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The Pennsylvania State University the Graduate School Department of Neuroscience 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&-"&!$5+& )+2./.",/&$,)&'()*!+,-/&6$/+)&",&.,-+#,$%&3#.,2.3%+/&$,)&-"&$2-&.,&$22"#)$,2+&7.-1& /(21&'()*!+,-/8&9"2.$%&+!"-.",/:&"#&!"#+&3#+2./+%4&!"#$%&+!"-.",/:&$#+&)+0.,+)&$/& ).00+#.,*&0#"!&6$/.2&+!"-.",/&.,&-1$-&-1+4&$#+&.,-#.,/.2$%%4&%.,5+)&-"&-1+&.,-+#+/-/&"#& 7+%0$#+&+.-1+#&"0&/"2.+-4&$/&$&71"%+&"#&"0&3+#/",/&"-1+#&-1$,&-1+&$*+,-8&&Based on 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
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