Fear signals vulnerability and appeasement, not threat.

Humans are not only fearful apes, but we also communicate our fear using social cues. Social fear displays typically elicit care and assistance in the real world and the lab. But in the psychology and neuroscience literature fearful expressions are commonly interpreted as "threat cues." The fearful ape hypothesis suggests that fearful expressions should be instead considered appeasement and vulnerability cues.

Emotion recognition impairments and social well-being following right-hemisphere stroke.

Accurately recognizing and responding to the emotions of others is essential for proper social communication and helps bind strong relationships that are particularly important for stroke survivors. Emotion recognition typically engages cortical areas that are predominantly right-lateralized including superior temporal and inferior frontal gyri - regions frequently impacted by right-hemisphere stroke. Since prior work already links right-hemisphere stroke to deficits in emotion recognition, this research aims to extend these findings to determine whether impaired emotion recognition after right-hemisphere stroke is associated with worse social well-being outcomes. Eighteen right-hemisphere stroke patients (≥6 months post-stroke) and 21 neurologically healthy controls completed a multimodal emotion recognition test (Geneva Emotion Recognition Test - Short) and reported engagement in social/non-social activities and levels of social support. Right-hemisphere stroke was associated with worse emotion recognition accuracy, though not all patients exhibited impairment. In line with hypotheses, emotion recognition impairments were associated with greater loss of social activities after stroke, an effect that could not be attributed to stroke severity or loss of non-social activities. Impairments were also linked to reduced patient-reported social support. Results implicate emotion recognition difficulties as a potential antecedent of social withdrawal after stroke and warrant future research to test emotion recognition training post-stroke.

Bilateral amygdala damage linked to impaired ability to predict others' fear but preserved moral judgements about causing others fear.

The amygdala is a subcortical structure implicated in both the expression of conditioned fear and social fear recognition. Social fear recognition deficits following amygdala lesions are often interpreted as reflecting perceptual deficits, or the amygdala's role in coordinating responses to threats. But these explanations fail to capture why amygdala lesions impair both physiological and behavioural responses to multimodal fear cues and the ability to identify them. We hypothesized that social fear recognition deficits following amygdala damage reflect impaired conceptual understanding of fear. Supporting this prediction, we found specific impairments in the ability to predict others' fear (but not other emotions) from written scenarios following bilateral amygdala lesions. This finding is consistent with the suggestion that social fear recognition, much like social recognition of states like pain, relies on shared internal representations. Preserved judgements about the permissibility of causing others fear confirms suggestions that social emotion recognition and morality are dissociable.

Global Variation in Subjective Well-Being Predicts Seven Forms of Altruism.

The geographic prevalence of various altruistic behaviors (nonreciprocal acts that improve other people's welfare) is not uniformly distributed, but whether this reflects variation in a superordinate construct linked to national-level outcomes or cultural values is unknown. We compiled data on seven altruistic behaviors across 48 to 152 nations and found evidence that these behaviors reflect a latent construct positively associated with national-level subjective well-being (SWB) and individualist values, even when we controlled for national-level wealth, health, education, and shared cultural history. Consistent with prior work, our results showed that SWB mediated the relationship between two objective measures of well-being (wealth and health) and altruism (n = 130). Moreover, these indirect effects increased as individualist values increased within the subset of countries (n = 90) with available data. Together, our results indicate that altruism increases when resources and cultural values provide objective and subjective means for pursuing personally meaningful goals and that altruistic behaviors may be enhanced by societal changes that promote well-being.

The Caring Continuum: Evolved Hormonal and Proximal Mechanisms Explain Prosocial and Antisocial Extremes.

Implicit in the long-standing disagreements about whether humans' fundamental nature is predominantly caring or callous is an assumption of uniformity. This article reviews evidence that instead supports inherent variation in caring motivation and behavior. The continuum between prosocial and antisocial extremes reflects variation in the structure and function of neurohormonal systems originally adapted to motivate parental care and since repurposed to support generalized forms of care. Extreme social behaviors such as extraordinary acts of altruism and aggression can often be best understood as reflecting variation in the neural systems that support care. A review of comparative, developmental, and neurobiological research finds consistent evidence that variations in caring motivations and behavior reflect individual differences in sensitivity to cues that signal vulnerability and distress and in the tendency to generalize care outward from socially close to distant others. The often complex relationships between caring motivation and various forms of altruism and aggression are discussed.

Empathic emotion regulation in prosocial behaviour and altruism.

Emotions evoked in response to others' distress are important for motivating concerned prosocial responses. But how emotion regulation shapes prosocial responding is not yet well understood. We tested the role of empathic emotion regulation in promoting prosocial motivation and costly donations across two studies, first in a community sample and then in a sample of altruistic kidney donors and a matched comparison sample. Participants engaged in hopeful and distancing reappraisals while viewing images of others in distress, then decided whether to help by donating to charity. Whereas hope was expected to evoke approach-based motivation indexed by increased donations, distance was expected to evoke avoidance-based motivation indexed by decreased donations, via varying effects of the two reappraisals on positive and negative affect. Across both studies, both reappraisals decreased negative affect and hopeful reappraisal increased positive affect. In the community sample, hope resulted in higher donations than distancing. Altruists were more prosocial overall, but the associations between affect and donation behaviour in this group mirrored the hopeful reappraisal in the community sample, suggesting that altruists might adopt this strategy by default. These findings clarify the role of empathic emotion regulation in prosocial behaviour and also independent effects of positive and negative affect.

Callous and uncaring traits are associated with reductions in amygdala volume among youths with varying levels of conduct problems.

BACKGROUND: The emergence of callous unemotional (CU) traits, and associated externalizing behaviors, is believed to reflect underlying dysfunction in the amygdala. Studies of adults with CU traits or psychopathy have linked characteristic patterns of amygdala dysfunction to reduced amygdala volume, but studies in youths have not thus far found evidence of similar amygdala volume reductions. The current study examined the association between CU traits and amygdala volume by modeling CU traits and externalizing behavior as independent continuous variables, and explored the relative contributions of callous, uncaring, and unemotional traits. METHODS: CU traits and externalizing behavior problems were assessed in 148 youths using the Inventory of Callous Unemotional Traits (ICU) and the Child Behavior Checklist (CBCL). For a subset of participants (n = 93), high-resolution T1-weighted images were collected and volume estimates for the amygdala were extracted. RESULTS: Analyses revealed that CU traits were associated with increased externalizing behaviors and decreased bilateral amygdala volume. These results were driven by the callous and uncaring sub-factors of CU traits, with unemotional traits unrelated to either externalizing behaviors or amygdala volume. Results persisted after accounting for covariation between CU traits and externalizing behaviors. Bootstrap mediation analyses indicated that CU traits mediated the relationship between reduced amygdala volume and externalizing severity. CONCLUSIONS: These findings provide evidence that callous-uncaring traits account for reduced amygdala volume among youths with conduct problems. These findings provide a framework for further investigation of abnormal amygdala development as a key causal pathway for the development of callous-uncaring traits and conduct problems.

Extraordinary Altruists Exhibit Enhanced Self-Other Overlap in Neural Responses to Distress.

Shared neural representations during experienced and observed distress are hypothesized to reflect empathic neural simulation, which may support altruism. But the correspondence between real-world altruism and shared neural representations has not been directly tested, and empathy's role in promoting altruism toward strangers has been questioned. Here, we show that individuals who have performed costly altruism (donating a kidney to a stranger; n = 25) exhibit greater self-other overlap than matched control participants ( n = 27) in neural representations of pain and threat (fearful anticipation) in anterior insula (AI) during an empathic-pain paradigm. Altruists exhibited greater self-other correspondence in pain-related activation in left AI, highlighting that group-level overlap was supported by individual-level associations between empathic pain and firsthand pain. Altruists exhibited enhanced functional coupling of left AI with left midinsula during empathic pain and threat. Results show that heightened neural instantiations of empathy correspond to real-world altruism and highlight limitations of self-report.

Externalizing behavior severity in youths with callous-unemotional traits corresponds to patterns of amygdala activity and connectivity during judgments of causing fear.

Callous-unemotional (CU) traits characterize a subgroup of youths with conduct problems who exhibit low empathy, fearlessness, and elevated externalizing behaviors. The current study examines the role of aberrant amygdala activity and functional connectivity during a socioemotional judgment task in youths with CU traits, and links these deficits to externalizing behaviors. Functional magnetic resonance imaging was used to compare neural responses in 18 healthy youths and 30 youths with conduct problems and varying levels of CU traits as they evaluated the acceptability of causing another person to experience each of several emotions, including fear. Neuroimaging analyses examined blood oxygenation level dependent responses and task-dependent functional connectivity. High-CU youths exhibited left amygdala hypoactivation relative to healthy controls and low-CU youths primarily during evaluations of causing others fear. CU traits moderated the relationship between externalizing behavior and both amygdala activity and patterns of functional connectivity. The present data suggest that CU youths' aberrant amygdala activity and connectivity affect how they make judgments about the acceptability of causing others emotional distress, and that these aberrations represent risk factors for externalizing behaviors like rule breaking and aggression. These findings suggest that reducing externalizing behaviors in high-CU youths may require interventions that influence affective sensitivity.

Emotion and personal space: Neural correlates of approach-avoidance tendencies to different facial expressions as a function of coldhearted psychopathic traits.

In social interactions, humans are expected to regulate interpersonal distance in response to the emotion displayed by others. Yet, the neural mechanisms implicated in approach-avoidance tendencies to distinct emotional expressions have not been fully described. Here, we investigated the neural systems implicated in regulating the distance to different emotions, and how they vary as a function of empathy. Twenty-three healthy participants assessed for psychopathic traits underwent fMRI scanning while they viewed approaching and withdrawing angry, fearful, happy, sad and neutral faces. Participants were also asked to set the distance to those faces on a computer screen, and to adjust the physical distance from the experimenter outside the scanner. Participants kept the greatest distances from angry faces, and shortest from happy expressions. This was accompanied by increased activation in the dorsomedial prefrontal and orbitofrontal cortices, inferior frontal gyrus, and temporoparietal junction for angry and happy expressions relative to the other emotions. Irrespective of emotion, longer distances were kept from approaching faces, which was associated with increased activation in the amygdala and insula, as well as parietal and prefrontal regions. Amygdala activation was positively correlated with greater preferred distances to angry, fearful and sad expressions. Moreover, participants scoring higher on coldhearted psychopathic traits (lower empathy) showed reduced amygdala activation to sad expressions. These findings elucidate the neural mechanisms underlying social approach-avoidance, and how they are related to variations in empathy. Hum Brain Mapp 38:1492-1506, 2017. © 2016 Wiley Periodicals, Inc.

Amygdala-midbrain connectivity indicates a role for the mammalian parental care system in human altruism.

Costly altruism benefitting a stranger is a rare but evolutionarily conserved phenomenon. This behaviour may be supported by limbic and midbrain circuitry that supports mammalian caregiving. In rodents, reciprocal connections between the amygdala and the midbrain periaqueductal grey (PAG) are critical for generating protective responses toward vulnerable and distressed offspring. We used functional and structural magnetic resonance imaging to explore whether these regions play a role in supporting costly altruism in humans. We recruited a rare population of altruists, all of whom had donated a kidney to a stranger, and measured activity and functional connectivity of the amygdala and PAG as altruists and matched controls responded to care-eliciting scenarios. When these scenarios were coupled with pre-attentive distress cues, altruists' sympathy corresponded to greater activity in the left amygdala and PAG, and functional connectivity analyses revealed increased coupling between these regions in altruists during this epoch. We also found that altruists exhibited greater fractional anisotropy within the left amygdala-PAG white matter tract. These results, coupled with previous evidence of altruists' increased amygdala-linked sensitivity to distress, are consistent with costly altruism resulting from enhanced care-oriented responses to vulnerability and distress that are supported by recruitment of circuitry that supports mammalian parental care.

Neural and cognitive characteristics of extraordinary altruists.

Altruistic behavior improves the welfare of another individual while reducing the altruist's welfare. Humans' tendency to engage in altruistic behaviors is unevenly distributed across the population, and individual variation in altruistic tendencies may be genetically mediated. Although neural endophenotypes of heightened or extreme antisocial behavior tendencies have been identified in, for example, studies of psychopaths, little is known about the neural mechanisms that support heightened or extreme prosocial or altruistic tendencies. In this study, we used structural and functional magnetic resonance imaging to assess a population of extraordinary altruists: altruistic kidney donors who volunteered to donate a kidney to a stranger. Such donations meet the most stringent definitions of altruism in that they represent an intentional behavior that incurs significant costs to the donor to benefit an anonymous, nonkin other. Functional imaging and behavioral tasks included face-emotion processing paradigms that reliably distinguish psychopathic individuals from controls. Here we show that extraordinary altruists can be distinguished from controls by their enhanced volume in right amygdala and enhanced responsiveness of this structure to fearful facial expressions, an effect that predicts superior perceptual sensitivity to these expressions. These results mirror the reduced amygdala volume and reduced responsiveness to fearful facial expressions observed in psychopathic individuals. Our results support the possibility of a neural basis for extraordinary altruism. We anticipate that these findings will expand the scope of research on biological mechanisms that promote altruistic behaviors to include neural mechanisms that support affective and social responsiveness.

The role of adolescence in geographic variation in violent aggression.

In explaining variation in violent aggression across populations, the age structures of those populations must be considered. Adolescents between the ages of 15 and 25 are disproportionately responsible for violent aggression in every society, and increases in violence tend to follow population "youth bulges." Large numbers of adolescents in equatorial regions may account for observed relationships between geography and violence.

Understanding amygdala responsiveness to fearful expressions through the lens of psychopathy and altruism.

Because the face is the central focus of human social interactions, emotional facial expressions provide a unique window into the emotional lives of others. They play a particularly important role in fostering empathy, which entails understanding and responding to others' emotions, especially distress-related emotions such as fear. This Review considers how fearful facial as well as vocal and postural expressions are interpreted, with an emphasis on the role of the amygdala. The amygdala may be best known for its role in the acquisition and expression of conditioned fear, but it also supports the perception and recognition of others' fear. Various explanations have been supplied for the amygdala's role in interpreting and responding to fearful expressions. They include theories that amygdala responses to fearful expressions 1) reflect heightened vigilance in response to uncertain danger, 2) promote heightened attention to the eye region of faces, 3) represent a response to an unconditioned aversive stimulus, or 4) reflect the generation of an empathic fear response. Among these, only empathic fear explains why amygdala lesions would impair fear recognition across modalities. Supporting the possibility of a link between fundamental empathic processes and amygdala responses to fear is evidence that impaired fear recognition in psychopathic individuals results from amygdala dysfunction, whereas enhanced fear recognition in altruistic individuals results from enhanced amygdala function. Empathic concern and caring behaviors may be fostered by sensitivity to signs of acute distress in others, which relies on intact functioning of the amygdala.

Neighborhood income and the expression of callous-unemotional traits.

Callous-unemotional (CU) traits, including an uncaring nature and reduced empathy, represent a strongly heritable pattern of socio-emotional responding linked with elevated risk for severe, persistent delinquent behavior. Although evidence suggests that CU traits vary continuously across the population, research linking CU traits and delinquency is often conducted with incarcerated or clinical samples, obscuring potential heterogeneity in this relationship across the full range of high-CU individuals. Using a nationally representative sample, this study examines the role of neighborhood income in moderating the association between CU traits and delinquency in terms of both level and type of offending. Findings corroborate the link between CU traits and delinquency and suggest that the link between high-CU traits and violent delinquency may be unique to youth living in low-income neighborhoods.

Geographical differences in subjective well-being predict extraordinary altruism.

Altruistic kidney donation is a form of extraordinary altruism, the antecedents of which are poorly understood. Although well-being is known to increase the incidence of prosocial behaviors and there is significant geographical variation in both well-being and altruistic kidney donation in the United States, it is unknown whether geographical variation in well-being predicts the prevalence of this form of extraordinary altruism. We calculated per capita rates of altruistic kidney donation across the United States and found that an index of subjective well-being predicted altruistic donation, even after we controlled for relevant sociodemographic variables. This relationship persisted at the state level and at the larger geographic regional level. Consistent with hypotheses about the relationship between objective and subjective well-being, results showed that subjective well-being mediated the relationship between increases in objective well-being metrics, such as income, and altruism. These results suggest that extraordinary altruism may be promoted by societal factors that increase subjective well-being.

Impairments in facial affect recognition associated with autism spectrum disorders: a meta-analysis.

Autism spectrum disorders (ASDs) are characterized by social impairments, including inappropriate responses to affective stimuli and nonverbal cues, which may extend to poor face-emotion recognition. However, the results of empirical studies of face-emotion recognition in individuals with ASD have yielded inconsistent findings that occlude understanding the role of face-emotion recognition deficits in the development of ASD. The goal of this meta-analysis was to address three as-yet unanswered questions. Are ASDs associated with consistent face-emotion recognition deficits? Do deficits generalize across multiple emotional expressions or are they limited to specific emotions? Do age or cognitive intelligence affect the magnitude of identified deficits? The results indicate that ASDs are associated with face-emotion recognition deficits across multiple expressions and that the magnitude of these deficits increases with age and cannot be accounted for by intelligence. These findings suggest that, whereas neurodevelopmental processes and social experience produce improvements in general face-emotion recognition abilities over time during typical development, children with ASD may experience disruptions in these processes, which suggested distributed functional impairment in the neural architecture that subserves face-emotion processing, an effect with downstream developmental consequences.

Ethical reasoning versus empathic bias: a false dichotomy?

Does empathy necessarily impede equity in altruism? Emerging findings from cognitive and affective science suggest that rationality and empathy are mutually compatible, contradicting some earlier, prominent arguments that empathy impedes equitable giving. We propose alternative conceptualizations of relationships among empathy, rationality, and equity, drawing on interdisciplinary advances in altruism research.

Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits.

BACKGROUND: Psychopathic traits are associated with increases in antisocial behaviors such as aggression and are characterized by reduced empathy for others' distress. This suggests that psychopathic traits may also impair empathic pain sensitivity. However, whether psychopathic traits affect responses to the pain of others versus the self has not been previously assessed. METHOD: We used whole-brain functional magnetic resonance imaging to measure neural activation in 14 adolescents with oppositional defiant disorder or conduct disorder and psychopathic traits, as well as 21 healthy controls matched on age, gender, and intelligence. Activation in structures associated with empathic pain perception was assessed as adolescents viewed photographs of pain-inducing injuries. Adolescents imagined either that the body in each photograph was their own or that it belonged to another person. Behavioral and neuroimaging data were analyzed using random-effects analysis of variance. RESULTS: Youths with psychopathic traits showed reduced activity within regions associated with empathic pain as the depicted pain increased. These regions included rostral anterior cingulate cortex, ventral striatum (putamen), and amygdala. Reductions in amygdala activity particularly occurred when the injury was perceived as occurring to another. Empathic pain responses within both amygdala and rostral anterior cingulate cortex were negatively correlated with the severity of psychopathic traits as indexed by PCL:YV scores. CONCLUSIONS: Youths with psychopathic traits show less responsiveness in regions implicated in the affective response to another's pain as the perceived intensity of this pain increases. Moreover, this reduced responsiveness appears to predict symptom severity.