Patricia L. Lockwood

Amygdala Response to Preattentive Masked Fear in Children With Conduct Problems: The Role of Callous-Unemotional Traits

OBJECTIVE In children with conduct problems, high levels of callous-unemotional traits are associated with amygdala hypoactivity to consciously perceived fear, while low levels of callous-unemotional traits may be associated with amygdala hyperactivity. Behavioral data suggest that fear processing deficits in children with high callous-unemotional traits may extend to stimuli presented below conscious awareness (preattentively). The authors investigated the neural basis of this effect. Amygdala involvement was predicted on the basis of its role in preattentive affective processing in healthy adults and its dysfunction in previous studies of conduct problems. METHOD Functional MRI was used to measure neural responses to fearful and calm faces presented preattentively (for 17 ms followed by backward masking) in boys with conduct problems and high callous-unemotional traits (N=15), conduct problems and low callous-unemotional traits (N=15), and typically developing comparison boys (N=16). Amygdala response to fearful and calm faces was predicted to differentiate groups, with the greatest response in boys with conduct problems and low callous-unemotional traits and the lowest in boys with conduct problems and high callous-unemotional traits. RESULTS In the right amygdala, a greater amygdala response was seen in boys with conduct problems and low callous-unemotional traits than in those with high callous-unemotional traits. The findings were not explained by symptom levels of conduct disorder, attention-deficit hyperactivity disorder, anxiety, or depression. CONCLUSIONS These data demonstrate differential amygdala activity to preattentively presented fear in children with conduct problems grouped by callous-unemotional traits, with high levels associated with lower amygdala reactivity. The studys findings complement increasing evidence suggesting that callous-unemotional traits are an important specifier in the classification of children with conduct problems.

Association of Callous Traits with Reduced Neural Response to Others’ Pain in Children with Conduct Problems

Summary Children with conduct problems (CP) persistently violate others’ rights and represent a considerable societal cost [1]. These children also display atypical empathic responses to others’ distress [2], which may partly account for their violent and antisocial behavior. Callous traits index lack of empathy in these children and confer risk for adult psychopathy [3]. Investigating neural responses to others’ pain is an ecologically valid method to probe empathic processing [4], but studies in children with CP have been inconclusive [5, 6]. Using functional magnetic resonance imaging (fMRI), we measured neural responses to pictures of others in pain (versus no pain) in a large sample of children with CP and matched controls. Relative to controls, children with CP showed reduced blood oxygen level-dependent responses to others’ pain in bilateral anterior insula (AI), anterior cingulate cortex (ACC), and inferior frontal gyrus, regions associated with empathy for pain in previous studies [7, 8]. In the CP group, callous traits were negatively associated with responses to others’ pain in AI and ACC. We conclude that children with CP have atypical neural responses to others’ pain. The negative association between callous traits and AI/ACC response could reflect an early neurobiological marker indexing risk for empathic deficits seen in adult psychopathy.

Dissecting empathy: High levels of psychopathic and autistic traits are characterized by difficulties in different social information processing domains

Individuals with psychopathy or autism spectrum disorder (ASD) can behave in ways that suggest lack of empathy towards others. However, many different cognitive and affective processes may lead to unempathic behavior and the social processing profiles of individuals with high psychopathic vs. ASD traits are likely different. Whilst psychopathy appears characterized by problems with resonating with others’ emotions, ASD appears characterized by problems with cognitive perspective-taking. In addition, alexithymia has previously been associated with both disorders, but the contribution of alexithymia needs further exploration. In a community sample (N = 110) we show for the first time that although affective resonance and cognitive perspective-taking are related, high psychopathic traits relate to problems with resonating with others’ emotions, but not cognitive perspective taking. Conversely, high ASD traits relate to problems with cognitive perspective-taking but not resonating with others’ emotions. Alexithymia was associated with problems with affective resonance independently of psychopathic traits, suggesting that different component processes (reduced tendency to feel what others feel and reduced ability to identify and describe feelings) comprise affective resonance. Alexithymia was not associated with the reduced cognitive perspective-taking in high ASD traits. Our data suggest that (1) elevated psychopathic and ASD traits are characterized by difficulties in different social information processing domains and (2) reduced affective resonance in individuals with elevated psychopathic traits and the reduced cognitive perspective taking in individuals with elevated ASD traits are not explained by co-occurring alexithymia. (3) Alexithymia is independently associated with reduced affective resonance. Consequently, our data point to different component processes within the construct of empathy that are suggestive of partially separable cognitive and neural systems.

Emotion Regulation Moderates the Association between Empathy and Prosocial Behavior

Theory and evidence suggest that empathy is an important motivating factor for prosocial behaviour and that emotion regulation, i.e. the capacity to exert control over an emotional response, may moderate the degree to which empathy is associated with prosocial behaviour. However, studies to date have not simultaneously explored the associations between different empathic processes and prosocial behaviour, nor whether different types of emotion regulation strategies (e.g. cognitive reappraisal and expressive suppression) moderate associations between empathy and prosocial behaviour. One hundred–and-ten healthy adults completed questionnaire measures of empathy, emotion regulation and prosocial tendencies. In this sample, both affective and cognitive empathy predicted self-reported prosocial tendencies. In addition, cognitive reappraisal moderated the association between affective empathy and prosocial tendencies. Specifically, there was a significant positive association between empathy and prosocial tendencies for individuals with a low or average tendency to reappraise but not for those with a high tendency to reappraise. Our findings suggest that, in general, empathy is positively associated with prosocial behaviour. However, this association is not significant for individuals with a high tendency for cognitive reappraisal.

The role of the midcingulate cortex in monitoring others' decisions

A plethora of research has implicated the cingulate cortex in the processing of social information (i.e., processing elicited by, about, and directed toward others) and reward-related information that guides decision-making. However, it is often overlooked that there is variability in the cytoarchitectonic properties and anatomical connections across the cingulate cortex, which is indicative of functional variability. Here we review evidence from lesion, single-unit recording and functional imaging studies. Taken together, these support the claim that the processing of information that has the greatest influence on social behavior can be localized to the gyral surface of the midcingulate cortex (MCCg). We propose that the MCCg is engaged when predicting and monitoring the outcomes of decisions during social interactions. In particular, the MCCg processes statistical information that tracks the extent to which the outcomes of decisions meet goals when interacting with others. We provide a novel framework for the computational mechanisms that underpin such social information processing in the MCCg. This framework provides testable hypotheses for the social deficits displayed in autism spectrum disorders and psychopathy.

The anatomy of empathy: Vicarious experience and disorders of social cognition

Highlights • The anatomy of vicarious experience in animal and human studies is reviewed.• The ACC gyrus and anterior insula are central to vicarious experience.• Vicarious experience can rely on both shared and non-shared neural responses.• Aspects of vicarious experience may be atypical in psychopathy and autism.

Neural responses to fearful eyes in children with conduct problems and varying levels of callous-unemotional traits

BACKGROUND Children with conduct problems (CP) are a heterogeneous group. Those with high levels of callous-unemotional traits (CP/HCU) appear emotionally under-reactive at behavioural and neural levels whereas those with low levels of CU traits (CP/LCU) appear emotionally over-reactive, compared with typically developing (TD) controls. Investigating the degree to which these patterns of emotional reactivity are malleable may have important translational implications. Instructing participants with CP/HCU to focus on the eyes of fearful faces (i.e. the most salient feature) can ameliorate their fear-recognition deficits, but it is unknown whether this is mediated by amygdala response. It is also unknown whether focusing on fearful eyes is associated with increased amygdala reactivity in CP/LCU. METHOD Functional magnetic resonance imaging (fMRI) was used to measure neural responses to fearful and calm faces in children with CP/HCU, CP/LCU and TD controls (n = 17 per group). On half of trials participants looked for a blue dot anywhere within target faces; on the other half, participants were directed to focus on the eye region. RESULTS Reaction time (RT) data showed that CP/LCU were selectively slowed in the fear/eyes condition. For the same condition, CP/LCU also showed increased amygdala and subgenual anterior cingulate cortex (sgACC)/orbitofrontal cortex (OFC) responses compared with TD controls. RT and amygdala response to fear/eyes were correlated in CP/LCU only. No effects of focusing on the eye region were observed in CP/HCU. CONCLUSIONS These data extend the evidence base suggesting that CU traits index meaningful heterogeneity in conduct problems. Focusing on regulating reactive emotional responses may be a fruitful strategy for children with CP/LCU.

Neurocomputational mechanisms of prosocial learning and links to empathy.

Significance Prosocial behaviors are essential for social bonding and cohesion, but the mechanisms that underpin these behaviors are still poorly understood. Using computational modeling and neuroimaging, we show that people can learn to benefit others and that this learning is underpinned by reinforcement learning signals in the subgenual anterior cingulate cortex (sgACC). However, there is substantial individual variability in people’s ability for prosocial learning. More empathic people learn faster and have more selective responses in the sgACC when benefitting others. Our results thus reveal a computational mechanism driving prosocial learning in humans and why empathy and prosocial behavior may be linked. This framework could help to explain reduced empathy and prosocial behavior in people with disorders of social cognition. Reinforcement learning theory powerfully characterizes how we learn to benefit ourselves. In this theory, prediction errors—the difference between a predicted and actual outcome of a choice—drive learning. However, we do not operate in a social vacuum. To behave prosocially we must learn the consequences of our actions for other people. Empathy, the ability to vicariously experience and understand the affect of others, is hypothesized to be a critical facilitator of prosocial behaviors, but the link between empathy and prosocial behavior is still unclear. During functional magnetic resonance imaging (fMRI) participants chose between different stimuli that were probabilistically associated with rewards for themselves (self), another person (prosocial), or no one (control). Using computational modeling, we show that people can learn to obtain rewards for others but do so more slowly than when learning to obtain rewards for themselves. fMRI revealed that activity in a posterior portion of the subgenual anterior cingulate cortex/basal forebrain (sgACC) drives learning only when we are acting in a prosocial context and signals a prosocial prediction error conforming to classical principles of reinforcement learning theory. However, there is also substantial variability in the neural and behavioral efficiency of prosocial learning, which is predicted by trait empathy. More empathic people learn more quickly when benefitting others, and their sgACC response is the most selective for prosocial learning. We thus reveal a computational mechanism driving prosocial learning in humans. This framework could provide insights into atypical prosocial behavior in those with disorders of social cognition.

Distinct Subtypes of Apathy Revealed by the Apathy Motivation Index

Apathy is a debilitating but poorly understood disorder characterized by a reduction in motivation. As well as being associated with several brain disorders, apathy is also prevalent in varying degrees in healthy people. Whilst many tools have been developed to assess levels of apathy in clinical disorders, surprisingly there are no measures of apathy suitable for healthy people. Moreover, although apathy is commonly comorbid with symptoms of depression, anhedonia and fatigue, how and why these symptoms are associated is unclear. Here we developed the Apathy-Motivation Index (AMI), a brief self-report index of apathy and motivation. Using exploratory factor analysis (in a sample of 505 people), and then confirmatory analysis (in a different set of 479 individuals), we identified subtypes of apathy in behavioural, social and emotional domains. Latent profile analyses showed four different profiles of apathy that were associated with varying levels of depression, anhedonia and fatigue. The AMI is a novel and reliable measure of individual differences in apathy and might provide a useful means of probing different mechanisms underlying sub-clinical lack of motivation in otherwise healthy individuals. Moreover, associations between apathy and comorbid states may be reflective of problems in different emotional, social and behavioural domains.

Prosocial apathy for helping others when effort is required

Prosocial acts—those that are costly to ourselves but benefit others—are a central component of human coexistence1–3. While the financial and moral costs of prosocial behaviours are well understood4–6, everyday prosocial acts do not typically come at such costs. Instead, they require effort. Here, using computational modelling of an effort-based task, we show that people are prosocially apathetic. They are less willing to choose to initiate highly effortful acts that benefit others compared with those benefitting themselves. Moreover, even when choosing to initiate effortful prosocial acts, people exhibit superficiality, exerting less force into the actions that benefit others than those that benefit themselves. These findings were replicated, and were present whether the other person was anonymous or not, and when choices were made to earn rewards or avoid losses. Importantly, the least prosocially motivated people had higher subclinical levels of psychopathy and social apathy. Thus, although people sometimes ‘help out’, they are less willing to benefit others and are sometimes ‘superficially prosocial’, which may characterize everyday prosociality and its disruption in social disorders.