Elise M. Cardinale

Mediation of the Relationship Between Callous-Unemotional Traits and Proactive Aggression by Amygdala Response to Fear Among Children With Conduct Problems

IMPORTANCE Among youths with conduct problems, callous-unemotional (CU) traits are known to be an important determinant of symptom severity, prognosis, and treatment responsiveness. But positive correlations between conduct problems and CU traits result in suppressor effects that may mask important neurobiological distinctions among subgroups of children with conduct problems. OBJECTIVE To assess the unique neurobiological covariates of CU traits and externalizing behaviors in youths with conduct problems and determine whether neural dysfunction linked to CU traits mediates the link between callousness and proactive aggression. DESIGN, SETTING, AND PARTICIPANTS This cross-sectional case-control study involved behavioral testing and neuroimaging that were conducted at a university research institution. Neuroimaging was conducted using a 3-T Siemens magnetic resonance imaging scanner. It included 46 community-recruited male and female juveniles aged 10 to 17 years, including 16 healthy control participants and 30 youths with conduct problems with both low and high levels of CU traits. MAIN OUTCOMES AND MEASURES Blood oxygenation level-dependent signal as measured via functional magnetic resonance imaging during an implicit face-emotion processing task and analyzed using whole-brain and region of interest-based analysis of variance and multiple-regression analyses. RESULTS Analysis of variance revealed no group differences in the amygdala. By contrast, consistent with the existence of suppressor effects, multiple-regression analysis found amygdala responses to fearful expressions to be negatively associated with CU traits (x = 26, y = 0, z = -12; k = 1) and positively associated with externalizing behavior (x = 24, y = 0, z = -14; k = 8) when both variables were modeled simultaneously. Reduced amygdala responses mediated the relationship between CU traits and proactive aggression. CONCLUSIONS AND RELEVANCE The results linked proactive aggression in youths with CU traits to hypoactive amygdala responses to emotional distress cues, consistent with theories that externalizing behaviors, particularly proactive aggression, in youths with these traits stem from deficient empathic responses to distress. Amygdala hypoactivity may represent an intermediate phenotype, offering new insights into effective treatment strategies for conduct problems.

Neural and cognitive characteristics of extraordinary altruists

Significance Altruism, and particularly costly altruism toward strangers, such as altruistic kidney donation, represents a puzzling phenomenon for many fields of science, including evolutionary biology, psychology, and economics. How can such behavior be explained? The propensity to engage in costly altruism varies widely and may be genetically mediated, but little is known about the neural mechanisms that support it. We used structural and functional brain imaging to compare extraordinary altruists, specifically altruistic kidney donors, and controls. Altruists exhibited variations in neural anatomy and functioning that represent the inverse of patterns previously observed in psychopaths, who are unusually callous and antisocial. These findings suggest extraordinary altruism represents one end of a caring continuum and is supported by neural mechanisms that underlie social and emotional responsiveness. 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.

When psychopathy impairs moral judgments: neural responses during judgments about causing fear

Psychopathy is a disorder characterized by reduced empathy, shallow affect and behaviors that cause victims distress, like threats, bullying and violence. Neuroimaging research in both institutionalized and community samples implicates amygdala dysfunction in the etiology of psychopathic traits. Reduced amygdala responsiveness may disrupt processing of fear-relevant stimuli like fearful facial expressions. The present study links amygdala dysfunction in response to fear-relevant stimuli to the willingness of individuals with psychopathic traits to cause fear in other people. Thirty-three healthy adult participants varying in psychopathic traits underwent whole-brain fMRI scanning while they viewed statements that selectively evoke anger, disgust, fear, happiness or sadness. During scanning, participants judged whether it is morally acceptable to make each statement to another person. Psychopathy was associated with reduced activity in right amygdala during judgments of fear-evoking statements and with more lenient moral judgments about causing fear. No group differences in amygdala function or moral judgments emerged for other emotion categories. Psychopathy was also associated with increased activity in middle frontal gyrus (BA 10) during the task. These results implicate amygdala dysfunction in impaired judgments about causing distress in psychopathy and suggest that atypical amygdala responses to fear in psychopathy extend across multiple classes of stimuli.

The Impact of Autism Spectrum Disorder and Alexithymia on Judgments of Moral Acceptability

One’s own emotional response toward a hypothetical action can influence judgments of its moral acceptability. Some individuals with autism spectrum disorder (ASD) exhibit atypical emotional processing, and moral judgments. Research suggests, however, that emotional deficits in ASD are due to co-occurring alexithymia, meaning atypical moral judgments in ASD may be due to alexithymia also. Individuals with and without ASD (matched for alexithymia) judged the moral acceptability of emotion-evoking statements and identified the emotion evoked. Moral acceptability judgments were predicted by alexithymia. Crucially, however, this relationship held only for individuals without ASD. While ASD diagnostic status did not directly predict either judgment, those with ASD did not base their moral acceptability judgments on emotional information. Findings are consistent with evidence demonstrating that decision-making is less subject to emotional biases in those with ASD.

Callous-unemotional traits drive reduced white-matter integrity in youths with conduct problems

BACKGROUND Callous-unemotional (CU) traits represent a significant risk factor for severe and persistent conduct problems in children and adolescents. Extensive neuroimaging research links CU traits to structural and functional abnormalities in the amygdala and ventromedial prefrontal cortex. In addition, adults with psychopathy (a disorder for which CU traits are a developmental precursor) exhibit reduced integrity in uncinate fasciculus, a white-matter (WM) tract that connects prefrontal and temporal regions. However, research in adolescents has not yet yielded similarly consistent findings. METHOD We simultaneously modeled CU traits and externalizing behaviors as continuous traits, while controlling for age and IQ, in order to identify the unique relationship of each variable with WM microstructural integrity, assessed using diffusion tensor imaging. We used tract-based spatial statistics to evaluate fractional anisotropy, an index of WM integrity, in uncinate fasciculus and stria terminalis in 47 youths aged 10-17 years, of whom 26 exhibited conduct problems and varying levels of CU traits. RESULTS Whereas both CU traits and externalizing behaviors were negatively correlated with WM integrity in bilateral uncinate fasciculus and stria terminalis/fornix, simultaneously modeling both variables revealed that these effects were driven by CU traits; the severity of externalizing behavior was not related to WM integrity after controlling for CU traits. CONCLUSIONS These results indicate that WM abnormalities similar to those observed in adult populations with psychopathy may emerge in late childhood or early adolescence, and may be critical to understanding the social and affective deficits observed in this population.

Is costly punishment altruistic? Exploring rejection of unfair offers in the Ultimatum Game in real-world altruists

In the Ultimatum Game (UG), incurring a cost to punish inequity is commonly termed altruistic punishment. This behaviour is thought to benefit others if the defector becomes more equitable in future interactions. However, clear connections between punishment in the UG and altruistic behaviours outside the laboratory are lacking. We tested the altruistic punishment hypothesis in a sample of extraordinarily altruistic adults, predicting that if punishing inequity is predictive of altruism more broadly, extraordinary altruists should punish more frequently. Results showed that punishment was not more prevalent in extraordinary altruists than controls. However, a self-reported altruism measure previously linked to peer evaluations but not behaviour, and on which extraordinary altruists and controls did not differ, did predict punishment. These findings support suggestions that altruistic punishment in the UG is better termed costly punishment and may be motivated by social, but not necessarily prosocial, concerns. Results also support prior suggestions that self-reported altruism may not reliably predict altruistic behaviour.

Power Plays Expressive Mimicry of Valid Agonistic Cues

Both transient and stable facial cues have evolved as essential features of social communication in humans. Accumulating research links actual and perceived aggression to a higher ratio between the height and bizygomatic width of a person’s face (facial width-to-height ratio [WHR]) and shows that digitally increasing this ratio can alter apparent aggressiveness. We present evidence that facial behaviors associated with anger—the state most closely associated with aggressive intentions—also increase facial WHR, mimicking the facial morphology of aggressive individuals. In Study 1, individuals induced to appear aggressive naturally increased their facial WHR using anger-related facial behaviors. In Study 2, we found that validated anger expressions increased facial WHR and that this change predicts increased attributions of aggressiveness. We also found statistical suggestions that anger-related facial behaviors may serve as cues that overrepresent the expresser’s aggressiveness. Our findings suggest that facial behaviors associated with anger may have emerged to facilitate aggressive encounters.

Social discounting and distance perceptions in costly altruism

Extraordinary acts of altruism towards strangers represent puzzling phenomena not easily explained by dominant biological models of altruism, such as kin selection and reciprocity1–3. These theories stipulate that genetically or socially close others should be the beneficiaries of costly generosity4,5. Extraordinary altruists exhibit increased empathic sensitivity and a fast, intuitive decision-making style6,7, but no clear explanation yet exists for the most perplexing feature of these altruists, which is that they incur significant risks to benefit strangers5. Here, we considered two related proximal mechanisms—social discounting (valuational) and social distancing (perceptual)—that have been proposed to explain why costly help is preferentially given to close others. We hypothesized that variations in one or both mechanisms drive costly altruism towards distant others. We show that extraordinary altruists exhibit reduced social discounting, with altruists discounting the subjective value of outcomes for socially distant others less than controls. Group differences in social discounting were associated with self-reported other-oriented preferences and could not be accounted for by variation in social distancing. These results suggest a psychological mechanism by which costly helping behaviour towards genetically and socially close others might be extended to unrelated others.

Impact of Psychopathy on Moral Judgments about Causing Fear and Physical Harm.

Psychopathy is a personality variable associated with persistent immoral behaviors. Despite this, attempts to link moral reasoning deficits to psychopathic traits have yielded mixed results with many findings supporting intact moral reasoning in individuals with psychopathic traits. Abundant evidence shows that psychopathy impairs responses to others’ emotional distress. However, most studies of morality and psychopathy focus on judgments about causing others physical harm. Results of such studies may be inconsistent because physical harm is an imperfect proxy for emotional distress. No previous paradigm has explicitly separated judgments about physical harm and emotional distress and assessed how psychopathy affects each type of judgment. In three studies we found that psychopathy impairs judgments about causing others emotional distress (specifically fear) but minimally affects judgments about causing physical harm and that judgments about causing fear predict instrumental aggression in psychopathy. These findings are consistent with reports linking psychopathy to insensitivity to others’ fear, and suggest that sensitivity to others’ fear may play a fundamental role in the types of moral decision-making impaired by psychopathy.

The Reliability and Validity of the Inventory of Callous Unemotional Traits: A Meta-Analytic Review:

In the fifth edition of the Diagnostic and Statistical Manual of Mental Disorders, a Limited Prosocial Emotions specifier was added to the conduct disorder diagnostic criteria to designate a subgroup of children who exhibit callous unemotional (CU) traits. The Inventory of Callous Unemotional Traits (ICU) is the only dedicated measure of CU traits and was influential in the development of the Limited Prosocial Emotions specifier. Despite its role in the research and diagnosis of CU traits, some questions have persisted regarding the internal consistency and validity of the ICU and its three subscales: callous, uncaring, and unemotional. Results of a meta-analysis revealed acceptable internal consistency and external validity for total ICU, callous, and uncaring scores, but not unemotional scores. These results support the utility of the total ICU, callous, and uncaring scales, but indicate weaknesses in the scale or construct of unemotionality as it relates to interpersonal callousness, uncaring, and antisociality.