Theory of Mind and Empathy As Multidimensional Constructs Neurological Foundations

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Top Lang Disorders Vol. 34, No. 4, pp. 282–295 Copyright c 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins Theory of Mind and Empathy as Multidimensional Constructs Neurological Foundations

Jonathan Dvash and Simone G. Shamay-Tsoory

Empathy describes an individual’s ability to understand and feel the other. In this article, we review recent theoretical approaches to the study of empathy. Recent evidence supports 2 possible empathy systems: an emotional system and a cognitive system. These processes are served by separate, albeit interacting, brain networks. When a cognitive empathic response is generated, the theory of mind (ToM) network (i.e., medial prefrontal cortex, superior temporal sulcus, temporal poles) and the affective ToM network (mainly involving the ventromedial prefrontal cortex) are typically involved. In contrast, the emotional empathic response is driven mainly by simulation and involves regions that mediate emotional experiences (i.e., amygdala, insula). A decreased empathic response may be due to deﬁcits in mentalizing (cognitive ToM, affective ToM) or in simulation processing (emotional empathy), with these deﬁcits mediated by different neural systems. It is proposed that a balanced activation of these 2 networks is required for appropriate social behavior. Key words: emotion, empathy, inferior frontal gyrus, mirror neurons, simulation, theory of mind, ventromedial prefrontal cortex

NE of the core functions of individu- have provided evidence of the multidimen- O als living within a society is the attribu- sional nature of ToM. In this article, we review tion of mental states to others. This function, main approaches to the study of the neural ba- known as theory of mind (ToM) or “mental- sis of ToM and empathy (including tasks used izing” (Frith, 1999), enables an individual to to elicit them), describe the neurological un- understand or predict another person’s be- derpinnings for the multidimensional nature havior and to react accordingly. Much of the of ToM and empathy, and discuss these find- research on ToM has viewed it as a unitary ings in relation to clinical interventions. construct, focusing on cognitive mentalizing about others—thinking about the thoughts, ToM AND EMPATHY intentions, and beliefs of others. Technologi- cal advances in neuroscience enabling the in- The ability to infer the thoughts and feel- vestigation of neurophysiological functioning ings of others is critical for appropriate and ef- fective social interactions and discourse comprehension, but it is not sufficient. Belief un- Author Affiliations: Department of Special derstanding does not guarantee emotion un- Education, Bar Ilan University, Ramat Gan, Israel (Dr Dvash); and Department of Psychology, derstanding; emotion understanding does not University of Haifa, Haifa, Israel (Dr guarantee empathy; and empathy does not Shamay-Tsoory). guarantee sympathy as manifested by kind- Drs. Dvash and Shamay-Tsoory have indicated that ness to people (Davis & Stone, 2003). Hence, they have no financial and no nonfinancial relation- empathy is the link between knowing the ships to disclose. thoughts and feelings of others, experiencing Corresponding Author: Jonathan Dvash, PhD, De- partment of Special Education, School of Education, them, and responding to others in caring, sup- Bar Ilan University, Max ve-Anna Webb St, Ramat Gan portive ways. 52900, Israel ([email protected]). Theory of mind is part of a person’s DOI: 10.1097/TLD.0000000000000040 empathic ability, a broader term that also 282

encompasses the emotional aspect of infer- Broadly speaking, empathy refers to the ring and sharing the emotional experiences reactions of one individual to the observed of another. Empathy is a central theme in the experiences of another (Davis, 1994). Some psychological sciences, as well as in neuro- scholars view empathy as a cognitive process, science, and has become a prominent field of stressing the ability to engage in the cognitive research in recent years. Empathy describes process of adopting another individual’s psy- an individual’s ability to understand and feel chological perspective. This process, which the other. Because empathy links one’s feel- can be termed cognitive empathy (and when ings about the self to feelings about the other, including an inference on affective aspects it is a fundamental part of the social fabric can also be known as affective ToM or af- of emotion. In examining empathy and ToM, fective cognitive ToM), may be defined as an the natural focus of cognitive and psychody- active attempt by one person to get “inside” namic psychologists is on psychological pro- another’s mind or to approach someone men- cesses rather than on brain mechanisms. Yet, tally through a deliberate intellectual effort. recent experimental studies have shown that In other words, cognitive empathy describes impaired empathy is observed in both neuro- a situation in which the subject is an active logical and psychiatric populations, suggest- agent deliberately attempting to step outside ing that empathy may be mediated by dedi- the self and “into” the other’s experiences; it cated neural networks (Brothers, 1990). involves a cognitive recognition of the emo- Researchers and clinical personnel are ex- tions of others. This process may involve pressing increased concerns regarding “loss perspective taking (Eslinger, 1998) and ToM of empathy.” In Great Britain, Baron-Cohen (Shamay-Tsoory, Tomer, Goldsher, Berger, & (2011) published the book, Zero Degrees of Aharon-Peretz, 2004). It is thought to be de- Empathy, in which he describes patterns of pendent on several cognitive capacities, such ToM skills and empathy deficits in persons as cognitive flexibility and memory (Davis, with autism, Asperger’s syndrome, and a vari- 1994; Eslinger, 1998; Grattan, Bloomer, Ar- ety of psychiatric conditions.1 In the book, chambault, & Eslinger, 1994). Born for Love: Why Empathy Is Essential Other studies in the field have used a def- and Endangered, Perry and Szalavitz (2010) inition of empathy that showcases its affec- explain how empathy develops or is threat- tive aspects. Such studies refer to the ability ened as a result of genetics and social inter- to experience affective reactions to the ob- actions. The most recent version of the Diag- served experiences of others as “affective em- nostic and Statistical Manual of Mental Dis- pathy” (Davis, 1994). According to this view, orders, Fifth Edition (American Psychiatric empathy may be regarded as an emotional re- Association, 2013), added specifiers regard- action of the observer when perceiving that ing “callous-unemotional” behaviors to the di- another is experiencing or is about to expe- agnostic criteria for disruptive behavior dis- rience an emotion. There is, however, a criti- orders in children. These specifiers describe cal difference between cognitive empathy (af- behaviors associated with deficits in empa- fective cognitive ToM) and emotional or af- thy (e.g., callous disregard of the feelings of fective empathy. Whereas cognitive empathy others) and affective interpersonal ToM (e.g., involves cognitive understanding of another lack of remorse or guilt; shallow or deficient person’s perspective, emotional empathy in- affect). cludes appropriating these feelings, at least on a gross level (pleasant-unpleasant; Mehrabian & Epstein, 1972). Previously, it was argued that the various aspects of empathy are inter- 1In the United States, this book was published under the related and interact throughout development title, The Science of Evil: On Empathy and the Origins (Hoffman, 1978). Recent theories of empathy, of Guilt. however, have introduced multidimensional

(Davis, 1994) and integrative (Decety & Jack- eye gaze, Yoni’s facial expression, or the eye son, 2004; Preston & de Waal, 2002) mod- gaze and facial expression of the face to which els that bind several aspects of empathy and Yoni is referring. In the cognitive conditions, empathy-related behaviors. Considering this both Yoni’s facial expression and the verbal definition of empathy, it appears that affective cue are emotionally neutral, whereas in the empathy is the basis for cognitive empathic affective conditions, both cues provide af- ability. Furthermore, it appears that cognitive fective information (i.e., Yoni is thinking of empathy, as opposed to affective empathy, in- [cognitive condition] vs. Yoni loves [affec- volves creating a cognitive ToM regarding the tive condition]). That is, the cognitive condi- other’s mental and emotional states. tion requires understanding beliefs about the other’s beliefs and desires (Yoni is thinking INVESTIGATING ToM AND EMPATHY of the toy that ___ wants) whereas the affec- CONSTRUCTS tive condition involves understanding of one’s emotions with regard to the other’s emotions Evidence for the neural bases of multi- (Yoni loves the toy that ___ loves). The “Yoni” ple dimensions of ToM has come from sev- task has been used in studies of neurologi- eral sources: functional neuroimaging stud- cal (Shamay-Tsoory et al., 2007) and psychi- ies of neurotypical participants, patients atric populations (Shamay-Tsoory et al., 2007, with brain injuries or psychopathologies, 2010), as well as in a recent neuroimaging and children and adolescents with diagnosed study (Bodden et al., 2013). developmental disabilities such as autism. Shamay-Tsoory and colleagues (Shamay- Shamay-Tsoory and colleagues have published Tsoory et al., 2007; Shamay-Tsoory, Tomer, an extensive set of studies on the neu- & Aharon-Peretz, 2005) also have developed a roanatomical bases of cognitive and affec- variety of vignettes that require participants to tive ToM (e.g., Abu-Akel & Shamay-Tsoory, employ cognitive or affective ToM. For exam- 2011; Shamay-Tsoory & Aharon-Peretz, 2007; ple in a vignette involving cognitive sarcasm, Shamay-Tsoory, Harari, Aharon-Peretz, & Lev- Joe goes into the bank manager’s office and kovitz, 2010; Shamay-Tsoory, Tibi-Elhanany, cannot find anywhere to sit down because all & Aharon-Peretz, 2007). the chairs are occupied with documents and Considering the contrasts between these folders. Joe says to the bank manager, “Your two views of ToM, cognitive ToM involves office is so tidy!” Participants are asked, “Why thinking about thoughts, intentions, or be- did Joe say that? Did Joe think the office was liefs whereas affective ToM involves thinking tidy? Was the office tidy?” In a task involving about feelings. To elicit both aspects in neu- affective sarcasm, a father forgets to pick up roimaging studies, participants may be asked his son after school, leaving him in the rain for to judge mental or emotional states on the ba- some time. When the father and son finally get sis of verbal and eye gaze cues of a cartoon home, the mother says to the father, “You are figure (e.g., see Shamay-Tsoory & Aharon- such a good father.” Participants are asked, Peretz, 2007; Shamay-Tsoory et al., 2010). The “Why did mom say that? Did mom think dad task consists of showing a series of cartoon was a good father? Was dad a good father on outlines of a face (named “Yoni”) and four this occasion?” colored pictures of objects belonging to a Other types of tasks for neuroimaging inves- single category (e.g., fruits, animals), one in tigations have involved either self-referencing each corner of a computer screen. (One can (which can be considered intrapersonal ToM) view the materials at http://sans.haifa.ac.il/ or other-referencing (which can be con- Downloads.html.) The participant’s task is to sidered interpersonal ToM). For example, point to the image to which Yoni is referring Jenkins and Mitchell (2011) had partici- based on a sentence that appears at the top of pants evaluate adjectives for how they would the screen and available cues, such as Yoni’s describe either themselves or the then-current

president of the United States. Three dif- they discover it is filled with M & Ms. They ferent sets of adjectives were assessed, re- are then asked what they thought was in ferring to (a) stable personality traits (e.g., the box when they first saw it (intrapersonal in general, how brave?); (b) current mental cognitive ToM) and how they felt about what states (e.g., in the moment, how bored?); and they thought was in the box when they (c) stable physical attributes (e.g., physically, first saw it (intrapersonal affective ToM). how tall?). Kana, Klein, Klinger, Travers, and Performance on these interpersonal and Klinger (2013) had high-functioning adults intrapersonal ToM tasks was differentiated with autism and neurotypical adults make in typically developing children and children yes–no decision about whether visually pre- with autism and Asperger’s syndrome. sented adjectives (e.g., smart, unhappy)de- Empathy is sometimes measured with ques- scribed themselves (self-judgment) or their tionnaires such as the Interpersonal Reactiv- favorite teacher (other-judgment). In a sim- ity Index (Davis, 1983), which measures two ilar study, Lombardo et al. (2010) had neu- types of empathy—affective cognitive and af- rotypical adults make mental reflections about fective empathy. Affective cognitive items in- themselves or the Queen of England. On the volve perspective taking or the ability to trans- self-task, participants judged on a scale from pose oneself into fictional situations. The af- 1(not at all likely)to4(very likely) how fective empathy items tap persons’ feelings of likely they would be to agree personally with warmth, compassion, or concern for others or opinion questions (e.g., “How likely are You feelings of anxiety or discomfort from tense to think that keeping a diary is important?”). interpersonal settings. Examples of affective On the other task, the same mentalizing judg- cognitive items are “When I am reading an in- ments were made, except this time they were teresting story or novel I imagine how I would in reference to how likely the British Queen feel if the events in the story were happening would be to agree with opinion questions to me” or “I try to look at everybody’s side of (e.g., “How likely is the Queen to think that a disagreement before I make a decision.” Ex- keeping a diary is important?”). amples of affective empathy items are “I am of- Behavioral studies not employing func- ten quite touched by things that I see happen” tional imaging have shown that performance or “When I see someone being taken advan- on interpersonal and intrapersonal ToM tage of, I feel kind of protective toward them.” tasks can be disassociated—that is, children Studies employing these tasks with func- can perform differently on the two tasks. tional magnetic resonance imaging and tran- Lucariello and colleagues (Lucariello, Durand, scranial magnetic stimulation (TMS) have pro- & Yarnell, 2007; Tine & Lucariello, 2012) vided evidence that ToM is differentiated into compared development of interpersonal and cognitive and affective dimension ToM (think- intrapersonal ToM by asking children to ing about thoughts, intentions, or beliefs vs. respond to vignettes that required cognitive thinking about feelings); and each of these and affective reflections on others or on dimensions is further differentiated into in- themselves. For example, for an interper- terpersonal and intrapersonal ToM (thinking sonal ToM task, children were told a story about the thoughts and emotions of others about Sally/Sam who sees a Band-Aid box. vs. reflecting on and regulating one’s own The box is opened and she or he sees that thoughts and emotions). it contains crayons. The children are then asked what Sally/Sam first thought was in the NEUROANATOMICAL EVIDENCE FOR box (cognitive interpersonal ToM) and how ToM AND EMPATHY DIMENSIONS Sally/Sam felt about what they thought was in the box (affective intrapersonal ToM). For an Cognitive ToM intrapersonal ToM task, children are shown Numerous brain regions have been identi- a toothpaste box. The box is opened and fied as participating in cognitive ToM. These

include the medial prefrontal cortex (mPFC), tened to stories about character’s thoughts or superior temporal sulcus (STS), temporopari- mental states than when listening to descrip- etal junction (TPJ), and temporal poles (Frith tions of physical attributes or bodily sensa- & Singer, 2008; Saxe & Powell, 2006; Saxe, tions (Saxe et al., 2009; Saxe & Powell, 2006). Whitﬁeld-Gabrieli, & Scholz, Pelphrey, 2009; Moreover, Young et al. (2010) have shown Schilbach et al., 2012; Van Overwalle & that a disruption in the functioning of the Baetens, 2009; Young, Camprodon, Hauser, right TPJ using TMS can result in a reduction Pascual-Leone, & Saxe, 2010). Figure 1 pro- of the participant’s use of mental state infor- vides a graphic representation of these neu- mation in moral judgments. The mPFC, on the roanatomical regions. contrary, supports the attribution of more en- It has been further suggested that the TPJ during traits and qualities of others, as well is mainly in charge of transient mental infer- as of the self (Saxe & Powell, 2006; Schilbach ences about other people (e.g., their goals, et al., 2012; Van Overwalle & Baetens, 2009). desires, and beliefs). In support of this conclu- Supporting this conclusion, Saxe and Powell sion, several studies have found that bilateral (2006) found the mPFC to be activated in both TPJ was recruited more when participants lis- a belief reasoning task and a self-reﬂection task. Kalbe et al. (2010) reported that cognitive ToM also was impaired by 1-Hz repetitive TMS, which interfered with cortical activity of the dorsolateral prefrontal cortex.

Affective ToM and empathy Studies indicate a neuroanatomical and behavioral dissociation within the mPFC, distin- guishing between dorsomedial (dmPFC) and ventromedial (vmPFC) prefrontal cortex areas, with the dmPFC more associated with cognitive and interpersonal ToM and the vmPFC more associated with affective and intrapersonal ToM (Abu-Akel & Shamay-Tsoory, 2011; Choi-Kain & Gunderson, 2008; Kalbe et al., 2010; Shamay-Tsoory & Aharon-Peretz, 2007). Conventionally, lesions in the vmPFC have been associated with impaired affective ToM. These areas are also illustrated in Figure 1. Figure 1. Neuroanatomical areas associated with Neuroanatomical evidence supports two ToM. Cognitive ToM is associated with the dACC; possible empathy systems: an emotional sys- dorsal lateral prefrontal cortex; dmPFC, superior tem (i.e., emotional empathy) and a more temporal sulcus, and temporal parietal junction. Af- cognitive system (i.e., cognitive empathy or fective ToM is associated with the inferior frontal affective ToM). This model is illustrated in gyrus, orbital frontal cortex, and vmPFC. Intraper- Figure 2. These systems are dissociable and sonal ToM is associated with the PCun, PCC, MCC, may be activated in different situations. In vmPFC, and vACC. dACC = dorsal anterior cin- this model, affective ToM is a more advanced gulate cortex; dmPFC = dorsal medial prefrontal cortex; MCC = middle cingulate cortex; mPFC = emotional form of mentalizing, rather than medial prefrontal cortex; PCC = posterior cingu- what has been called “emotional contagion” late cortex; PCun = precuneus; ToM = theory of (Sebastian et al., 2012; Shamay-Tsoory, 2010, mind; vACC = ventral anterior cingulate cortex; 2011). Affective empathy is suggested to be vmPFC = ventromedial prefrontal cortex. dependent on the inferior frontal gyrus (IFG),

Figure 2. An illustration of the two systems for empathy representing dissociation between cognitive and emotional empathy. A further distinction has been proposed between two types of ToM processes: Cognitive ToM (taking the cognitive perspective of another) and affective ToM (building a theory over what another person feels). ACC = anterior cingulate cortex; mPFC = medial prefrontal cortex; STS = superior temporal sulcus; ToM = theory of mind; TP = temporal parietal; vmPFC = ventromedial prefrontal cortex.

anterior cingulate cortex, amygdala, and in- processing). The cortical midline structures sula via the vmPFC. Evidence from lesion (constituting the mPFC, the anterior, middle, studies suggests that individuals with dam- and posterior cingulate cortices, and the pre- age to the vmPFC are speciﬁcally impaired cuneus) are thought to integrate functionally in affective cognitive ToM (cognitive empa- self-related thought and planning (Northoff thy), whereas patients with lesions in the et al., 2006; van der Meer, Costafreda, Ale- IFG, insula, amygdala, or anterior cingu- man, & David, 2010). late cortex are impaired in affective empa- A distinction between actions generated by thy and emotion recognition (Shamay-Tsoory, the self and those generated by others is one Aharon-Peretz, & Perry, 2009). of the elementary prerequisites for mentalizing (Mitchell, 2009). However, whereas emo- Interpersonal and intrapersonal ToM tional empathy requires making a distinction and empathy between the self and others, a network in- Imaging studies on self-reﬂection indicate volving the vmPFC, and to some extent the that cortical midline structures, which are a TPJ, appears to be responsible for shared rep- set of regions in the midline of the cortex arch- resentations of self and others during higher ing around the corpus callosum, are involved level inference-based processes (Zaki, Bolger, in intrapersonal ToM activities (self-referential & Ochsner, 2009). Therefore, it has been

suggested that vmPFC participation in self- have indeed suggested that the connections reflection redefines this region as a key region between the vmPFC and the limbic system necessary for evaluating similarities and differ- underline the region’s centrality to emotional ences between one’s own mental states and self-reflection. To conclude, cognitive empa- those of others (Mitchell, 2009). It is conceiv- thy appears to be tied to higher order cogni- able that situations involving affective ToM tive functions that necessitate self/other dis- require more self-reflection than situations in- tinction and cognitive and affective ToM. The volving cognitive ToM, which are generally self/other distinction and affective ToM, in more detached. The vmPFC, which is strongly turn, involve a broader neural network, the tied to the amygdala, appears to be particu- core of which is the vmPFC (and to some ex- larly important to affective mentalizing rather tent the TPJ). than to neutral or cognitive forms of mentalizing. In line with this notion, it was suggested EXPLAINING ToM AND AFFECTIVE in a recent meta-analysis that the vmPFC is EMPATHY more frequently activated by self-related judgments whereas dmPFC is more frequently ac- Researchers have offered two primary ex- tivated by other-related judgments (Denny, planations for how persons are able to at- Kober, Wager, & Ochsner, 2012). tribute mental states and emotions to others. Patients with ToM impairments, such as The “theory theory” (TT) holds that some- individuals with autism, have been reported how people acquire a theory of the mental to demonstrate impairments in self/other dis- realm. According to this view, people employ tinction (Kana et al., 2013). Lombardo et al. ToM to attribute intentional states to other (2010) found that neurotypical individuals people (Churchland, 1998). Namely, they use used the vmPFC and the middle cingulate cor- cognitive terms to construe situations involv- tex when self-referencing/mentalizing as com- ing the other, thus constructing a theory by pared with other-referencing/mentalizing. In which they understand the object (Premack contrast, persons with autism used the vmPFC & Woodruff, 1978). In other words, in line and middle cingulate cortex for both self- and with the TT thesis, people adopt a theoretical other-referencing. These researchers argued stance to gain an understanding of the other’s that unusual activation of the vmPFC for other- mental state (Gallagher, 2001). referencing in addition to self-reflection may In contrast to the TT explanation of cogni- explain the mentalizing impairments found in tive ToM, the simulation perspective explains autism. that the mental states of others are repre- Further studies have accumulated evidence sented by tracking or matching these states regarding a dissociation between affective and with resonant states of one’s own. Employing cognitive ToM in neurological and psychiatric imagination, mental pretense, or perspective disorders such as Parkinson’s disease (Polleti taking, the attributor covertly tries to mimic et al., 2012), multiple sclerosis (Roca et al., the mental activity of the target through mir- 2014), schizophrenia (Shur, Shamay-Tsoory, roring processes. For example, if you have run & Levkovitz, 2008), psychopathy (Shamay- in 10-km race on a hot day, you can put your- Tsoory et al., 2010), and borderline person- self in the place of similar runners and have a ality disorder (Choi-Kain & Gunderson, 2008; sense of what they are thinking and feeling as Harari et al., 2010). Taken together, these they run the last kilometer. studies suggest that the vmPFC constitutes a Therefore, this perspective emphasizes the core region within the larger mentalizing net- use of “shared representations” in empathy. work (also pertaining to the mPFC, STS, and For instance, one’s autobiographical memory temporal poles) that participates in self/other may contribute to one’s ability to simulate the distinctions and in affective ToM. The results emotions of others. Autobiographical mem- of a meta-analysis (van der Meer et al., 2010) ory, or the ability to recall one’s specific past

experiences, differs from semantic memory, observed motor acts (e.g., grasping, holding, which is simply knowledge of facts and con- bringing to the mouth) as well as a mecha- cepts. Autobiographical memory requires the nism for understanding the intentions of oth- ability to project oneself through time and ers (Avenanti, & Urgesi, 2013; Iacoboni, 2009; hence requires self-mentalizing or intraper- Iacoboni et al., 2005; Pfeifer et al., 2009; Riz- sonal ToM. There is growing evidence that zolatti & Craighero, 2004; Waytz & Mitchell, remembering the past and the ability to men- 2011). talize about others share an extensive func- Mirror neurons are thus active both dur- tional neuroanatomy, implying that these pro- ing the execution and observation of an ac- cesses share analogous mechanism (Mitchell, tion. It has been suggested that, given the 2009; Rabin, Gilboa, Stuss, Mar, & Rosen- observation-execution properties of the mir- baum, 2010; Spreng & Mar, 2012). On the ba- ror neuron system, it is particularly well suited sis of a meta-analysis of neuroimaging studies, for providing the pertinent mechanism for van der Meer et al. (2010) suggested that while motor empathy, imitation, and emotional con- the vmPFC is responsible for emotional self- tagion. reflection, a network that includes the mPFC A “mirror-like” activity has been identified and medial temporal lobes is responsible for in humans in the IFG and in the inferior pari- integrating self-referential representation (in- etal lobule. The IFG has been suggested as trapersonal ToM) and autobiographical mem- being capable of recognizing the aims or in- ory. Although there are conflicting reports on tentions of actions through their resemblance the role of autobiographical memory in men- to stored representations of these actions talizing about others (or simulating the experi- (Avenanti & Urgesi, 2011; Enticott et al., 2012; ence of others), persons are more likely to use Rizzolatti, Fabbri-Destro, & Cattaneo, 2009; autobiographic information (use simulation) also see Hickok, 2009 for a critical review of when they perceive others as more similar the mirror neuron theory in humans). Consis- to themselves than different from themselves tent and strong evidence exists for IFG par- (Perry, Hendler, & Shamay-Tsoory, 2011). ticipation in emotional contagion and emo- It has been further suggested that the affec- tion recognition. Indeed, further support for tive aspect of empathy also includes an “expe- simulation-like activity in humans has also rience sharing” component that is more auto- been found in studies examining various basic matic and implicit (Keysers, Kaas, & Gazzola, and complex emotions (Benuzzi, Lui, Duzzi, 2010). The identification of a class of neu- Nichelli, & Porro, 2008; Blakemore, Bristow, rons in the primate premotor cortex, known Bird, Frith, & Ward, 2005; Ebisch et al., 2008; as mirror neurons, has provided some clues Jabbi, Swart, & Keysers, 2007; Krach et al., as to how this mechanism works and has 2011; Masten, Morelli, & Eisenberger, 2011; greatly reinforced the simulation perspective. Mobbs et al., 2009; Morrison, Lloyd, di Pel- Mirror neurons were first discovered in the legrino, & Roberts, 2004; Prehn-Kristensen premotor cortex of macaque monkeys. These et al., 2009; Singer et al., 2004; Singer, 2006; are neurons that fire as the monkey performs Wicker et al., 2003). Furthermore, overt fa- object-directed actions such as grasping, tear- cial mimicry (as measured by electromyogra- ing, manipulating, and holding, yet they also phy or through observation) has been shown fire when the animal observes another ani- to be related to emotional contagion and mal or human being performing similar ac- emotion understanding (Niedenthal, 2007). tions. Mirror properties were found in human Mirror-like activity in the human IFG, which subjects with inferior frontal and posterior is related to emotional facial expressions, may parietal cortical involvement (Iacoboni et al., imply that these regions may be deployed 2005). In the context of social cognition, it has to transform observed facial expressions into been proposed that mirror neurons may pro- a pattern of neural activity that would be vide a neural mechanism for recognizing the appropriate for generating similar facial

expressions and could constitute the neural might be inferences or thoughts based on log- basis for emotional contagion (Keysers & Gaz- ical relations or contextual and situational in- zola, 2006). Moreover, some neuroimaging formation or simulation triggered by autobi- studies centered on emotion recognition and ographical memories. It is possible that un- empathizing with people who are subject to der normal circumstances, every interaction serious threat or severe harm, further sub- with a protagonist may independently trig- stantiating the particular role of the IFG in ger both an emotional response (emotional emotional empathy (Nummenmaa, Hirvonen, empathy) and a cognitive evaluation of the Parkkola, & Hietanen, 2008; Schulte-Ruther, individual’s state of mind and point of view Markowitsch, Fink, & Piefke, 2007). (cognitive empathy; Shamay-Tsoory, Aharon- Emotional empathy, through simulation Peretz, & Perry, 2009). In the past few years, processes, also includes motor and percep- data from naturalistic models point to the tual components. Various studies have shown suggestion that in complex social situations that watching someone else in pain or being individuals use multiple empathic processes touched triggers an internal sensorimotor sim- rather than distinct, depending on the con- ulation of the observed somatic experience in text and relevance to social goals and cues the observer (e.g., Avenanti, Bueti, Galati, & (Zaki & Ochsner, 2012). Hence, although Aglioti, 2005; Bufalari, Aprile, Avenanti, Di, both the emotional and cognitive components & Aglioti, 2007; Keysers et al., 2004). This of empathy may work autonomously, in natu- sensorimotor resonant mechanism, mediated ral social situations, every empathic response by somatomor cortices (such as SI, SII, mo- evokes both types of components to some ex- tor and premotor cortices, etc.) was found tent (Zaki & Ochsner, 2012), depending on critical for understanding other’s emotions variables such as the social context (Harris (Adolphs, Damasio, Tranel, Cooper, & Dama- & Fiske, 2006), the level of distress (Jackson, sio, 2000; Borgomaneri, Gazzola, & Avenanti, Brunet, Meltzoff, & Decety, 2006), or the per- 2014; Pitcher, Garrido, Walsh, & Duchaine, ceived similarity between the individual and 2008). The activity in these cortices was also the protagonist (Hein, Silani, Preuschoff, Bat- found to correlate with psychological fac- son, & Singer, 2010; Mitchell et al., 2005). tors (suggested in behavioral studies to af- In conclusion, although the simulation per- fect the degree of empathy), such as person- spective may be more suitable in explaining ality traits of the empathizer (Avenanti, Minio- emotional empathic processing, TT processes Paluello, Bufalari, & Aglioti, 2009; Schaefer may underlie cognitive empathy. Therefore, et al., 2013) and the attitude toward the tar- decreased empathic response may be due to get’s social membership (Avenanti, Sirigu, & deﬁcits in mentalizing (cognitive ToM, affec- Aglioti, 2010), with the possibility to predict tive ToM) or in simulation processing (emo- prosocial behavior in real-life situations (Ma, tional empathy), with these deﬁcits mediated Wang, & Han, 2011). by different neural systems. One central hy- It should be noted that the role of mirror pothesis is that simulation processing under- neurons in simulation has been challenged lies emotional empathy whereas ToM under- (Hickok, 2009). Mirror neurons, however, lies the cognitive empathic response. These would not have to explain all simulations. Wal- processes are served by separate, albeit inter (2012) suggests a low road and a high road teracting, brain networks. When a cognitive to empathy. Mirror neurons are hypothesized empathic response is generated, the ToM net- to function in the low road, responding more work (i.e., mPFC, STS, temporal poles) and or less automatically to facial expressions and the affective ToM network (mainly involv- body movements. They could account for ing the vmPFC) are typically involved. In emotional contagion. In a high road to em- contrast, the emotional empathic response pathy, empathic processes are induced top- is driven mainly by simulation and involves down by higher cognitive processes, which regions that mediate emotional experiences

(i.e., amygdala, insula). We can assume that ToM may improve a person’s understanding balanced activation of these two networks is of others’ thoughts and behaviors; however, required for appropriate social behavior. they are unlikely to have much effect on affective ToM and affective empathy. Conse- IMPLICATIONS quently, professionals providing clinical ser- vices to children, adolescents, and adults with Theory of mind deficits are considered to ToM deficits should develop ToM profiles for be at the heart of the social difficulties exhib- their clients that are comprehensive. Westby ited by persons with autism and Asperger’s and Robinson (2014), for example, provide syndrome and are common in children and a framework for assessing and intervening in adolescents who are deaf or hard of hear- these multiple aspects of ToM. This includes ing (Kimhi, 2014; Stanzione & Schick, 2014) documenting strengths and deficits along all and have been associated with the social ToM dimensions—interpersonal and intraper- problems exhibited by persons with brain in- sonal cognitive and affective ToM and affec- juries, degenerative neurological conditions, tive empathy. Then, clinicians can design in- and psychiatric diagnoses. Assessments and terventions to target the specific deficits. interventions for persons with ToM deficits Finally, an intervention that aims to im- have focused typically on assessing and de- prove clinical indices of social dysfunction veloping interpersonal cognitive ToM as a needs to take into account the complex rela- way to improve social skills. Results of neuro- tions between empathic processes. Although science studies, however, indicate that ToM is existing studies have identified variables af- a multidimensional rather than a unitary con- fecting cognitive and affective empathy, less struct and that possessing knowledge of the is known about the relations between these thoughts and feelings of others does not en- processes. As interventions are designed to sure empathy for others. affect performance in complex situations and Although dissociations can be made be- not just simplified ToM tasks, studies should tween several empathic processes, these pro- focus on naturalistic approaches using eco- cesses work together in naturalistic situations. logically valid tools that simulate real-life situ- As the work on the neural underpinnings ations. It is such tools that will illuminate em- of ToM and empathy reviewed in this arti- pathic processes that enhance how humans cle shows, interventions addressing cognitive interact.

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