that emotional intelligence and the ability to exercise personal judgments in decision making were highly correlated. They also discussed the high correlation between emotional and social intelligence and that correlation to human performance, suggesting that these intelligences may be a better indicator of performance and success in life more than IQ. Discovering the link between emotional and social aptitude and quality of life and well-being has and will continue to encourage research in the present areas of study.
A final reason the present research is important is the relatively modest number of neuroscientific studies that have observed these phenomena. Moreover, although a small number of adult studies have been conducted on the neural substrates underlying cognition and emotion involved in moral emotions, to our knowledge, no studies have directly investigated these substrates in normal developing children. Even related research studies to our current research, such as empathy to others in pain and the mirror system in watching another’s motor movements, are very limited in their study in children (Ohnishi et al., 2004; Decety et al., 2008) and have only researched a limited age range in childhood and hence have not investigated development.
8) Future questions and directions
By far, the most important application for this research is the establishment of a template for the social moral emotional brain in typical children and adolescents and the dynamics of that template/network with age. The formulation of this template is the first
202 major step towards early detection and intervention in individuals with deficiencies or a disorder in social moral emotional processing. The atypical neural activations that exhibited altered social, moral, and/or behavioral ramifications as discussed in the introduction, seen in disorders such as ADHD, psychopathology, antisocial personality disorder, William Syndrome, autism, were regions detected in our sample to be “normal.”
These atypical populations will benefit greatly as we continue these studies and incorporate appropriate detection and intervention procedures.
Going a step further, developmental theorists posit that if children that experience empathy and take action to self-regulate emotions are more likely to engage in prosocial behaviors and help in negating antisocial aggressive acts towards others (Zahn-Waxler
1990). Early education, training, and intervention resulting from the developmental research, is critical for the promotion of these behaviors.
The future of what this research has to offer is endless. It has even been speculated that this kind of research, before the century is over, will present major ethical issues on whether genetic engineering should be used to create the optimal social brain
(Trancredi 2005).
Another future direction for this research is related to what Davidson (2004) refers to as affective style, which is more of a personal or individual approach to studying emotions. According to Davidson, affective styles are consistently different between persons in their threshold to respond, emotional reactivity, duration, and regulation, and these differences play a crucial role in shaping variations in well-being. Affective style is most pronounced and extreme in humans and therefore needs more intermediate levels of investigation that is not so categorical. While Davidson focuses on only the emotional
203 domain, we posit that social and moral differences are also widespread and that perhaps profile styles should be evaluated in these areas as well. One example of those measures is interpersonal sensitivity, closely related to what Moll et al. (2002) term moral sensitivity, and is defined as the ‘ability to perceive and respond with care to the internal states of another. Future research will take into account these differences in styles and sensitivities and if needed, intervention can be tailored to an individual. This research will also need to be purposeful in understanding the antecedents of those states, and predicting the subsequent events that will result.
Although the present research discussed thus far has concentrated on normal populations and those that have deficiencies evidenced by social, moral, and/or emotional problems that are in some cases, dangerous to society, a group of person has not been mentioned. This group consists of those persons on the other side of the social moral and/or emotional spectrum—the moral exemplars (Moll, de Oliveira-Souza et al.
2003). Persons in this group, such as Jesus Christ, Mother Theresa, Gandhi, exhibit extreme prosocial altruistic behavior. Whereas as a dissociation exists between moral knowledge/values and judgments/behavior in psychopaths, moral exemplars make judgments and behave in a way, almost automatically, that is inseparable to their moral knowledge and values (Colby and Damon 1992).
Although not investigated in the present studies, the behavioral literature suggests gender differences in the processing of moral knowledge where females have more care/personal based orientations and males have more justice/impersonal orientations
(Gilligan 1977; Jaffee and Hyde 2000). Because of the relatively new neuroscientific study devoted to this area, these further delineations of male and female, although
204 assumed, have not been thoroughly investigated (Moll, de Oliveira-Souza et al. 2002).
Considering these assumed differences, future studies need to be conducted to reveal the neural underpinnings of these gender-based differences.
205
APPENDIX
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
206
! ! ! ! Controlled Semantic Semantic !"#$%&'( Controlled Oral Word Controlled Controlled Fluency Fluency +,%( -%./%0( 12./%/.%33( )*( Oral Word Association Oral Word Oral Word Raw Raw Semantic Semantic Association Scaled Association Association Score Scaled Fluency Fluency Raw Score Score Percentile Interpretation Total Score Percentile Interpretation ! ! ! ! ! ! ! ! ! ! "#! #$! %&'(! )*+,-! 45 14 91% Above Average 35 9 /70! 12(3&+(! "6! #7! 8(9&'(! )*+,-! 27 8 25% Average 41 12 740! 12(3&+(! "/! #4! 8(9&'(! <(=-! 34 11 63% Average 41 12 740! 12(3&+(! ".! #.! %&'(! )*+,-! 29 9 37% Average 53 17 550! FGH(''(I-! "4! #.! %&'(! )*+,-! 26 8 25% Average 51 16 5:0! FGH(''(I-! "$! #$! %&'(! )*+,-! 36 11 63% Average 39 11 $/0! 12(3&+(! "7! #4! 8(9&'(! )*+,-! 30 9 37% Average 45 13 :.0! 1J@2(!12(3&+(! ":! ##! 8(9&'(! )*+,-! 16 6 9% Below Average 31 10 4A0! 12(3&+(! "5! #A! 8(9&'(! )*+,-! 16 8 25% Average 41 15 540! 1J@2(!12(3&+(! "#A! #A! 8(9&'(! <(=-! 27 12 75% Average 26 6 50! K('@E!12(3&+(! "##! #/! %&'(! )*+,-! 26 9 37% Average 28 8 640! 12(3&+(! "#6! ##! 8(9&'(! )*+,-! 32 12 9% Below Average 41 14 5#0! 1J@2(!12(3&+(! "#/! #4! 8(9&'(! )*+,-! 30 9 37% Average 33 9 /70! 12(3&+(! "#.! #/! %&'(! )*+,-! 25 8 25% Average 30 9 /70! 12(3&+(! "#4! #$! 8(9&'(! )*+,-! 34 10 50% Average 32 8 640! 12(3&+(! "#$! #/! %&'(! )*+,-! 33 11 63% Average 44 14 5#0! 1J@2(!12(3&+(! "#7! 5! 8(9&'(! )*+,-! 26 6 9% Below Average 32 10 4A0! 12(3&+(! "#:! #7! %&'(! )*+,-! 26 7 16% Below Average 29 7 #$0! K('@E!12(3&+(! "#5! #4! 8(9&'(! )*+,-! 20 13 84% Above Average 35 13 :.0! 1J@2(!12(3&+(!
207
! ! ! ! ! ! ! ! ((((((((((17A%(B(57AA".='9(!7&=28(?%C2D=70(!&28%3( ! ?20E.(FA7'=7.28(G"7'=%.'( Subject Social ).D%.'709( ID Age Gender Handedness Competence Antisocial Behavior Social Social T- % Functioning T- % Functioning Raw Scaled Raw Score Rank Level Raw Score Rank Level EQ Score EQ Level "#! #$! %&'(! )*+,-! 117 47 33 Average 45 45 40 Average 75 112 High "6! #7! 8(9&'(! )*+,-! 131 53 55 Average 52 48 56 Average 72 104 Average "/! #4! 8(9&'(! <(=-! 125 50 44 Average 65 54 77 Average 71 102 Average ".! #.! %&'(! )*+,-! 98 38 13 At Risk 89 65 91 At Risk 63 89 Low "4! #.! %&'(! )*+,-! 120 48 37 Average 54 49 59 Average 72 107 Average "$! #$! %&'(! )*+,-! 149 62 92 High Functioning 41 42 24 Average 62 91 Average "7! #4! 8(9&'(! )*+,-! 132 53 55 Average 45 45 40 Average 76 113 High ":! ##! 8(9&'(! )*+,-! 134 56 67 Average 51 46 43 Average 65 95 Average "5! #A! 8(9&'(! )*+,-! 133 55 65 Average 38 41 16 Average 70 102 Average "#A! #A! 8(9&'(! <(=-! 136 57 72 Average 56 49 55 Average 58 94 Low "##! #/! %&'(! )*+,-! 122 49 40 Average 68 56 77 Average 65 94 Average "#6! ##! 8(9&'(! )*+,-! 145 60 85 High Functioning 37 40 11 Average 63 92 Average "#/! #4! 8(9&'(! )*+,-! 146 59 81 High Functioning 45 45 40 Average 63 93 Average "#.! #/! %&'(! )*+,-! 143 60 85 High Functioning 47 44 36 Average 64 92 Average "#4! #$! 8(9&'(! )*+,-! 144 58 78 Average 65 54 77 Average 63 89 Low "#$! #/! %&'(! )*+,-! 139 56 68 Average 38 42 22 Average 76 112 High "#7! 5! 8(9&'(! )*+,-! N/A N/A N/A N/A N/A N/A N/A N/A 73 108 High "#:! #7! %&'(! )*+,-! N/A N/A N/A N/A N/A N/A N/A N/A 73 107 High "#5! #4! 8(9&'(! )*+,-! N/A N/A N/A N/A N/A N/A N/A N/A 61 86 Low !
208
! ! ! 4)+H( 4)+H( 4)+H( !"#$%&'( 470/( 4E:*( 4)+H( 4)+H( 4)+H(
209
! Chapman- !"#$%&'( Cook +,%( -%./%0( 12./%/.%33( WRAT3 WRAT3 WRAT3 WRAT3 Speed of Ravens )*( Raw Absolute Standard Grade Reading (AB) Raw Score Score Score Score Raw Score Score ! ! ! ! ! ! ! ! "#! #$! %&'(! )*+,-! 45 520 101 HS 15 11 "6! #7! 8(9&'(! )*+,-! 42 514 95 HS 8 12 "/! #4! 8(9&'(! <(=-! 49 529 115 Post HS 20 12 ".! #.! %&'(! )*+,-! 40 511 99 8 9 11 "4! #.! %&'(! )*+,-! 42 514 103 HS 8 11 "$! #$! %&'(! )*+,-! 46 522 103 HS 15 12 "7! #4! 8(9&'(! )*+,-! 52 533 122 Post HS 21 11 ":! ##! 8(9&'(! )*+,-! 42 514 121 HS 6 12 "5! #A! 8(9&'(! )*+,-! 39 509 120 7 10 12 "#A! #A! 8(9&'(! <(=-! 37 505 108 6 7 N/A "##! #/! %&'(! )*+,-! 43 515 106 HS 10 N/A "#6! ##! 8(9&'(! )*+,-! 46 522 124 HS 18 11 "#/! #4! 8(9&'(! )*+,-! 50 530 115 Post HS N/A 11 "#.! #/! %&'(! )*+,-! 46 522 113 HS 19 11 "#4! #$! 8(9&'(! )*+,-! 54 537 120 Post HS 14 12 "#$! #/! %&'(! )*+,-! 43 515 106 HS N/A N/A "#7! 5! 8(9&'(! )*+,-! 44 517 133 HS 7 N/A "#:! #7! %&'(! )*+,-! 49 529 108 Post HS N/A N/A "#5! #4! 8(9&'(! )*+,-! 45 520 104 HS N/A N/A
210
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