Abigail A. Marsh

Reduced Amygdala Response to Fearful Expressions in Children and Adolescents With Callous-Unemotional Traits and Disruptive Behavior Disorders

OBJECTIVEnExtensive work implicates abnormal amygdala activation in emotional facial expression processing in adults with callous-unemotional traits. However, no research has examined amygdala response to emotional facial expressions in adolescents with disruptive behavior and callous-unemotional traits. Moreover, despite high comorbidity of callous-unemotional traits and attention deficit hyperactivity disorder (ADHD), no research has attempted to distinguish neural correlates of pediatric callous-unemotional traits and ADHD.nnnMETHODnParticipants were 36 children and adolescents (ages 10-17 years); 12 had callous-unemotional traits and either conduct disorder or oppositional defiant disorder, 12 had ADHD, and 12 were healthy comparison subjects. Functional MRI was used to assess amygdala activation patterns during processing of fearful facial expressions. Patterns in the callous-unemotional traits group were compared with those in the ADHD and comparison groups.nnnRESULTSnIn youths with callous-unemotional traits, amygdala activation was reduced relative to healthy comparison subjects and youths with ADHD while processing fearful expressions, but not neutral or angry expressions. Functional connectivity analyses demonstrated greater correlations between the amygdala and the ventromedial prefrontal cortex in comparison subjects and youths with ADHD relative to those with callous-unemotional traits. Symptom severity in the callous-unemotional traits groups was negatively correlated with connectivity between amygdala and ventromedial prefrontal cortex.nnnCONCLUSIONSnThis is the first study to demonstrate reduced amygdala responsiveness in youths with callous-unemotional traits. These findings support the contention that callous and unemotional personality traits are associated with reduced amygdala response to distress-based social cues.

Abnormal ventromedial prefrontal cortex function in children with psychopathic traits during reversal learning.

CONTEXTnChildren and adults with psychopathic traits and conduct or oppositional defiant disorder demonstrate poor decision making and are impaired in reversal learning. However, the neural basis of this impairment has not previously been investigated. Furthermore, despite high comorbidity of psychopathic traits and attention-deficit/hyperactivity disorder, to our knowledge, no research has attempted to distinguish neural correlates of childhood psychopathic traits and attention-deficit/hyperactivity disorder.nnnOBJECTIVEnTo determine the neural regions that underlie the reversal learning impairments in children with psychopathic traits plus conduct or oppositional defiant disorder.nnnDESIGNnCase-control study.nnnSETTINGnGovernment clinical research institute.nnnPARTICIPANTSnForty-two adolescents aged 10 to 17 years: 14 with psychopathic traits and oppositional defiant disorder or conduct disorder, 14 with attention-deficit/hyperactivity disorder only, and 14 healthy controls.nnnMAIN OUTCOME MEASUREnBlood oxygenation level-dependent signal as measured via functional magnetic resonance imaging during a probabilistic reversal task.nnnRESULTSnChildren with psychopathic traits showed abnormal responses within the ventromedial prefrontal cortex (Brodmann area 10) during punished reversal errors compared with children with attention-deficit/hyperactivity disorder and healthy children (P < .05 corrected for multiple comparisons).nnnCONCLUSIONSnTo our knowledge, this study provides the first evidence of abnormal ventromedial prefrontal cortex responsiveness in children with psychopathic traits and demonstrates this dysfunction was not attributable to comorbid attention-deficit/hyperactivity disorder. These findings suggest that reversal learning impairments in patients with developmental psychopathic traits relate to abnormal processing of reinforcement information.

Oxytocin improves specific recognition of positive facial expressions

BackgroundOxytocin is a neuropeptide that is associated with increased trust. Perceptions of trustworthiness are associated with detection of positive facial affect, which suggests that oxytocin may enhance the recognition of positive facial affect. The present study tests this hypothesis.MethodsA double-blind, between-groups design was used, with 50 volunteers randomly assigned to receive intranasally administered oxytocin or placebo. Thirty-five minutes following the administration of oxytocin or placebo, participants identified anger, disgust, fear, happiness, sadness, and surprise expressions that were morphed with neutral faces such that they varied from 10% to 100% intensity.ResultsOxytocin significantly and specifically improved the recognition of happy facial expressions; no significant differences in recognition of other expression were found. The improvement was not associated with gender, response biases, or changes in mood, and it was most pronounced for subtle expressions.ConclusionsAcute oxytocin administration enhances healthy adults’ ability to accurately identify positive emotional facial expressions. These findings reinforce oxytocin’s role in facilitating affiliative interactions and have implications for the treatment of conditions that are marked by social affiliation deficits.

Disrupted Reinforcement Signaling in the Orbitofrontal Cortex and Caudate in Youths With Conduct Disorder or Oppositional Defiant Disorder and a High Level of Psychopathic Traits

OBJECTIVEnDysfunction in the amygdala and orbitofrontal cortex has been reported in youths and adults with psychopathic traits. The specific nature of the functional irregularities within these structures remains poorly understood. The authors used a passive avoidance task to examine the responsiveness of these systems to early stimulus-reinforcement exposure, when prediction errors are greatest and learning maximized, and to reward in youths with psychopathic traits and comparison youths.nnnMETHODnWhile performing the passive avoidance learning task, 15 youths with conduct disorder or oppositional defiant disorder plus a high level of psychopathic traits and 15 healthy subjects completed a 3.0-T fMRI scan.nnnRESULTSnRelative to the comparison youths, the youths with a disruptive behavior disorder plus psychopathic traits showed less orbitofrontal responsiveness both to early stimulus-reinforcement exposure and to rewards, as well as less caudate response to early stimulus-reinforcement exposure. There were no group differences in amygdala responsiveness to these two task measures, but amygdala responsiveness throughout the task was lower in the youths with psychopathic traits.nnnCONCLUSIONSnCompromised sensitivity to early reinforcement information in the orbitofrontal cortex and caudate and to reward outcome information in the orbitofrontal cortex of youths with conduct disorder or oppositional defiant disorder plus psychopathic traits suggests that the integrated functioning of the amygdala, caudate, and orbitofrontal cortex may be disrupted. This provides a functional neural basis for why such youths are more likely to repeat disadvantageous decisions. New treatment possibilities are raised, as pharmacologic modulations of serotonin and dopamine can affect this form of learning.

Nonverbal “Accents” Cultural Differences in Facial Expressions of Emotion

We report evidence for nonverbal “accents,” subtle differences in the appearance of facial expressions of emotion across cultures. Participants viewed photographs of Japanese nationals and Japanese Americans in which posers muscle movements were standardized to eliminate differences in expressions, cultural or otherwise. Participants guessed the nationality of posers displaying emotional expressions at above-chance levels, and with greater accuracy than they judged the nationality of the same posers displaying neutral expressions. These findings indicate that facial expressions of emotion can contain nonverbal accents that identify the expressers nationality or culture. Cultural differences are intensified during the act of expressing emotion, rather than residing only in facial features or other static elements of appearance. This evidence suggests that extreme positions regarding the universality of emotional expressions are incomplete.

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

BACKGROUNDnPsychopathic 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.nnnMETHODnWe 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.nnnRESULTSnYouths 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.nnnCONCLUSIONSnYouths with psychopathic traits show less responsiveness in regions implicated in the affective response to anothers pain as the perceived intensity of this pain increases. Moreover, this reduced responsiveness appears to predict symptom severity.

What Do I Think You're Doing? Action Identification and Mind Attribution

The authors examined how a perceivers identification of a target persons actions co-varies with attributions of mind to the target. The authors found in Study 1 that the attribution of intentionality and cognition to a target was associated with identifying the targets action in terms of high-level effects rather than low-level details. In Study 2, both action identification and mind attribution were greater for a liked target, and in Study 3, they were reduced for a target suffering misfortune. In Study 4, it was again found that action identification and mind attribution were greater for a liked target, but like that for the self or a liked other, positive actions were identified at higher levels than negative actions, with the reverse being true for disliked others. In Study 5, the authors found that instructing participants to adopt the targets perspective did not affect mind attribution but did lead to higher level identifications of the targets actions.

Reduced amygdala response in youths with disruptive behavior disorders and psychopathic traits: Decreased emotional response versus increased top-down attention to nonemotional features

OBJECTIVEnAmygdala dysfunction has been reported to exist in youths and adults with psychopathic traits. However, there has been disagreement as to whether this dysfunction reflects a primary emotional deficit or is secondary to atypical attentional control. The authors examined the validity of the contrasting predictions.nnnMETHODnParticipants were 15 children and adolescents (ages 10–17 years) with both disruptive behavior disorders and psychopathic traits and 17 healthy comparison youths. Functional MRI was used to assess the response of the amygdala and regions implicated in top-down attentional control (the dorsomedial and lateral frontal cortices) to emotional expression under conditions of high and low attentional load.nnnRESULTSnRelative to youths with disruptive behavior disorders and psychopathic traits, healthy comparison subjects showed a significantly greater increase in the typical amygdala response to fearful expressions under low relative to high attentional load conditions. There was also a selective inverse relationship between the response to fearful expressions under low attentional load and the callous-unemotional component (but not the narcissism or impulsivity component) of psychopathic traits. In contrast, the two groups did not differ in the significant recruitment of the dorsomedial and lateral frontal cortices as a function of attentional load.nnnCONCLUSIONSnYouths with disruptive behavior disorders and psychopathic traits showed reduced amygdala responses to fearful expressions under low attentional load but no indications of increased recruitment of regions implicated in top-down attentional control. These findings suggest that the emotional deficit observed in youths with disruptive behavior disorders and psychopathic traits is primary and not secondary to increased top-down attention to nonemotional stimulus features.

Reduced amygdala-orbitofrontal connectivity during moral judgments in youths with disruptive behavior disorders and psychopathic traits.

We used functional magnetic resonance imaging (fMRI) to investigate dysfunction in the amygdala and orbitofrontal cortex in adolescents with disruptive behavior disorders and psychopathic traits during a moral judgment task. Fourteen adolescents with psychopathic traits and 14 healthy controls were assessed using fMRI while they categorized illegal and legal behaviors in a moral judgment implicit association task. fMRI data were then analyzed using random-effects analysis of variance and functional connectivity. Youths with psychopathic traits showed reduced amygdala activity when making judgments about legal actions and reduced functional connectivity between the amygdala and orbitofrontal cortex during task performance. These results suggest that psychopathic traits are associated with amygdala and orbitofrontal cortex dysfunction. This dysfunction may relate to previous findings of disrupted moral judgment in this population.

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

IMPORTANCEnAmong 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.nnnOBJECTIVEnTo 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.nnnDESIGN, SETTING, AND PARTICIPANTSnThis 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.nnnMAIN OUTCOMES AND MEASURESnBlood 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.nnnRESULTSnAnalysis 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 =u2009-12; k = 1) and positively associated with externalizing behavior (x = 24, y = 0, z =u2009-14; k = 8) when both variables were modeled simultaneously. Reduced amygdala responses mediated the relationship between CU traits and proactive aggression.nnnCONCLUSIONS AND RELEVANCEnThe 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.