Social attachment and aversion in human moral cognition

Neuroscience and Biobehavioral Reviews 33 (2009) 456–465

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Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev

Review

Social attachment and aversion in human moral cognition Jorge Moll a,*, Jay Schulkin b,1 a b

Cognitive and Behavioral Neuroscience Unit, LABS-D’Or Hospital Network, Rio de Janeiro, RJ 22281-080, Brazil Departments of Physiology and Biophysics and Neuroscience, Center for Brain Basis of Cognition, Georgetown University, School of Medicine, Washington, DC 20007, USA

A R T I C L E I N F O

A B S T R A C T

Article history: Received 10 March 2008 Received in revised form 28 November 2008 Accepted 8 December 2008

Modern neuroscience is beginning to substantiate Darwin’s notion that the roots of human morality lie in social instincts, present in several species. The role of primitive motivational–emotional systems in human morality still remains under-recognized, however. Based on recent experimental evidence and classic neuroanatomical data, we here portray a view of how ‘‘ancient’’ limbic–neurohumoral systems of social attachment and aversion are crucially involved in human moral behaviors, including altruism, empathic concern and aggression. Rather than being a mere evolutionary remnant of our ancestors, such limbic–neurohumoral systems are tightly integrated with cortical mechanisms to enable complex moral sentiments and values, which powerfully influence our choices in socio-cultural settings. Exploring the underlying mechanisms of human social attachment and aversion will provide new insights and foster novel experimental paradigms for the study of moral cognition and behavior. ß 2008 Elsevier Ltd. All rights reserved.

Keywords: Attachment Social Moral Cognition Emotion Anti-social Disgust Prefrontal cortex Limbic

Contents 1. 2. 3. 4.

5.

6.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neuroscience and moral judgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The role of moral sentiments and values in moral judgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neurohumoral systems and morality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Social attachment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Social aversion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The roles of reason and emotion in morality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Cognitive control in moral judgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Cognitive–emotional integration in moral judgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion and future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction An intuitive sense of fairness, concern for others, and observance of cultural norms permeates human social existence (Smith, 1759/1966; Kant, 1790/1956; Sabini and Schulkin, 1994).

* Corresponding author. Tel.: +55 21 2538 3641; fax: +55 21 2538 3630. E-mail addresses: [email protected] (J. Moll), [email protected] (J. Schulkin). 1 Tel.: +1 202 862 2504; fax: +1 202 554 4346. 0149-7634/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2008.12.001

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This social sensibility is the essence of human morality, which emerges from sophisticated integration of cognitive, emotional and motivational mechanisms (Moll et al., 2005a,b) which are shaped through cultural exposure (Kagan, 1984; Zeki and Goodenough, 2004). Morality is thus a product of our cultural and biologic evolutionary history and represents an important adaptive element for social cohesion and cooperation (Darwin, 1871/1982; Brothers, 1990). By refraining from satisfying his immediate self-concerned desires and opting for socially enhancing actions instead, a member of a social group increases his own reputation, and becomes more likely to be supported by his

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comrades in the future (Trivers, 1971; Frank, 1988; Nowak and Sigmund, 2005). How exactly nature implemented such mechanisms in our brains is a mystery that is beginning to be unveiled. In recent years, neuroscientific research has started to provide important contributions to the knowledge of fundamental aspects of human morality. However, there is still a critical need of better conceptual integration of these preliminary hints with other lines of evidence. We here provide a view on (a) the organization of primitive neurohumoral emotional and motivational mechanisms involved in social attachment and aversion, present in several species; (b) how these neurohumoral mechanisms interact with isocortical ones to enable moral judgments, sentiments and values humans; and (c) how this view on the functional organization of human morality may help sharpen future research questions. To this aim, we will first briefly review new lines of evidence of neuroscience of morality, with special emphasis on the role of evolutionarily ‘‘ancient’’ neurohumoral systems, and how they relate to uniquely human manifestations of morality. 2. Neuroscience and moral judgment The first clues that the moral faculties of the mind could be impaired while leaving overall cognition intact came from occasional reports of acquired brain damage causing morally improper behaviors in formerly socially adjusted individuals (Macmillan, 2000). Interest in this issue was reawakened more recently by systematic studies of acquired personality changes due to brain damage, mostly to the frontal lobes (Eslinger and Damasio, 1985; Saver and Damasio, 1991; Tranel et al., 2002). Given the similarities with developmental psychopathy (Cleckley, 1976; Hare, 2003), such impairments in social conduct were dubbed ‘‘acquired sociopathy’’ (Saver and Damasio, 1991). A review of lesion studies of patients with acquired sociopathy and preserved general cognitive abilities showed, however, that current models of normal social conduct have emphasized the prefrontal cortex (PFC) at the expense of other brain regions (Moll et al., 2003). During the past few years, however, a number of functional magnetic resonance imaging (fMRI) studies on normal volunteers have contributed rich material for our understanding of the moral brain. In an early experiment investigating the neural underpinnings of moral judgment, volunteers were scanned during the auditory presentation of short statements, on each of which they were asked to make silent categorical judgments (right vs. wrong) (De Oliveira-Souza and Moll, 2000; Moll et al., 2001). Some statements had an explicit moral content (The judge condemned an innocent man), while others were factual statements without moral content (Telephones never ring). When the moral condition was contrasted to the factual one, the medial frontal gyrus and medial and lateral sectors of the frontopolar cortex (FPC), isocortical regions that are especially well-developed in our species (Allman et al., 2002), were strongly activated. The right anterior temporal cortex (aTC) and the left angular gyrus/superior temporal sulcus (STS) region were also strongly activated by moral judgments. Effects on these cortical regions could not be explained on the basis of overall emotional arousal, as additional analyses revealed. Subsequently, Greene and colleagues (Greene et al., 2001) probed another important aspect of moral judgment using fMRI. Normal subjects were exposed to moral and non-moral dilemmas that were structurally more complex than the simple statements described above, imposing a higher load of reasoning and conflict. Moral dilemmas were divided into moral-personal (the agent directly inflicts an injury to another person to avoid a worse disaster) and moral-impersonal (the agent does it in indirect ways, such as by pressing a button). The moral-personal condition, to a greater extent than the moralimpersonal condition, evoked a similar pattern of activation as the

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one described in Oliveira-Souza and Moll’s study. Since then, several other studies have addressed additional key issues in moral judgments, including the contribution of general emotional arousal, presence of bodily harm, response times, semantic content, cognitive load, conflict, intention, consequences vs. means, emotional regulation, justice vs. care-based judgments and interaction with theory of mind (Berthoz et al., 2002; Moll et al., 2002a,b; Heekeren et al., 2003; Greene et al., 2004; Heekeren et al., 2005; Borg et al., 2006; Harenski and Hamann, 2006; Robertson et al., 2007; Young et al., 2007). These studies have significantly extended our knowledge on the neural substrates of moral judgment and emotions, emphasizing the consistent involvement of lateral and medial sectors of the orbitofrontal cortex (OFC), FPC, amygdala, precuneus, STS region and aTC. Despite these advances, which were made possible in large part due to a substantial development in functional imaging techniques, the role of subcortical/limbic structures in morality still remains obscure. This can be explained both by technical limitations (fMRI is intrinsically less sensitive to detect activity in those regions) and by the lack of robust models and detailed knowledge on the role of specific subcortical/limbic circuits and their functional relationships with isocortical regions in the context of human moral cognition. As we will show, recent experimental evidence and conceptual advances point to some interesting ways of further probing these relationships. 3. The role of moral sentiments and values in moral judgment One critical aspect of morality is that the ability to make ‘‘cool’’ moral judgments – for example, that one should treat children with care and respect the rights of others – does not necessarily translates into actual moral conduct. Rational moral judgment and outward behaviors often dissociate in normal people and, much more consistently and dramatically, certain patients with brain damage and psychiatric disorders (e.g., Eslinger and Damasio, 1985; Hare, 2003). What makes moral judgments translate into real-life action? Moral sentiments, which have long been recognized as a powerful motivational forces (Hume, 1739/ 1984; Smith, 1759/1966), stand out as strong candidates. Along with sentiments, personal commitment to values also plays a crucial role in moral behavior, though their psychological and biological underpinnings are still even less well understood. Social or moral values can be defined as social concepts which acquire intrinsic motivational salience for a given individual or society (e.g., honesty, courage, autonomy, benevolence; see Zahn et al., 2009). One fMRI study, which controlled for the effects of non-moral emotional arousal, provided initial clues on the functional anatomy of moral sentiments. In this study, participants were exposed passively to pictures that varied in their moral content and emotional salience (Moll et al., 2002b). Activation of the anterior insula, amygdala and subcortical structures were observed for both moral and non-moral unpleasant stimuli. The FPC, medial OFC and posterior STS region, however, were selectively activated by moral stimuli. The engagement of the same brain networks by morally salient stimuli independently of task contingencies across different studies suggested that such network may underlie a moral sensitivity mechanism, by which certain social situations automatically trigger moral sentiments (Moll et al., 2002b). Moral sensitivity allows humans to quickly apprehend the moral implications in a social situation depending on context, agency and consequences of one’s choices, through the experience of specific moral sentiments (Moll et al., 2007b; Schulkin, 2004, 2008). Moral sentiments have been shown to be culturally ubiquitous (Fessler, 1999; Shweder et al., 1987), despite the wide diversity of

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Table 1 Predicted relationships between moral sentiments and putative neurocognitive components. Affiliation/ attachment (present = P)

Guilt Shame Embarrassment Pride Indignation/anger (selfish) Indignation/anger (moral/empathic)) Contempt/disgust Pity/compassion Love/tenderness Awe/elevation Gratitude

P

P P P P P

Aversion (S = self, O = other)

S S (S)

Attribution of personal value/reputation (increased, +; decreased, )

Evaluation of action outcome of situation (good, +; bad, )

To self by another

To self

– – (+)

To self by oneself – –

(+) (+)

To other

–

–

( ) ( ) + –

–

( )

+ + +

(+) (+) +

+

O O O

(+)

To other by oneself

Agency for outcome (S = self, O = other)

(+) – ( ) – (+) (+)

S S (S) (S) O O (O) (O) (O) O O

Symbols (+, , P, S/O) indicate a key role of the respective cognitive–emotional variable in the genesis of the corresponding moral sentiment. When between brackets, symbols indicate that the role of the corresponding component for a given moral sentiment can be variable, dubious or just modulatory (but not essential).

how they can be tied to specific cultural and situational contingencies (Brown, 1991; Ehrlich, 2000). These sentiments are intrinsically linked to daily social interactions. Anticipated or actual violations of one’s own principles and beliefs trigger aversive feelings such as guilt and shame (Eisenberg, 2000). Standing up to one’s core values, on the other hand, will tend to trigger positive feelings such as pride and joy. Moral sentiments are thus strong motivators for human action in social contexts. Moral sentiments depend on the engagement of several cognitive processes, including action and conceptual knowledge, emotion and motivation, requiring a tight integration among human isocortical and limbic circuits (Moll et al., 2007a). As such, moral sentiments should neither be considered to be either purely ‘‘cognitive’’ or ‘‘emotional’’ (Parrott and Schulkin, 1993; Barton, 2004; Nichols, 2002; Phillips and Prinz, 2006), nor a simple sum of ‘‘cognition’’ and ‘‘emotion’’. It has been proposed that specific moral sentiments will be elicited depending on the precise recruitment of component neural and psychological processes (Moll et al., 2005b, 2007b), which include: basic forms of affiliative (attachment-related), anger, anxiety and hedonic states (Schulkin et al., 1998), agency, intentionality (Decety and Grezes, 2006) and prospective thinking and outcome prediction (Grafman, 1995; Schultz and Dickinson, 2000), among others (see Table 1). It has been postulated that such psychological states arise from integration of the above-mentioned components across largescale distributed networks by way of temporal binding mechanisms (Moll et al., 2005b; see Fig. 1), similarly to what has been shown for integrated visuo-spatial perception (Engel and Singer, 2001; Singer, 2001). Sentiments can be tentatively clustered on the basis of neurobiological and phenomenological components (Moll et al., 2007b). The ‘‘prosocial’’ cluster includes guilt, embarrassment, compassion, and gratitude, which promote cooperation, helping, reciprocity, reparative actions and social conformity. A subclass of those, the so-called empathic moral sentiments (guilt, gratitude and compassion), putatively share the attachment component, and play a central role in behaviors linked to emotional empathy (Batson, 1991; Batson et al., 1991; Eisenberg, 2000). On the other hand, sentiments linked to interpersonal aversion – the othercritical sentiments (disgust, contempt and anger/indignation) – are experienced when others violate norms or one’s ‘‘rights’’, and endorse aggression, punishment, group dissolution and social reorganization (Allport, 1954; Haidt, 2003; Moll et al., 2005a). Still, acting in accord to one’s own values often triggers self-praising sentiments – among which pride is the prototype, while witnessing praiseworthy actions of others will lead to the

experience of other-praising sentiments – gratitude when one is the recipient of such actions, and admiration when praiseworthy actions are directed to a third-party. Recent neuroimaging studies have started to reveal specific brain activation patterns associated with distinct types of moral sentiments (Moll et al., 2007a; Takahashi et al., 2008; Zahn et al., 2009). Although no one-to-one correspondence has been found between single brain regions and specific moral sentiments, certain regions do respond more reliably to certain clusters. The lateral OFC, anterior cingulate/ dorsomedial PFC and the anterior insula are more consistently activated by disgust and anger/indignation (social aversion) (Phillips et al., 1998; Wicker, 2003; Moll et al., 2005a; Zahn et al., 2009), whereas the FPC is more reliably activated by prosocial sentiments, including guilt, embarrassment and compassion (Takahashi et al., 2004; Moll et al., 2007a). Empathic sentiments (compassion and guilt) were found to be more selective for the subgenual/medial OFC, in addition to the FPC (Moll et al., 2007a; Zahn et al., 2009), whereas gratitude and pride activated mainly the septal–hypothalamic area (Zahn et al., 2009). Interestingly, the lateral OFC is also activated by guilt, perhaps due to self-aversive responses, and the anterior medial OFC/FPC were engaged by indignation when the ‘‘victims’’ were a third-party (‘‘empathic’’ indignation) (Moll et al., 2007a) and when punishing a ‘‘villain’’ (King et al., 2006) or a non-cooperator (De Quervain et al., 2004), i.e., when acting according to personal moral values (e.g., justice, reciprocity). 4. Neurohumoral systems and morality As reviewed above, moral judgment, sentiments and values critically involve motivational–emotional neural mechanisms which have a long evolutionary history. Although these mechanisms are known to play fundamental roles in the regulation of social and motivated behavior of several social species, their putative relationships to human morality are still poorly understood. Since Darwin, the question of whether our prosocial moral instinct is unique among species has been actively pursued. There is general consensus today that the building blocks of morality have strong evolutionary bases. The origins of morality need thus to be sought among certain primitive motivational–emotional mechanisms that can readily be identified in other social species. These mechanisms can be operationally organized into two broad classes: one linked to approach and affiliation, and the other linked to aversion and rejection. While attachment promotes care, cooperation and reciprocity toward in-group members, aversion

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Fig. 1. Brain regions implicated in human moral cognition. Cortical regions implicated in moral cognition include the sectors of the prefrontal cortex (frontopolar, medial and lateral orbitofrontal cortex, anterior dorsolateral prefrontal cortex and additional ventromedial regions), the anterior temporal lobes, and the superior temporal sulcus/ temporo-parietal junction (Weissenberger et al., 2001; Moll et al., 2002a,b, 2003). Subcortical structures include the extended amygdala, hypothalamus, basal forebrain (especially the septal region), ventral striatum-pallidum, subgenual region and the rostral brainstem tegmentum. It has been postulated that integration across these corticolimbic structures gives rise to event–feature–emotion complexes (EFEC), possibly by temporal binding mechanisms. Main components include: (1) action/event sequence knowledge (provided by representations within specific prefrontal subregions; (2) social perceptual features (stored in posterior sectors of the temporal cortex, especially the superior temporal sulcus/temporo-parietal junction) and conceptual knowledge of social behaviors (stored in the anterior temporal cortex, especially in the superior region); and (3) central motive or basic emotional states (Stellar, 1954/1994), such as anger, attachment, sadness and sexual arousal (provided by the limbic structures listed above). The picture also illustrates how compassion, a specific moral sentiment, can emerge in a given situation (e.g., visiting an orphanage) through integration across specific subcomponents of the moral cognition network. The PFC enables prospective assessments (for example, this orphan child will likely face several difficulties throughout her life), while the superior temporal sulcus/temporo-parietal junction and the anterior temporal cortex contribute with social perceptual (sad facial expression and body posture) and conceptual social knowledge (understanding ‘‘helplessness’’ and ‘‘loneliness’’), respectively. Limbic regions contribute with the experiential ingredients of sadness, anxiety and attachment. The full-blown subjective experience of compassion, as well as of other moral sentiments, depends on the functional integration across these key cognitive–affective components.

fosters blame, prejudice and group dissolution (De Waal, 1998; Schulkin, 2000). A critical step of human evolution might have involved the functional adaptation of basal forebrain–limbic circuits linked to social attachment and aversion, which are readily identified in other species, and their integration with greatly expanded isocortical regions. Intertwining of social attachment/aversion and complex social knowledge through cultural learning became thus a unique feature of human nature (Han and Northoff, 2008; Moll and de Oliveira-Souza, 2008). These aspects will be articulated in more detail below. MacLean (1990) proposed a demarcation among the neomammalian, paleo-mammalian, and reptilian levels to account for the evolution of the brain. According to this perspective, the

human neural axis is a repository of phylogenetic layers, starting with the reptilian brain (‘‘basic instincts’’, e.g., aggression and sex), which is enveloped by the paleo-mammalian brain (limbicmediated emotions), then crowned by the neo-mammalian and the expanded human neocortex. The burden of scientific evidence, however, challenged the validity of such hierarchical, phylogenetically layered models originally proposed by 19th century thinkers and elaborated early 20th century researchers (e.g., Broca, 1863; MacLean, 1990), broadening the anatomy of the limbic system and its functional relationships to ‘‘higher’’ cognitive related to neocortical systems (see also Nelson and Panksepp, 1998; Herbert and Schulkin, 2002). The successful development of this broadened view of the limbic brain partially owes to the

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discovery of the chemical architecture of the central nervous system. Specifically regarding social behavior was the discovery of molecules (e.g., oxytocin, corticotrophin-releasing hormone, vasopressin) that exert central roles in prosocial and reward-related motivations (Carter et al., 1999; Nelson and Panksepp, 1998; Herbert and Schulkin, 2002). 4.1. Social attachment Attachment provides the basic ingredient for inter-individual bonding and affiliative behaviors, such as mother–offspring ties. This depends on subcortical and limbic structures, including the ventral striatum, septal nuclei, amygdala and hypothalamus (Insel and Fernald, 2004; Keverne and Curley, 2004; Carter et al., 1999). A broad array of neuropeptides contributes to attachment behaviors in animals. Neuropeptides which have a role in rewarding and affiliative states in animals include vasopressin, oxytocin, serotonin, cocaine- and amphetamine-regulated transcript (CART) peptide, dopamine and peptide Y (Carter et al., 1999; Herbert and Schulkin, 2002). Distinct peptides can promote prosocial behaviors in different ways: for example, neuropeptide Y acts on the ventral striatum and perifornical region and has both anxietyrelieving properties and rewarding effects, while oxytocin promotes social bonds and mediate animal contact and comfort (Insel and Young, 2001). Serotonin has also been shown to promote constructive social interactions by decreasing aggression, an effect that may be in part mediated through regulation of oxytocin expression (Young and Leyton, 2002). These mechanisms, we argue, are the key motivators of prosocial behaviors observed in the sophisticated sphere of human morality. Since similar mechanisms can be adapted to serve new functions during the evolution of a species, we hypothesize that the human proclivity to develop and attach to abstract sociocultural constructs such as moral values may spring from integration of more ‘‘primitive’’ motivational systems with complex cortical representations. Specifically, prosocial values, such as the ‘‘friendship’’ and ‘‘loyalty’’ and the dispositions they evoke in the agent, could emerge by connecting culturally shaped information represented in cortical structures (e.g., conceptual and action knowledge related to ‘‘friendliness’’ or ‘‘friendly manners’’, represented in frontal and temporal association cortex) with affiliative motivations arising from limbic circuits (Moll et al., 2005b; Zahn et al., 2009). This interaction of affiliative experience with social concepts (Zahn et al., 2007), social perceptual features and prediction of action outcomes thus provides the basis for sentiments such as compassion, guilt, gratitude and empathy (Eisenberg, 2000; Harris, 2003; Moll et al., 2005b). Recent studies have started to demonstrate the role of attachment-related neural mechanisms in humans. Structures of the brain reward system, i.e., the midbrain ventral tegmental area and ventral striatum, along with basal forebrain structures, were engaged when humans looked at their own babies or at romantic partners (Bartels and Zeki, 2004; Aron et al., 2005). Furthermore, other studies have provided causal evidence for the effects of oxytocin on human social behavior. In a sequential economic game involving trust, Zak et al. (2004) found that oxytocin levels were higher in subjects who received a monetary transfer signaling an intention to trust, in comparison to an unintentional monetary transfer of the same amount from another player. Higher oxytocin levels were associated with increased likelihood of reciprocation. Decreasing social anxiety or fear might also be an important effect of oxytocin, a hypothesis that was strengthened by a recent pharmacological fMRI study. In this study, Kirsch et al. (2005) showed that oxytocin attenuated amygdala activation to fearful stimuli. In another study, Kosfeld et al. (2005) showed that intranasal administration of oxytocin induced more cooperation in

an anonymous economic game by boosting interpersonal trust. In this game, the first player chooses to transfer an amount of money (if any) to another player. The amount is multiplied, and the second player may choose how much he/she will transfer back to the first player (i.e., reciprocation). Exogenous oxytocin administration was associated with increased amounts transfers in the trust game by first movers. A recent fMRI experiment provided evidence for a direct link between altruistic decision-making in cultural settings to the functions of the brain reward and social attachment systems. In this study, subjects were scanned while they made real-life decisions about whether to donate to or to oppose a number of charities (Moll et al., 2006). Decisions, depending on trial type, could be either financially costly or non-costly to the participant. In other trials, participants were able to receive ‘‘pure’’ monetary rewards (without consequences for the charities). The charities were associated with causes with important societal implications, such as abortion, children’s rights, nuclear energy, war and euthanasia. Both pure monetary rewards and decisions to donate activated the mesolimbic reward system, in agreement with the warm glow hypothesis – it feels good to be good (Andreoni, 1990); these findings were supported and extended by another recent investigation by Harbaugh et al. (2007), who showed that the mesolimbic system was also activated by ‘‘mandatory’’ donations. In addition, in Moll et al.’s study, a direct comparison of decisions to donate to the pure monetary reward condition revealed that donations selectively activated subgenual–septal area, which is intimately related to social attachment in other species (Freedman et al., 2000; Young and Wang, 2004; Carter et al., 1999) (Fig. 2). These findings extend the role of fronto-limbic networks in social cooperation from interpersonal economic interactions, as addressed by a number of studies (Sanfey et al., 2003; De Quervain et al., 2004; Singer et al., 2004; Delgado et al., 2005; King-Casas et al., 2005), to the realm of internalized values and preferences shaped by culture (for recent reviews, see Fehr and Camerer, 2007, and Sanfey, 2007). In another study, a pair of subjects played for money in a sequential trust game. In pairs of individuals who developed a strategic interaction, cooperating most of time but failing to trust when the financial ‘‘temptation’’ was high, the reward regions of the brain were more involved (e.g., the ventral tegmental area). In contrast, cooperation decisions in pairs who developed ‘‘unconditional trust’’ were accompanied by activation in the septal region, suggesting that genuine trust and commitment to cooperate is related to social attachment (Krueger et al., 2007). It should be emphasized that donation and cooperation decisions in the above-described experiments were fully rational but nonetheless engaged specific limbic circuits intimately associated with motivational–emotional mechanisms. 4.2. Social aversion Inter-individual aggression typically occurs in disputes concerning sex, territory, power and food, being necessary to guarantee individual survival in several species. In social animals, e.g., non-human primates, aggressive inclinations key for the building of complex social hierarchies of dominance and power, which regulate access to food resources, mating and other social privileges (Byrne and Whiten, 1988; De Waal, 1998). Social status marks one as a ‘‘good’’ or ‘‘poor’’ partner for future interactions and inclusion in social cooperation networks. In humans, from whom subjective feelings can be obtained, interpersonal aggression is typically accompanied by the experience of anger, frustration, disgust and contempt (Allport, 1954; Haidt, 2003; Rozin and Fallon, 1987). Neural and humoral systems underlying aggressive behaviors have been studied in several species, with extensive evidence pointing to the role of dopaminergic and serotonergic

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Fig. 2. Brain regions involved in donation and opposition to charitable organizations. Brain regions showing increased activation in a functional magnetic resonance imaging (fMRI) study of charitable donations to societal causes (such as abortion, children’s rights, nuclear energy, war and euthanasia). (a) Both pure monetary rewards (an experimental control condition) 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 sectors striatum (STR). (b) The subgenual–septal area (SG), however, was selectively activated by decisions to donate, as compared to pure monetary rewards (both by costly and non-costly 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, and was present both for costly and non-costly decisions (conjunction analysis). The frontopolar (FPC) and ventral medial prefrontal cortex (mPFC) were activated when volunteers made costly decisions, i.e., when they voluntarily chose to sacrifice own monetary resources either to donate to a charity or to oppose to it (conjunction analysis). (c) An additional analysis of covariance, previously not reported, explored the relationship between individual scores on the empathic concern subscale of the Interpersonal Reactivity Index scale (Davis, 1983) of participants and the activations evoked by costly donations to charity. Robust and anatomically specific effects (peak, R = 0.72, p = 0.0007; display R = 0.55) were restricted to the anterior medial OFC (medOFC).

pathways. In primates, both dopamine and serotonin exert modulatory effects of on social interactions, which depend on social status (Edwards and Kravitz, 1997; Morgan et al., 2002; Muehlenbein et al., 2004). Although enhanced dopaminergic and serotonergic action have been related to increased dominance, these neurochemical systems probably exert partially separable effects. Increased serotonergic activity decreases harm avoidance and hostility and increases dominance in human social interactions (Brody et al., 2000). It has been suggested that some of these serotonergic effects are regulated by oxytocin release and social contact, or through the corticotrophin-releasing hormone, linked to social withdrawal (Thompson et al., 2004). D2-class receptor dopaminergic antagonism leads to selective disruption in anger recognition in humans, in line with the importance of dopamine mediating aggression social-agonistic encounters (Lawrence et al., 2002). When tied to sophisticated social cognitive mechanisms of reputation assessment, prospective thinking and recognition of abstract rules, the primitive neurobiological substrates of anger may well be the core motivational force for instrumental and ‘‘moralistic’’ aggression in humans (Arsenio and Lemerise, 2004; Moll et al., 2005a). Several recent studies have linked violent behavior in humans to monoamine oxidase (an enzyme involved in metabolizing dopamine, norepinephrine and serotonin) genotype (the ‘‘low’’ type), with strong interactions with the presence of severe environmental stressors during childhood, in addition to serotonin and dopamine genotypes (Alia-Klein et al., 2008; Manuck et al., 2002; Volavka et al., 2004). Disgust also plays a central role in social aversion. Proto-forms of disgust, associated with non-social functions, can be found in non-humans. Distaste, nausea and vomiting occurring following exposure to potentially toxic or contaminated foods and odors have a clear adaptive function (Darwin, 1872/1965; Rozin and Haidt, 1993; Rozin, 1999). In humans, disgust and its close relative, contempt, play a clear role in interpersonal settings (Calder et al., 2001; Jones, 2007). In contrast to anger, disgust and contempt are slower to fade out; they tend to ‘‘stick’’ or to become

a property of the object, intensely devaluing it (Rozin et al., 1999; Haidt, 2003). Thus, in the same way that neural systems underlying primitive forms of pleasure and social bonding operate in highly complex social situations associated with human cooperation, neural systems underlying aversive responses related to physical properties of odors and foods seem to have been adapted to sustain social disapproval (Moll et al., 2005a). Indeed, while morality often promotes cooperation and helping, it can also steer hostility among individuals and social groups (Moll et al., 2003; Jones, 2007). The close affiliations between disgust detection and experience might help explain the similarities among the neural substrates of disgust perception (Phillips et al., 1998; Sprengelmeyer et al., 1998), experience (Wicker, 2003; Moll et al., 2005a; Mataix-Cols et al., 2008) and their impairments due to brain lesions (Sprengelmeyer et al., 1996; Sprengelmeyer, 2007). Moral sentiments and values powerfully incite people to challenge others’ beliefs (here defined as ideas and facts that are accepted based on the evaluation of their ‘‘truth’’ content) and ideologies (Allport, 1954; Vogel, 2004). Several studies have implicated a number of brain regions and circuits in social aversion, including brainstem regions, the amygdala, basal forebrain and hypothalamic nuclei, pirifom and cingulate/dorsomedial frontal cortex, and temporal and frontal connections (Mega et al., 1997; Volavka, 1999; Calder et al., 2001; Moll et al., 2005a). The lateral OFC and neighboring agranular insula, in particular, have been specifically implicated in interpersonal aversive mechanisms (Bechara et al., 2000; Kringelbach, 2005), including punishment of non-cooperators in economic interactions (Sanfey et al., 2003; De Quervain et al., 2004) and anger responses (Blair et al., 1999; Bechara et al., 2000). Brain regions involved with basic forms of disgust and with emotionally mediated social disapproval, such as moral disgust, appear to be largely shared (Moll et al., 2005a). Accordingly, decisions to oppose a charities linked to societal causes, whether at a personal cost or at no cost, were associated with activity in the lateral OFC and anterior insula, in keeping with the suggestion that basic aversive

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mechanisms have been adapted to enable ‘‘culturalized’’ forms of disapproval (Moll et al., 2006) (see Fig. 2). Social psychology has long established that there are implicit and explicit mechanisms of social aversion in humans (Festinger, 1962; Sabini, 1982). Recent neuroimaging evidence revealed that brain systems involved to social aversion, including the insula, lateral OFC and amygdala, are recruited by mechanisms of racial bias and social exclusion, both in the brains of the agent and the target of prejudice (Eisenberger et al., 2003; Lieberman et al., 2005). Strong attachment to in-groups and lack of attachment to out-groups can be an important factor for the development of negative beliefs towards out-groups, unlocking social aversion mechanisms associated with emotions such as contempt, anger and disgust (Rozin and Haidt, 1993; Rozin, 1999). 5. The roles of reason and emotion in morality There is now little question about the importance of reason and emotion in human morality. However, debate remains concerning how cognition and emotion interact in moral judgment and behavior. According to one view put forth by Greene et al. (2004), in situations involving decision conflicts reason and emotion may conflict with each other. In such situation, a cognitive control mechanism must be invoked to overcome emotional biases so that a rational decision can be made. In contrast, another view proposes that emotion and reason normally operate in an integrative fashion in moral decisions, including in situations of conflict (Moll and de Oliveira-Souza, 2007). These distinct views are addressed and confronted below. 5.1. Cognitive control in moral judgment There is a long tradition in philosophy and psychology supporting the division of mental processes into two broadly separable types: (1) rational, effortful and explicit, and (2) intuitive, emotional and quick (De Neys and Glumicic, 2008). Such view is expressed in several modern psychological accounts which pit rational or cognitive processes against intuitive and emotional ones in the context of decision conflict (Kahneman and Frederick, 2007; Sunstein, 2005). According to the cognitive control and conflict theory of moral judgment (Greene et al., 2004), cognition and emotion will compete for behavioral output when pre-potent responses arising from ‘‘emotional brain regions’’ favor one outcome while ‘‘cognitive brain regions’’ favor another (Kahneman and Frederick, 2007; McClure et al., 2007). This dualprocess view is particularly intuitive: when faced with difficult choices – say, admitting a mistake or getting away unnoticed after misbehaving – we vividly experience a feeling of conflict. Failing to admit a mistake can thus be naturally interpreted as a failure of this control mechanism over our emotional responses. In fact, it has been consistently demonstrated that PFC lesions can lead to poor judgment, ‘‘disinhibition’’ and impaired decision-making (see Grafman, 1995 and Miller and Cohen, 2001 for reviews). This is the central tenet of the ‘‘central executive’’ concept, an over-arching controller of our behaviors that guides our choices according to performance criteria (Shallice and Burgess, 1996). Executive abilities include diverse specific cognitive functions such as behavioral inhibition, selective attention, working memory and cognitive control, among other sub-processes (Miller and Cohen, 2001). The PFC is known to be particularly important when we face unexpected and novel situations, especially when different behavioral options can be made. In line with this proposal, the cognitive conflict and control model of moral cognition postulates that sectors of the DLPFC, along with more posterior cortical areas, exert top–down control over ‘‘emotional brain regions’’, including the amygdala and medial PFC sectors (Greene et al., 2004). Rational

judgments in morally conflicting settings are believed to arise from successful inhibition or control of pre-potent emotional responses by cognition, whereas emotion-based choices would result from a failure of this suppression mechanism (McClure et al., 2007). Although the dual-process view is still widely supported, several investigators from fields of moral psychology and philosophy (Nichols, 2002; Pizarro and Bloom, 2003; De Neys and Glumicic, 2008) and neuroscience (e.g., Moll and de Oliveira-Souza, 2007) have raised important concerns on the validity of this arbitrary dissociation of cognition and emotion, as we discuss below. 5.2. Cognitive–emotional integration in moral judgment Sometimes behaviorally salient situations are straightforward, so that actions driven by automatic motivational–emotional mechanisms can be taken swiftly. In many occasions, however, complex contextual demands make behavioral choices difficult, and basic emotional responses can be insufficient to ensure appropriate behavioral choices. In the context of moral decisionmaking, moral dilemmas are the prototypical example. Moral dilemmas invoke dissonant choices of comparable motivational relevance, giving rise to a slow and effortful process that can be dubbed moral calculus (Gottfried, 1999; Moll et al., 2003). Moral dilemmas require a careful analysis of available choices according to outcomes and side effects, and how they relate to personal preferences and values. Such considerations depend on a host of higher-order cognitive abilities, which include prospective evaluations, cognitive flexibility and priority judgments. These rational processes, however, work in the service of goals which are, in essence, motivationally relevant. This is the subtle but essential element that distinguishes this integrative view from the cognitive control approach: true behavioral choices cannot be split into cognitive vs. emotional. In the context of classical moral dilemmas, choosing to kill or not one innocent to save five other lives represents the struggle between suffering the angst of becoming a murderer or, instead, bearing the responsibility of letting five people die because of an act of omission. This interpretation is in agreement with the finding that the PFC is spontaneously engaged whether or not decisions or behavioral outputs are required in moral scenarios, suggesting that the PFC does not merely manipulate information stored elsewhere in the brain, but in fact represents certain aspects of social knowledge, motivation or action. Recent neuroimaging studies showed that the PFC is involved in both voluntary enhancement and reduction of emotional experience (Ochsner et al., 2004; Kim and Hamann, 2007). It has been proposed that the PFC may play a central role in enabling the experience of moral sentiments and values, not through competition between cognitive and emotional mechanisms but through their integration. One proposed physiological mechanism for the interactions among cortical and subcortical– limbic brain regions is increased connectivity across this largescale network (Moll et al., 2005b) by way of temporal binding (Singer, 2001). Accordingly, one core aspect of most cortical regions, including the PFC, is their vast bi-projectional input to and from subcortical regions, an information processing feature that is central for the organization of action. This pattern of neural connectivity alone speaks against a strict ‘‘top–down’’ view. Recent investigations on brain-damaged patients have provided interesting clues on these aspects. Two independent studies demonstrated that patients with ventromedial PFC (VMPFC, including the medial OFC and FPC) damage tend to opt, more often that control subjects, for ‘‘utilitarian’’ choices in highly conflicting moral dilemmas (Ciaramelli et al., 2007; Koenigs et al., 2007). One possible interpretation would be that the emotional blunting observed in these patients might render them less sensitive to immediate emotional reactions. In other words,

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reduced aversive emotional experience when choosing to sacrifice an innocent person in order to save five other ones would favor ‘‘rational’’ or utilitarian choices (e.g., killing one instead of five). Intriguingly, another study in which patients with VMPFC damage played the Ultimatum game, an economic decision-making task, demonstrated the opposite behavioral pattern. When faced with the choice of accepting (or not) unfair but financially rewarding monetary offers from an anonymous player, patients tended to reject such offers, thereby punishing the non-cooperators and losing money (Koenigs and Tranel, 2007). Such costly choices are believed to arise from emotional arousal, being less ‘‘rational’’ according to standard economic theory. As discussed by Koenigs et al. (2007), these findings can neither be explained by overall emotional blunting and disruption of autonomic somatic markers (Damasio et al., 1990) nor by competing cognition and emotion processes (Greene et al., 2004). A more parsimonious explanation (Moll et al., 2007a) would be that these patients suffer from a selective deficit in experiencing prosocial sentiments such as guilt and compassion, while showing a relative preservation of othercritical sentiments, such as indignation and contempt – i.e., a dissociation within the moral sentiment domain. In sum, these findings point more strongly to function segregation between prosocial sentiments (associated with affiliative components, such as guilt and compassion) and socially aversive sentiments (indignation, contempt; Moll et al., 2005b, 2007a), than to dissociation between cognition and emotion in guiding moral evaluations. The hypothesis that an intact VMPFC is more critical for experience of prosocial, whereas dorsal and orbito-lateral sectors of the PFC are more relevant for socially aversive sentiments needs to be tested in future lesion and neuroimaging studies. In summary, these data support the notion that moral judgments and sentiments both rely on a close interplay of cortical and limbic circuits. Although some brain regions are intimately tied to motivational/regulatory mechanisms and others are less so, this does not imply clear anatomical boundaries (Pessoa, 2008) or hierarchical top–down relationships between cognition and emotion. Competition between behavioral options, instead, can only occur when available choices are emotionally salient. 6. Conclusion and future directions Clinical and experimental work has started to provide solid evidence on how cultural and biological factors interact to give rise to human morality. The identification of neural components and their relationships to psychological processes underlying moral cognition is providing critical knowledge for a better understanding of how our ‘‘moral nature’’ may foster not only prosocial and altruistic behaviors, but also out-group discrimination and violence. We have highlighted how basic neurohumoral mechanisms are fundamental to moral judgment and sentiments, which can be better explained by integration of specific cognitive– emotional processes than by competition between cognition and emotion. We have reviewed several lines of evidence linking specific neural structures and networks to certain clusters of moral sentiments and to values. This field of research is still in its infancy however, and our understanding on how these very complex and abstract representations are encoded in the human brain is still preliminary. Nonetheless, the past decade has witnessed a tremendous advance in both conceptual and methodological terms, and the availability of testable models and of powerful imaging, genetic and cognitive psychology methods will enable researchers to test and refine current working hypotheses on the neural and psychological bases of human moral cognition.

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