Neural Foundation of Morality

Neural Foundation of Morality Roland Zahn, Translational Congnitive Neuroscience of Affective Disorders Laboratory, The University of Manchester, School of Psychological Sciences, Manchester, UK. Ricardo de Oliveira-Souza and Jorge Moll, D’Or Institute for Research and Education (IDOR), Rio de Janeiro, Brazil Ó 2015 Elsevier Ltd. All rights reserved.

Abstract Moral behavior is one of the most sophisticated human abilities. Many social species behave altruistically toward their kin, but humans are unique in their ability to serve complex and changing societal needs. Cognitive neuroscience has started to elucidate specific brain mechanisms underpinning moral behavior, emotion, and motivation, emphasizing that these ingredients are also germane to human biology, rather than pure societal artifacts. The brain is where psychosocial learning and biology meet to produce the rich individual variability in moral behavior. This article discusses how cognitive neuroscience improves the understanding of this variability and associated suffering in neuropsychiatric conditions.

Introduction The terms moral and ethical derive from their respective Latin and Greek roots (moralis and ethikos). Literally, they would probably be best translated as in accordance with societal customs. Based on this, the authors have suggested an operational definition of moral behavior as behavior that is in accordance with other people’s needs or sociocultural norms (Zahn et al., 2011). Moral behavior requires at least two components: (1) knowing about sociocultural norms and the needs of others and (2) being motivated to act on this knowledge (Zahn et al., 2011). Distinguishing moral from selfish motivations in real life is often difficult, and cooperation in societies is usually not sustained on the basis of moral motivations alone. Instead, such morally motivated behaviors intermingle with self-serving ones that sustain individual survival in a complex interplay that often helps stabilize productive relations in social groups. Such behaviors essentially include codes of reciprocity (described in the economic and evolutionary literature, as a direct or indirect gain for somebody for cooperating in a society (Nowak and Sigmund, 2005)). Societies have therefore developed external reward and punishment systems, nowadays enshrined in law, work ethics, and other organizational regulations, to enforce behavior in accordance with communal welfare. Computational models have shown that individual variability in moral behavior may have sustained cooperation in small social groups that preceded our modern societies (Boyd et al., 2003; Boyd and Richerson, 2009). These studies suggest that in the absence of law enforcement systems, cooperation can only be sustained if at least a fraction of individuals are motivated to risk substantial resources in order to punish other individuals who behave immorally. Were these individuals perfectly economically ‘rational’ and purely selfishly motivated, there would be no incentive to do so in that they would usually lose more than they would win. Such costly behaviors have been referred to as ‘altruistic punishment.’ In these models, selfishly motivated individuals, known as ‘defectors,’ are kept in check by the ‘altruistic punishers.’ A third type of agents will contribute own resources to the community (‘contributors’). The debate

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in evolutionary sciences is how the genes of people who sacrifice their own resources could have survived evolutionary pressures. This is easy to explain in the small groups from which we are thought to originate, based on kinship-based genetic relatedness mechanisms. Thus, everything that was beneficial to the survival of the group would benefit the duplication of the gene pool, relative to individuals belonging to other small-scale societies. However, many evolutionary theorists need to explain sacrifices of one’s own resources in large-scale modern societies by nonmoral motivations, reverting to at least indirect benefits of cooperation for oneself or one’s family (West et al., 2007). This is because they disagree with the argument of group selection benefits, which is supported by Boyd et al., whose model proposes that cooperative societies enhance the survival chances of their genes in competition with noncooperative ones even in the absence of intragroup genetic relatedness. This view is also adopted by researchers performing neuroeconomic experiments to demonstrate altruistic behavior among strangers in the absence of direct or indirect benefits (Gintis et al., 2008). While it is beyond the scope of this chapter to delve into this fascinating debate further, important implications for the neuroscience of morality can be derived: 1. If gene selection has promoted moral motivations within societies, then these genes must have influenced brain mechanisms that support moral behaviors, because biological influences on human behavior are mediated by the brain. 2. If this was indeed the case, then those brain mechanisms must have also allowed for adaptation through cultural learning that allowed individuals to adapt to changing sociocultural environments, because the same behavior can be adaptive and maladaptive depending on cultural and situational contexts (e.g., ‘killing in war’ and ‘killing in peacetime’). 3. If individual variability in moral motivations was necessary to provide group survival advantages, then one should be able to identify different types of brains supporting different inclinations toward different balances of moral and selfish

International Encyclopedia of the Social & Behavioral Sciences, 2nd edition, Volume 16

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Neural Foundation of Morality

motivations that are further shaped by cultural learning. This would then allow for individuals ranging in their motivational inclinations from selfish to different degrees of preparedness to moral punishment or cooperation. This article will provide an overview of the human brain mechanisms that appear to be selective for moral as compared with selfish motivations (Section Cognitive-Anatomical Basis of Moral Motivation) thereby addressing the first question. The authors further devote a section to brain mechanisms underpinning social knowledge to address the second question (Section Cognitive-Anatomical Basis of Social Knowledge). They take the perspective here, that social knowledge can be used for moral as well as selfish purposes (e.g., manipulation and reputation gain) and is therefore not selective for the moral domain. To address the third question, the authors discuss evidence supporting individual differences in the neuroanatomy of moral motivations and relate this to the question of how these may contribute to mental health and suffering (Section Implications for Differential Vulnerability in Psychiatry). A large proportion of us suffer from psychiatric disorders at least once during our lifetime, for example, depression is estimated to affect 151 million people around the world (Funk, 2010). Our risk is significantly influenced by genetic factors as shown by studies comparing mono- and dizygotic twins (Kendler, 2006). Given the large number of affected people, it is tempting to speculate whether some psychiatric risk genes have carried advantages for psychosocial functioning and survival in order to be selected for by evolutionary pressures. If it is the variability between individuals within societies that makes these function most adaptively, this could explain the variability in how people navigate in the social world. This variability could then explain vulnerability to different types of mental health problems depending on the demands of one’s social environment. Some evolutionary thinkers support the idea that risk genes for psychiatric disorders could have adaptive functions through group selection (Wilson and Wilson, 2007). Others, in contrast, have argued that the polygenetic nature of these risk genes and their complex interactions with environmental factors can explain the high frequency of psychiatric disorders, despite their proposed evolutionary maladaptiveness (Keller and Miller, 2006). Brain mechanisms that influence social cognition and behavior are based on macroanatomical, microstructural, and neurochemical components that are employed to learn and adapt to complex information in our psychosocial environment. The advent of moral neuroscience was the discovery that disruptions of the macroanatomical structure of brains could lead to marked changes in moral behavior (Section Moral Behavior in Patients with Macroanatomical Brain Lesions). Microstructural changes were documented in postmortem studies of conditions such as autism (Casanova et al., 2002), a disorder of social cognition in general rather than moral cognition more specifically. Due to the difficulty in obtaining such data, however, there is not enough evidence on microstructural changes tied to moral behavior to be included here. Functional magnetic resonance imaging (fMRI) has been employed since the 2000s to study moral cognition and emotion. While this has provided us with a rich set of data, its interpretation needs cautious validation

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from lesion studies. This is because the results of functional activation-based neuroimaging depend as much on the psychological task conditions as they do on brain structure and function. fMRI, however, provides a unique opportunity to measure psychobiological interaction thereby capturing the results of brain adaptations to psychosocial learning (Section Functional Neuroimaging of Moral Cognition and Emotion). Electrophysiological properties of the brain are probably closest to human experience and novel techniques of analyzing electroencephalography and magnetic encephalography have opened up great possibilities. The evidence base using these techniques in moral cognition is still quite narrow and will therefore not be reviewed here. Transcranial magnetic stimulation is a way to simulate brain lesions and has been employed in moral neuroscience, but its use is restricted to areas near the skull surface and thereby does not allow for a systematic study of several of the brain regions known to be relevant from patient lesion studies. Neurochemical influences on moral cognition and emotion have been reviewed elsewhere and are beyond the scope of this article (Moll and Schulkin, 2009). Finally, the authors will not review correlations between gene polymorphisms with neuroimaging data. This is because the focus of this article is on understanding the neural rather than the genetic prerequisites of moral behavior. Section Cognitive-Anatomical Models of Moral Cognition and Emotion briefly summarizes the conflicting neurocognitive models of moral cognition and emotion and lays the ground for future directions for research.

Moral Behavior in Patients with Macroanatomical Brain Lesions In 1888, Leonore Welt, a Swiss physician, reviewed a series of patients with damage to the frontal cortex, who showed marked changes in moral character as judged by their jocular childish or aggressive behavior (Welt, 1888). Interestingly, their general intelligence was preserved. Phineas Gage, the now famous US American patient (Damasio et al., 1994), with an iron-bar injury to his medial frontal lobes was one of the cases reviewed by Dr Welt. Based on postmortem neuropathology and injury pattern, she concluded that the most consistent structure damaged in all cases was the right medial orbitofrontal cortex. While this was probably the first systematic evidence for a causal role of specific brain structures for enabling moral behavior, it also marked the beginning of a controversy about the function of the frontal lobes. This is because systematic studies of patients with head injuries during the First World War confirmed earlier case reports of some patients with frontal lesions and no behavioral change (Teuber, 2009). This lack of impairment in some patients could of course be explained by insufficient characterization of the lesion or lack of sensitivity of clinical observation. However, it could also point to individual variability in cognitive-anatomical architecture leading some patients to be more sensitive than others to frontal brain lesions. In the 1980s, brain computed tomography became available in clinical settings and led to a renaissance of neuropsychological case studies. Eslinger & Damasio sparked new

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interest in the neural basis of behavior counter to moral rules by describing EVR, a patient with ventral frontal lobe damage due to tumor resection (Eslinger and Damasio, 1985). He exhibited difficulty in making daily life decisions and made choices that led to a ruin of his financial fortunes as well as his marriage. At the same time, he showed normal functioning on classical tests of executive functioning such as the Wisconsin Card Sorting test, which is usually impaired in patients with left dorsolateral frontal lesions, which was not damaged in EVR. In the same decade, a neurodegenerative disease, originally described by Arnold Pick in the late nineteenth century, became recognized as a relatively common form of early-onset dementia that could be reliably diagnosed before death (Snowden et al., 2001). These patients exhibited varying degrees of frontal and anterior temporal atrophy captured in the term ‘frontotemporal lobar degeneration.’ This led to cumulating evidence on inappropriate social behavior in these patients (Bozeat et al., 2000) that was independently associated with right anterior temporal and ventromedial frontal atrophy (Liu et al., 2004). Patients with right anterior temporal lesions behave as inappropriately as patients with ventral frontal atrophy. For example, in their clinic, the authors saw a patient (further referred to as ‘the singing lady’) with isolated right anterior temporal lobe atrophy, who lost her job, because of kissing and singing to customers at work, who also sang happy birthday to her parents on the cemetery. Studies in patients with brain lesions were often hampered by the lack of neuropsychological tasks that could probe cognitive functions relevant to the observed behavioral changes and largely relied on carer reports. Loss of guilt was reported by carers of patients with ventromedial (prefrontal cortex) lesions (Koenigs et al., 2007) and neurodegeneration in this area, which included the subgenual cingulate cortex, was associated with loss of interpersonal warmth as judged by carers (Sollberger et al., 2009). Inappropriate behavior in these patients often goes against societal needs or needs of others and therefore clearly has moral implications. However, the disruption of which cognitive and emotional components leads to this behavioral change is disputable. Patients with ventral frontal lesions were found to show intact social knowledge when asked about their behavior (Saver and Damasio, 1991; Eslinger and Damasio, 1985). Similarly, Mendez et al. found in their patients with frontotemporal lobar degeneration that knowledge of moral rules was intact when assessed on a questionnaire, but nevertheless patients failed to act on these rules (Mendez et al., 2000). This may lead to the hypothesis that moral motivation and knowledge may be at least partly dissociable. The hypothetical causes of socially inappropriate behavior are 1. Loss of (access to) knowledge of appropriate social behavior (Zahn et al., 2009b). 2. Loss of the moral motivation to act upon intact social knowledge (Moll et al., 2005b). 3. Loss of the ability to suppress urges/drives (Brutkowski, 1965) with intact social knowledge of their inappropriateness and intact moral motivation to act upon this knowledge.

In order to test these different possibilities, one needs to probe moral motivations experimentally while controlling for social knowledge and vice versa. Two studies in patients with frontotemporal lobar degeneration have used this approach. One study showed that patients with damage of the right anterior temporal lobe displayed selective deficits on abstract knowledge of social behavior (i.e., social conceptual knowledge, e.g., what it means to act ‘tactfully’) relative to nonsocial conceptual knowledge (e.g., what it means to be ‘nutritious,’ Zahn et al., 2009b). Furthermore, selective deficits on social concepts were associated with inappropriate social behavior. The social concept discrimination task used to probe this particular type of social knowledge did not require moral motivations and controlled for the effects of positive or negative emotional valence. Interestingly, the right anterior temporal lobe atrophy patient, ‘the singing lady,’ exhibited a selective impairment on social concepts with relatively intact nonsocial concepts when using this test (Zahn et al., 2012). Another study showed that patients with frontotemporal lobar degeneration and relatively stronger involvement of the septal area were selectively impaired on a task probing guilt and pity, relative to other negative emotions such as embarrassment, disgust, and anger (Moll et al., 2011). The task controlled for the degree of social knowledge required by using similar statements to describe social situations in which one usually feels a particular moral feeling (e.g., “Your mother calls you one night, telling you she was not feeling well. You did not take her seriously and the next day she died” associated with guilt in 80% of a normative sample). Neurodegeneration of the frontopolar cortex was associated with selective loss of guilt, pity, and embarrassment compared with disgust and anger. These studies, together with evidence from fMRI reviewed below, indicate that moral motivations and social conceptual knowledge are associated with dissociable brain regions and can thus independently contribute to inappropriate social behavior. The third and most popular explanation for such behavior, however, is that these patients know about other people’s needs and are motivated to act on them, but that they have lost the ability to suppress selfish urges in subcortical regions that counteract their ability to act morally. This frontal-subcortical suppression view probably became influential because of the way conditioning experiments in nonhuman animals were interpreted (Brutkowski, 1965). To the authors’ knowledge, there is, however, no anatomical evidence supporting strictly unidirectional, inhibitory connections from frontal cortical to subcortical areas, which would support such a suppression mechanism. Furthermore, there is no evidence that selfish motivations are more dependent on subcortical than cortical mechanisms. On the contrary, there is evidence from case reports in patients with subcortical lesions that these may be associated with severe antisocial behavior. Subcortical lesion cases included hypothalamus, septal area, amygdala, and basal ganglia (Moll et al., 2003), but it is unclear how regularly these associations can be found. A more plausible version of the frontal-subcortical suppression model is mentioned below in which the frontal cortex is thought to control (Miller and Cohen, 2001) rather than suppress other areas of the brain.

Neural Foundation of Morality

In principle, one must consider another explanation for ‘immoral’ behavior after ventral frontal lesions, namely, that moral behavior requires more complex cognition and will thereby be nonspecifically impaired in large brain lesions. If this was the case, patients with similar degrees of brain damage and impairment should also show similar degrees of deviations from moral behavior. Interestingly, this is clearly not the case in that patients with Alzheimer’s dementia in similar mild to moderate stages of the disease do show intact interpersonal behavior in the overwhelming majority of cases (Bozeat et al., 2000). Alzheimer’s dementia typically leads to neurodegeneration of medial temporal, as well as medial and lateral parietal brain regions in these stages (Herholz, 2003). This means that moral behavior in a daily life context appears to be independent of these brain regions.

Functional Neuroimaging of Moral Cognition and Emotion Introduction When describing the function of a brain area, one can either describe (1) which type of task it is involved in carrying out (i.e., process-dependent description), (2) which information content it stores (i.e., content-dependent description), or (3) in which format it stores information (i.e., format-dependent description). The brain regions considered to be important for moral cognition and emotion were found to be involved in tasks and contents of different formats (e.g., visually presented pictures and written statements, reviewed in Moll et al., 2005b). However, because most people assume format independence of moral cognition and emotion, this was not rigorously investigated for most brain regions. Most fMRI studies of moral cognition and emotion have either taken a process- or a content-based approach to the design of their experiments. Describing a brain area as involved in a certain process or representation of a certain content is not very helpful in itself, unless one can make the case that there is some degree of selectivity of its involvement in that particular process or content compared with other processes or contents and other brain areas. This is because the less specifically a process or content is defined and tested, the more brain areas and cognitive components will be involved in it. So one could design experiments testing very broad functions, which will then involve a large set of brain areas, but this will not be very informative (i.e., add new information to what was known before). The authors have therefore focused on reviewing studies that chose experimental and control conditions in such a way that a high degree of selectivity of a given brain region for the function of interest could be derived. Claims of process selectivity are often not supported by generalizing across different types of contents and likewise content selectivity is often not supported by being tested across different tasks (processes). Future studies are needed to fill this gap. The broader involvement of a network of frontal, subcortical, and anterior temporal regions in moral cognition and emotion tasks, however, is generally agreed upon when considering the lesion and functional imaging literature (Moll et al., 2005b, 2008). In fMRI studies, posterior superior temporal, temporoparietal junction, and precuneus are also regularly activated in

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moral cognition and emotion tasks. The fact that patients with posterior cortical atrophy and Alzheimer’s disease do not usually show grossly abnormal social behavior (see above) implies that the involvement of these regions must be more subtle and it is unlikely that they will show the same degree of selectivity for moral cognition and emotion. Fronto-temporo-subcortical networks activated in response to morally relevant stimuli are highly overlapping with brain responses to other social cognition tasks (e.g., when having to think about mental states compared with physical inferences (‘theory of mind’) (Frith, 2007)). It is therefore important to define what distinguishes moral from social contents or processes. The authors define in this article social behavior as any type of behavior that has potential consequences for others. Thereby, any type of social behavior will have moral implications, subtle as they might be, in that it affects other individuals or society in general. Lonesome behaviors such as paper recycling at midnight when nobody watches are very good examples of social behaviors with moral implications in that the action of recycling motivating the action is driven by societal needs. When observing social behavior from the outside, there is therefore no way of distinguishing social from moral behavior. Only when hypothesizing about the different motivations driving these behaviors, it is that we are able to distinguish moral from selfish social behaviors. For example, unobserved behavior that supports societal needs such as a man recycling paper at night is more likely to be morally motivated than the same behavior with relevant others watching. For example, the recycling man could be motivated by trying to charm an ecologically conscious women observer whom he is sexually interested in. Thus, according to our definition here, what is special about moral relative to social contents and processes is their specificity for morally relative to selfishly motivated behavior. Selfish social behaviors require the same amount of mental state inferences as morally motivated social behaviors if they require manipulating other people. For both cases of morally or selfishly motivated behaviors, however, the level of engagement of social cognition mechanisms will depend on the level of the complexity of predictions about the effects of one’s behavior on others and associated social interactions. Nevertheless, there is quite a large repertoire of selfish behaviors that are nonsocial and thus require much less complex cognition, because social interaction is generally more complex and contextualized. This may explain why impairments of general social cognition appear to impair moral behavior more than selfish behavior in general. One example is the right anterior temporal lobe atrophy patient, ‘the singing lady,’ mentioned before, who showed a selective impairment on social conceptual knowledge, which impaired her understanding of social situations and thereby led her to violate social rules with a relatively intact ability to help herself to food, play Sudoku puzzles, and appear quite happy in her mood. When reviewing the functional imaging literature, the authors will therefore include brain regions that show some selectivity for social compared with nonsocial cognition even if they are most probably not special for moral functions proper. The authors will not, however, focus on brain regions such as the left lateral parietal and left dorsolateral prefrontal cortices whose

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specialization for social cognition is unlikely given the intact clinical appearance of social behavior in patients with focal lesions to these areas, such as aphasic stroke patients (Zahn et al., 2004).

Content-Based Subdivisions At the broadest level, morally relevant contents were compared with nonmorally relevant contents. This included verbal statements or pictures rated by participants according to their moral relevance before the fMRI experiment. Obviously, it is important to control for the emotional relevance in those experiments, which was done in at least some of the studies. Taken together, frontopolar, ventral frontal, subcortical, and anterior and posterior temporal sulcus were most consistently activated when comparing morally relevant with morally irrelevant materials (reviewed in Moll et al., 2005b). The difficulty lies in identifying the functional contribution of each of these areas in that one could argue that socially relevant materials have been found to engage similar brain areas and it is unclear to what extent any of these areas is selective for moral cognition and emotion. Should they be involved in more general social functions, it is also unclear which exact contribution they are making to moral cognition and emotion. It is a matter of debate, how to best subdivide different categories of morally relevant contents. One approach is to distinguish between harm-, disgust-, and dishonesty-related (Parkinson et al., 2011) or justice- and care-related (Ochsner et al., 2004) moral contents and these were shown to be associated with differential brain activation patterns. The difficulty, however, is to demonstrate that complex moral scenarios used in these studies differed mainly with regard to these categorical distinctions, or whether there were associated differences in other nonmeasured variables. The eighteenth century German philosopher Immanuel Kant distinguished the ability to judge what is morally right and wrong (“principium diiudicationis”) from the motivation (“principium motivationis”) to act morally (Kant, 1786/1903). He thereby anticipated a dissociation later found in some patients with ventral frontal brain lesions whose knowledge of how they should behave seems to be better preserved than their motivation to act accordingly (Eslinger and Damasio, 1985). The reverse dissociation can be observed as well. For example, the patient with a focal right anterior temporal lobe atrophy (‘the singing lady’) was selectively impaired on conceptual knowledge of social behavior as described before. Interestingly, she was among a minority of patients with frontotemporal lobar degeneration in which carers agreed that she appeared able to feel guilty. The authors probed this experimentally by giving her 22 sentences where she was described acting badly toward her best friend (negative selfagency condition: e.g., ‘You act in a stingy way toward Jane’), in the negative other-agency condition, the authors just reversed the agents and recipients thereby keeping the social knowledge required to understand the sentences equal (e.g., ‘Jane acts in a stingy way toward you’). Often, the patient did not understand what the concept (e.g., ‘stingy’) meant, but she was generally able to say whether it was a good or a bad thing to do (the most general form of social knowledge).

After each sentence she was asked to say out aloud the feeling she would feel in this situation and was given a selection from guilt, anger, pride, gratitude, and none/other. This allowed her to respond with guilt in 73% of the negative selfagency trials, rarely responding with anger (5%) in this condition. In the negative other-agency condition, however, she showed the reverse pattern (68% of anger and 5% of guilt). It thus appears that if she was given the right cues, she was able to experience guilt, but because of her impaired social conceptual understanding, she would often miss the cues of the situation in real life. The sections below review fMRI studies that have contributed to a better understanding of the interlocking but partly independent neural systems underpinning social knowledge and moral motivation.

Cognitive-Anatomical Basis of Social Knowledge Social knowledge has been defined as knowledge of one’s own and other people’s minds (Adolphs, 2009). Because ‘mind’ or ‘mental states’ are hard to break down neuropsychologically, the authors prefer defining social knowledge as denoting nonepisodic (i.e., semantic) knowledge of social sensory properties and social behavior (i.e., functions, see Figure 1). There is growing consensus among neuroscientists investigating semantic knowledge of objects, that this requires not only the representation of modality-specific sensory and motor features of objects (e.g., ‘the color of a robin,’ ‘the feel of its feathers’), but also a more abstract representation of the core aspects of what one means by, e.g., ‘robin.’ These core aspects are particularly important for understanding the behavior or functions of the things surrounding us. Based on evidence

Figure 1 The hypothesized neurocognitive components of social and moral knowledge are illustrated (modified from Zahn, R., OliveiraSouza, R., Moll, J., 2011. The neuroscience of moral cognition and emotion. In: Decety, J., Cacioppo, J. (Eds.), The Handbook of Social Neuroscience. Oxford University Press). The authors refer to nonepisodic long-term memory here and distinguish between sensory social knowledge presumably represented in the posterior superior temporal cortex and knowledge of social behaviors (i.e., functions). The latter is subdivided into two anatomically separable systems: (1) abstract conceptual (i.e., context-independent) knowledge of social behavior represented in the anterior temporal lobes (aTL) and (2) associative (i.e., context-dependent) knowledge of social behavior represented in frontosubcortical networks. Associative knowledge of social behavior is subdivided into a component representing knowledge of sequences of social actions (events) within frontopolar cortex (FPC) and ventral prefrontal cortex (PFC) (representing associations of action/ event sequences with motivational/emotional states) and a subcortical mesolimbic component representing ‘free-floating’ motivational/ emotional states (see also Figure 4).

Neural Foundation of Morality

from fMRI, repetitive transcranial magnetic stimulation, and a neurodegenerative disease of the anterior temporal lobes called semantic dementia (a subtype of frontotemporal lobar degeneration), the anterior temporal lobe has been identified as hosting this core representation of concepts that is independent of the context of the type of task, modality, or arbitrary associations (Ralph and Patterson, 2008). For example, ‘greeting colleagues’ is associated with ‘cheek kissing’ in Brazil, but people in Britain would not strongly associate the two at least in the context of British work life. Such context-dependent associations are important for context-appropriate social behavior. Wood and Grafman provide an overview on evidence linking the frontal cortex with one particular type of associative context-dependent knowledge, namely, the knowledge of sequences of events and actions (Wood and Grafman, 2003). More specifically, they hypothesized that the ventral frontal cortex represents socially relevant knowledge of sequences of events and actions. This knowledge about the context of sequences of actions enables us to appropriately choose an action in one sequential context (e.g., ‘cheek kissing of colleagues in Brazil’), but refrain from it in another (e.g., ‘Britain’). This context-dependent appropriateness of many of our actions could explain why patients with ventral frontal lesions, one of the earliest and most consistently affected areas in frontotemporal lobar degeneration, do something that is inappropriate in a particular context, but not necessarily totally out of character. For example, the authors saw an 80-year-old lady with frontotemporal lobar degeneration from Manchester, who patted bottoms of men as soon as they bent down. This was despite not feeling any sexual desire. When the men turned around, she said: “Oh, I am sorry, I was just checking where your wallet was.” Interestingly, her husband told us that she was patting other men’s bottoms at parties when younger, but now this behavior had generalized to nonparty contexts. fMRI studies have confirmed the hypothesis that regions within the anterior temporal lobes are selective for social versus nonsocial concepts and that this area stores these concepts in a context-independent way. Right superior anterior temporal activations were found irrespective of the context of emotional valence (negative, positive (Zahn et al., 2007, Zahn et al., 2009c)), agency (self or other (Zahn et al., 2009c)), and task (semantic (Zahn et al., 2007) or emotional judgment (Zahn et al., 2009c)). The localization of activations concurred with the lesion evidence reported above. Another study found a more middle anterior temporal area on the left side, which was shown to be more active for social concepts relative to nonsocial concepts as well as overlapping with a mentalizing task (Ross and Olson, 2010). Thus, anterior temporal lobe activations during mentalizing tasks (Frith, 2007) could be explained by accessing social conceptual knowledge to interpret the intentions of other people. Subsequently, the right superior anterior temporal lobe localization for social compared with nonsocial concepts has been independently confirmed (Skipper et al., 2011). Direct evidence regarding knowledge of sequences of events and actions within the ventral frontal lobes from functional neuroimaging is still emerging. The medial frontopolar cortex

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(BA10), however, was activated when participants had to decide whether actions/events (e.g., ‘order the food,’ ‘ask for the menu’) were in the right or wrong sequential order. This activation was relative to a control condition of deciding whether the events were printed in the same or different font (Krueger et al., 2007). This task-dependent activation does not prove the existence of sequence-specific contents in this area, but an additional analysis in which the frequency with which events/actions occurred revealed that different subsectors of the medial frontopolar cortex were activated more strongly depending on frequency of occurrence in daily life. This is better explained by content-, rather than process-specific models, because response time did not explain these differences. Another study confirmed these results by showing that the medial frontopolar area was the only brain region to linearly increase activation with increasing complexity of event sequences (Krueger et al., 2009). One conundrum is how to explain relatively intact social knowledge in patients with ventral frontal lesions that often encompass the frontopolar cortex. A possible explanation is that the intact anterior temporal lobe representation of context-independent social knowledge may help these patients answer theoretical questions about appropriate behavior, but that in order to probe this knowledge of complex consequences of behavior as required for the execution of real actions, one will need to develop more refined ways of experimental testing.

Cognitive-Anatomical Basis of Moral Motivation The term moral motivation was used by the eminent moral philosopher Francis Hutcheson (Bishop, 1996), who played an important role in highlighting the importance of what were later called ‘moral sentiments’ by Adam Smith (Smith, 1759/ 1966) – now mostly referred to as ‘moral emotions.’ Morally relevant materials will always be emotionally relevant (Haidt, 2001) unless one tries to take the perspective of an impartial spectator (Smith, 1759/1966). The same network of brain regions mentioned before to be selective for morally relevant compared with morally less relevant materials is therefore the starting point for the search of neural correlates of moral sentiments. Here, the authors summarize the evidence on those moral sentiments that were studied in more than two fMRI studies.

Guilt The anticipation of guilt is thought to play an important role in preventing us from acting immorally and to motivate reparative action (Tangney et al., 2007; Eisenberg, 2000). The experience of guilt has been associated with activations of the dorsal cingulate in an early study (Shin et al., 2000), but this did not use an emotional control condition and does therefore not allow conclusions about guilt selectivity. Frontopolar activations were found most reproducibly for guilt while using different control conditions (other-critical feelings such as indignation (Moll et al., 2007; Zahn et al., 2009c); anger toward self (Kedia et al., 2008); embarrassment (Takahashi et al., 2004); regret with no consequences for others (Morey et al., 2012); and sadness (Basile et al., 2011)). The subgenual cingulate cortex (including the posteriorly adjacent septal area in some studies) was found to be selectively activated for guilt compared with indignation

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toward others, but only when modeling individual variability in empathic concern (Zahn et al., 2009a), or guilt-proneness (Zahn et al., 2009c; Green et al., 2012). Interestingly, subgenual cingulate activations for guilt were independently reproduced (Morey et al., 2012; Basile et al., 2011). In contrast, another fMRI study found right lateral orbitofrontal and posterior dorsomedial prefrontal activations to be selective for guilt compared with shame and sadness (Wagner et al., 2011).

Pity (Compassion, Sympathy) Emotional empathy and pity are very closely related and empathy has been extensively studied using neuroscience methods (Decety and Grezes, 2006). Empathy is usually conceived of as simulating other people’s experiences, whereas sympathy requires an extra step of feeling for the other person (de Vignemont and Singer, 2006). The frontopolar cortex was activated most consistently for compassion versus a neutral control condition (ImmordinoYang et al., 2009), as well as compared with other-critical feelings (Moll et al., 2007) and compared with self-directed anger (Kedia et al., 2008). None of these studies investigated individual differences in the experience of pity and this may have led to a failure in detecting septal or subgenual cingulate regions engaged by empathic concern while feeling guilt (Zahn et al., 2009a). Interestingly, a study in adolescents and adults found septal/subgenual cingulate activations to be associated with how wrong people perceived depicted immoral actions, but their empathic sadness was associated with paracingulate cortex activation instead, among other regions (Decety et al., 2012).

approach has been to probe altruistic decisions compared with selfish decisions. If moral sentiments play a role in motivating these decisions, then one should find partly overlapping areas of brain activation.

Moral versus Selfish Decisions Figure 2 describes how people were asked to donate to charitable organizations while being in the fMRI scanner (Moll et al., 2006). They were presented with different payoffs for the organization and for themselves and could choose whether they wanted to accept the payoff or not. This allowed the identification of specific neural signatures within the septalsubgenual cingulate region of deciding to donate to charity compared with keeping money for oneself. The frontopolar and anterior orbitofrontal cortex were associated with sacrificing one’s money to either donate or punish an organization (i.e., costly decisions). Both monetary rewards and donation decisions were associated with ventral striatum activations. Interestingly, the lateral orbitofrontal cortex was associated with punishing organizations people disliked (e.g., the US National Rifle Association). The septal part of the nucleus accumbens, which is its medial aspect and often overlooked in imaging studies by describing this as ventral striatum activation, was subsequently detected for donation decisions in two fMRI studies (Hsu et al., 2008; Harbaugh et al., 2007). The subgenual cingulate region was also found to be more active in people with higher empathic concern while they made decisions to sacrifice some of their money to help others to avoid an electroshock (Feldman Hall et al., 2012).

Affiliative Motivational States Other-Critical (other-Blaming) Moral Sentiments Moral disgust (highly associated with contempt in the authors’ pilot studies) and moral anger (highly associated with indignation) are important to motivate altruistic punishment, which is of immense evolutionary importance as discussed. The most reproducibly activated region for these feelings is the lateral orbitofrontal cortex (other-critical vs prosocial moral sentiments (Moll et al., 2007); indignation/anger when being the victim of an action vs guilt when being the agent (Zahn et al., 2009c)). It remains unclear, however, whether regions within the lateral orbitofrontal cortex are selectively involved in other-critical feelings. This is because one study found moral disgust to activate this region more strongly than nonmoral disgust (Moll et al., 2005a), whereas another study found the lateral orbitofrontal cortex activated for both moral and nonmoral disgust compared with a neutral condition (Borg et al., 2008). Another study did report the frontopolar cortex for anger toward others when compared with anger toward self, but there was no comparison with prosocial moral sentiments to directly relate the results to the studies above (Kedia et al., 2008). Loss of anger and disgust were selectively associated with neurodegeneration of posterior dorsomedial prefrontal, dorsal anterior cingulate, and amygdala, when controlling for performance on pity, guilt, and embarrassment (Moll et al., 2011). While the above studies tested the neural correlate of the subjective experience of specific moral sentiments, another

One basic ingredient for empathic moral sentiments such as pity, guilt, as well as moral decisions based on these feelings is the ability to feel attached to other people (Moll et al., 2008; Moll and Schulkin, 2009). Social attachment such as pair bonding and mother–offspring bonding has been linked to subcortical structures in nonhuman animals (Insel and Young, 2001; Stack et al., 2002). The core subcortical areas implicated in social attachment in nonhuman animals include the preoptic-anterior hypothalamic area, septal region, amygdala, ventral striatum, and the bed nucleus of stria terminalis (Stack et al., 2002). These regions are rich in neuropeptide and monoaminergic receptors (oxytocin, vasopressin, dopamine, and opioid) that have been shown to influence attachment-related behaviors. Human fMRI studies on maternal and romantic love found activation of these key subcortical regions (Bartels and Zeki, 2004; Aron et al., 2005; Swain et al., 2007). A recent study confirmed the prediction that there are regions selectively involved in affiliative emotional/motivational states within the hypothalamic-septal region irrespective of positive or negative emotional valence and irrespective of the context of agency (Moll et al., 2012). This is in keeping with the fronto-temporo-subcortical integration model of moral motivation as arising from decontextualized (i.e., free floating) motivational states in subcortical areas that are bound together with conceptual and sequential action information in anterior temporal and frontal areas to produce the complex experience of moral sentiments and

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Figure 2 Brain regions activated when participants donated or were opposed to donate to charitable organizations during fMRI (Moll et al., 2006; figure adapted from Moll, J., Schulkin, J., 2009. Social attachment and aversion in human moral cognition. Neuroscience and Biobehavioral Reviews 33, 456–465). (a) Both pure monetary rewards and decisions to donate (with or without personal financial costs) activated the mesolimbic reward system, including the ventral tegmental area (VTA) and the ventral and dorsal striatum. (b) The septal-subgenual region (SG), however, was selectively activated by decisions to donate, as compared with pure monetary rewards (both by costly and noncostly decisions, conjunction analysis). The lateral orbitofrontal cortex (latOFC) was activated by decisions to oppose charities. This activation extended to the anterior insula and to the inferior dorsolateral prefrontal cortex (PFC) and was present both for costly and noncostly decisions (conjunction analysis). The frontopolar cortex (FPC) and ventral medial PFC (mPFC) were activated for costly decisions (when voluntarily sacrificing one’s own money either to donate to a charity or to oppose it (conjunction analysis).

motivations (which always entail a goal rather than just the free-floating motivational state, see Figure 4).

Moral Values Moral sentiments are often tied to abstract values described by social concepts such as ‘honesty.’ They thereby form moral values, which motivate behavior in a more stable way than the context-dependent rules about certain types of behaviors we feel guilty or proud of in particular situations. The right superior anterior temporal lobe was shown to be equally activated irrespective of the type of moral sentiment (guilt, pride, gratitude, and indignation) associated with sociomoral values, whereas different frontal-subcortical regions were associated with the different moral sentiments (Figure 3, (Zahn et al., 2009c)). This provides a neural architecture that allows social conceptual knowledge to be integrated with moral sentiments to give rise to the experience of moral values and thereby motivate behavior.

Process-Based Subdivisions Frontopolar and anterior dorsolateral prefrontal cortices were consistently found for moral judgment/reasoning tasks (Greene et al., 2004, 2001; Moll et al., 2001). It is unclear, however, whether these activations were selective for moral relative to nonmoral judgment (as compared, for example, in (Moll et al., 2001)), because moral judgments were carried out on moral contents and nonmoral judgments on

nonmoral contents, thus confounding process and content. In other approaches to moral judgments, different types of moral dilemmata were compared that differed in contents and were designed to probe different types of processes (Greene et al., 2004, 2001), but again confounding contents with process. The different theoretical interpretations of these findings will be briefly discussed in Section CognitiveAnatomical Models of Moral Cognition and Emotion. These data do not, however, allow the conclusion that moral reasoning as a process has a specific neuroanatomical substrate. Other investigators have sought to identify differences in implicit and explicit (Harenski and Hamann, 2006) moral cognition or real versus imagined moral decisions (Feldman Hall et al., 2012). While these may undoubtedly exist, these studies did not investigate whether the difference between these types of processing were selective for moral or social processing, which is the focus of this article.

Cognitive-Anatomical Models of Moral Cognition and Emotion Anterior dorsolateral prefrontal and frontopolar cortex were found to be activated in moral judgment tasks (Greene et al., 2004, 2001; Moll et al., 2001), but as discussed, there is no evidence for their selective involvement in moral versus nonmoral judgment. The frontopolar cortex does show selectivity for guilt compared with other-critical feelings

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Figure 3 Using fMRI in healthy participants this study investigated the neuroanatomical basis of abstract moral and social values (figure adapted from Zahn, R., Moll, J., Paiva, M.M.F., Garrido, G., Krueger, F., Huey, E.D., Grafman, J., 2009c. The neural basis of human social values: evidence from functional MRI. Cerebral Cortex 19, 276–283; Zahn, R., Oliveira-Souza, R., Moll, J., 2011. The neuroscience of moral cognition and emotion. In: Decety, J., Cacioppo, J. (Eds.), The Handbook of Social Neuroscience. Oxford University Press). Participants had to imagine actions in accordance with or counter to a value described by a written sentence and to decide whether they would feel pleasantly or unpleasantly about the action. After the scan, they rated the unpleasantness/pleasantness on a scale and chose labels that best described their feelings (the analysis compares each moral sentiment vs visual fixation and vs two other moral sentiments; only selective effects were reported). There were four experimental conditions: (1) positive self-agency: “Tom (first name of participant) acts generously toward Sam (first name of best friend)” – pride in this condition was associated with ventral tegmental, septal, and ventral medial FPC activation (not depicted); (2) positive other-agency: “Sam acts generously toward Tom” – gratitude in this condition was associated with hypothalamic activation; (3) negative self-agency: “Tom acts stingily toward Sam” – guilt in this condition was associated with subgenual cingulate cortex as well as ventral medial FPC activation (not depicted and only when modeling individual frequency of guilt trials); and (4) negative other-agency: “Sam acts stingily toward Tom” – indignation/anger in this condition was associated with lateral orbitofrontal/insular activation. In the center, one can see the right superior anterior temporal lobe (aTL) region showing equally strong activation during all moral sentiment and agency contexts; this region showed increased activity with increasing richness of conceptual details describing social behavior and is identical to the activation found in a semantic judgment task (Zahn et al., 2007). These results confirmed the right superior anterior temporal lobe as a context-independent store of social conceptual knowledge that allows us to understand the core meaning of social and moral values regardless of what exact feelings or actions one ties to the value.

(see above) and was also activated for affiliative versus nonaffiliative feelings (Moll et al., 2012). It is therefore unlikely to be involved in the process of judgment itself. Unpublished secondary data analyses show that frontopolar activations in the latter study were associated with the number of consequences people thought about during scanning as based on postscanning ratings. This confirms the prediction of the fronto-temporo-subcortical integration model that frontopolar activations contribute to moral cognition by representing consequences of one’s actions (Figure 4), a crucial ingredient of affiliative moral sentiments (i.e., guilt and pity). It remains controversial how to interpret frontal activations in moral cognition and emotion; the different models are briefly summarized in Table 1. Further details of the fronto-temporo-subcortical integration model of moral cognition and emotion are found in Figure 4. This model currently provides the most parsimonious explanation for different cortical activation patterns for different types of moral sentiments (guilt vs indignation). Furthermore, it is so far the only model predicting subcortical and cortical structures with selective involvement in moral motivations. This is consistent with the evidence presented in previous sections. The authors have provided a more detailed discussion of how different models explain the evidence regarding moral dilemma choice paradigms elsewhere (Moll et al., 2008).

Implications for Differential Vulnerability in Psychiatry The application of moral neuroscience to the study of psychiatric disorders is still in its infancy. It is likely, however, that moral neuroscience will play an important role in understanding differential vulnerability to certain psychiatric disorders. Here, the authors will focus on major depressive disorder (MDD), especially, its melancholic subtype, on the hypermoral, and psychopathy on the hypomoral end of a putative spectrum. This is a highly speculative perspective, but may prove fruitful for designing future experiments to probe this further. Psychopathy has been long conceived of as a disorder of moral motivation with a lack of guilt and pity while leaving the ability to manipulate others for one’s selfish needs intact (Cleckley, 1976). Callousness in patients with psychopathy (Hare, 2003) was indeed found to be associated with gray matter volume reduction in a network of brain regions including the frontopolar and subgenual cortex (de OliveiraSouza et al., 2008). The anterior subgenual cortex was also found to be less activated in response to moral violationdepicting pictures in incarcerated people with psychopathy compared with a control group (Harenski and Hamann, 2006). The right anterior temporal lobe was another area of abnormal activation in this study and showed gray matter volume loss in a further study in people with psychopathy

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Figure 4 Brain regions involved in moral functions based on evidence from brain lesions and functional neuroimaging (adapted from Zahn, R., Oliveira-Souza, R., Moll, J., 2011. The neuroscience of moral cognition and emotion. In: Decety, J., Cacioppo, J. (Eds.), The Handbook of Social Neuroscience. Oxford University Press; Moll, J., and Schulkin, J., 2009. Social attachment and aversion in human moral cognition. Neuroscience and Biobehavioral Reviews 33, 456–465; Moll, J., Zahn, R., de Oliveira-Souza, R., Krueger, F., Grafman, J., 2005b. Opinion: the neural basis of human moral cognition. Nature Reviews Neuroscience 6, 799–809). Cortical region: frontopolar cortex (FPC), medial and lateral ventral prefrontal cortex (PFC), right anterior dorsolateral PFC, anterior temporal lobes (aTL), and posterior superior temporal sulcus (pSTS). Subcortical structures include the extended amygdala, hypothalamus, basal forebrain (especially the preoptic and septal regions), basal ganglia, and midbrain regions. Integration across these corticolimbic structures gives rise to event-feature-emotion complexes (EFEC) by temporal binding according to the fronto-temporomesolimbic integration model (Moll et al., 2005b). The hypothesized cognitive-anatomical components are the following: (1) sequential knowledge of actions/events represented within PFC subregions. FPC: complex branching of consequences of actions and ventral PFC regions representing associative knowledge of motivational/emotional states embedded into sequential event/action contexts; (2) social sensory features stored in pSTS and abstract (i.e., context-independent) conceptual knowledge of social behavior stored in the anterior temporal cortex, especially in the superior sectors; (3) central motive or basic emotional states, such as ‘free-floating’ anger, attachment, sadness, and sexual arousal (represented by the subcortical structures listed earlier).

Table 1

Alternative models of the role of frontal cortex in social and moral behavior

Hypothesis label

Main claim

Top-down frontal cognitive control

Frontal cortex does not store linkages between stimulus and response, but it represents goals that control the information flow in other cortical and subcortical areas when an automatic response needs to be overcome (Miller and Cohen, 2001). Ventral (medial) frontal cortex stores linkages of subcortical ‘somatic markers’ and action knowledge in posterior brain areas. Explains problems with rapid and complex decision making after ventral (medial) frontal lesions (Bechara et al., 2000). Context-dependent knowledge of sequences of social actions/events is stored in ventral frontal (and frontopolar) cortex necessary to enable context-appropriate social behavior (Moll et al., 2005b). In this model, the frontal cortex stores sequential information linking stimuli and responses in different contexts.

Bottom–up subcortical control

Reciprocal fronto-temporo-subcortical integration

Three alternative models of frontal involvement in social and moral cognition are summarized. The influential cognitive control model has subsequently been extended to the moral domain as the dual-process model of moral cognition and emotion (Greene et al., 2004). The assumption of this model is that ‘rational’ or ‘cognitive’ processes relying on dorsolateral prefrontal and parietal cortex can be separated anatomically from ‘emotional’ processes relying on subcortical and ventromedial frontal areas. Therefore, the model predicts that rational and emotional processing of moral dilemmata leads to different choices. The authors have pointed out that the model fails to explain how different types of emotions (e.g., guilt and indignation) and different types of motivations (e.g., selfish vs moral) can be accounted for. The reciprocal fronto-temporo-subcortical integration model of moral cognition and emotion is based on representations of different types of contents within each brain area of the network. This allows for explaining dissociations between different types of contents relying on different parts of one larger brain area (Moll et al., 2008).

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(Muller et al., 2008). Frontopolar and anterior temporal lobe gray matter volume loss were reproduced as the distinctive feature of people with psychopathy compared with people with antisocial personality disorder, but no psychopathy (Gregory et al., 2012). The right uncinate fascicle, a white matter tract connecting temporal poles, ventral frontal cortices, and subcortical structures, was found to show decreased structural connectivity in people with psychopathy (Eslinger et al., 2004), which may be a result of the cortical changes described above or vice versa. MDD is associated with overgeneral forms of empathybased interpersonal guilt (e.g., ‘feeling responsible for everything,’ (O’Connor et al., 2002)), which remained detectable on remission of symptoms in a group of primarily melancholic subtype patients (Green et al., 2013) suggesting this as a trait vulnerability factor. One hypothesis is that increased guilt proneness in MDD may have an influence on helping behavior outside of depressive episodes (O’Connor et al., 2002). This link has so far, however, not been conclusively demonstrated and the overgeneral and uncontrollable nature of self-blame as proposed in an influential cognitive model of MDD (Abramson et al., 1978) could lead to the opposite prediction of a propensity to withdraw from helping others (Tangney et al., 2007). Overgeneralization of guilt (i.e., feeling guilty for everything and thus hating oneself as a result) was associated with functional disconnection of the right superior anterior temporal lobe and the septal-subgenual cingulate region in people with MDD whose symptoms had subsided (Green et al., 2012). This functional disconnection was only present for guilt and not for indignation, thus confirming the selectivity for overgeneral self-blame, explaining the relatively infrequent occurrence of violence in people with pure major depression (Green et al., 2013). This confirmed the prediction of frontotemporal integration as critical for adaptive moral motivations (Moll et al., 2005b). Further studies of neural correlates of moral sentiments in affective disorders are needed to confirm and extend these findings.

Conclusions and Future Directions The authors have presented evidence that the septalsubgenual cingulate and septohypothalamic area are currently the best candidates for hosting subregions with selective involvement in moral versus selfish motivations. The authors have further reviewed the reproducible involvement of the frontopolar cortex for prosocial moral sentiments relative to other-critical sentiments. None of the other brain areas activated in moral cognition and emotion tasks were yet shown to be credible candidates for selective involvement in moral relative to nonmoral motivations. Social knowledge as a critical prerequisite of moral cognition and emotion is only partly understood in that its context-independent (i.e., conceptual) aspects can be localized within the right anterior temporal lobe. Future studies are needed to confirm these findings and to extend the understanding of the functional contribution of different frontal brain regions. An exciting future of applying these new insights to an improved

pathophysiological understanding psychiatric disorders lies ahead.

and

treatment

of

See also: Cortical Areas Engaged in Movement: Neuroimaging Methods; Depression; Emotion in Cognition; Emotion, Perception and Expression of; Heuristics in Social Cognition; Limbic System; Moral Development, Cultural Differences In; Moral Development, Theories of; Morality: Evolution of; Prefrontal Cortex Development and Development of Cognitive Function; Prefrontal Cortex; Psychopathy.

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