Neural responses to affective and cognitive theory of mind in children with conduct problems and varying levels of callous-unemotional traits (original) (raw)
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Amygdala Hypoactivity to Fearful Faces In Boys With Conduct Problems and Callous-Unemotional Traits
American Journal of …, 2009
OBJECTIVE: Although early-onset conduct problems predict both psychiatric and health problems in adult life, little research has been done to index neural correlates of conduct problems. Emerging research suggests that a subgroup of children with conduct problems and elevated levels of callous-unemotional traits may be genetically vulnerable to manifesting disturbances in neural reactivity to emotional stimuli indexing distress. Using functional MRI, the authors evaluated differences in neural response to emotional stimuli between boys with conduct problems and elevated levels of callous-unemotional traits and comparison boys. METHOD: Seventeen boys with conduct problems and elevated levels of callous-unemotional traits and 13 comparison boys of equivalent age (mean=11 years) and IQ (mean=100) viewed blocked presentations of fearful and neutral faces. For each face, participants distinguished the sex of the face via manual response. RESULTS: Relative to the comparison group, boys with conduct problems and elevated levels of callous-unemotional traits manifested lesser right amygdala activity to fearful faces. CONCLUSIONS: This finding is in line with data from studies of adults with antisocial behavior and callous-unemotional traits (i.e., psychopaths), as well as from a recent study of adolescents with callous-unemotional traits, and suggests that the neural substrates of emotional impairment associated with callous-unemotional antisocial behavior are already present in childhood.
The ability to empathize relies in part on using one’s own affective experience to simulate the affective experience of others. This process is supported by a number of brain areas including the anterior insula (AI), anterior cingulate cortex (ACC), medial prefrontal cortex (mPFC), and the amygdala. Children with conduct problems (CP), and in particular those with high levels of callous-unemotional traits (CP/HCU) present with less empathy than their peers. They also show reduced neural response in areas supporting empathic processing when viewing other people in distress. The current study focused on identifying brain areas co-activated during affective introspection of: i) One’s own emotions (‘Own emotion’); ii) Others’ emotions (‘Other emotion’); and iii) One’s feelings about others’ emotions (‘Feel for other’) during fearful vs neutral scenarios in typically developing boys (TD; n = 31), boys with CP/HCU (n = 31), and boys with CP and low levels of CU (CP/LCU; n = 33). The conjunction analysis across conditions within the TD group revealed significant clusters of activation in the AI, ACC/mPFC, and occipital cortex. Conjunction analyses across conditions in the CP/HCU and CP/LCU groups did not identify these areas as significantly activated. However, follow-up analyses were not able to confirm statistically significant differences between groups across the whole network, and Bayes-factor analyses did not provide substantial support for either the null or alternate hypotheses. Post-hoc comparisons indicated that the lack of conjunction effects in the CP/HCU group may reflect reduced affective introspection in the ‘Other emotion’ and ‘Feel for other’ conditions, and by reduced affective introspection in the ‘Own emotion’ condition in the CP/LCU group. These findings provide limited and ultimately equivocal evidence for altered affective introspection regarding others in CP/HCU, and altered affective introspection for own emotions in CP/LCU, and highlight the need for further research to systematically investigate the precise nature of empathy deficits in children with CP.
NeuroImage, 2007
The goal of this study was to determine whether brain regions implicated in emotion processing show structural alterations in adolescents with conduct disorder (CD). Using an optimized voxel-based morphometry protocol, we compared grey matter volume in 12 patients with CD and 12 age-, sex-, and intelligence-matched control subjects. Grey matter volume in bilateral anterior insular cortex and the left amygdala was significantly reduced in CD patients compared to healthy control subjects. The insular grey matter abnormalities could be attributed to aggressive behaviour. Moreover, bilateral anterior insular grey matter volume in CD patients correlated significantly with empathy scores. These novel findings point at a joint neuroanatomical substrate underpinning aggressive behaviour and impaired capacity of empathy and suggest a critical role for the anterior insula in regulating social behaviour.
"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 callousunemotional 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 study’s findings complement increasing evidence suggesting that callous-unemotional traits are an important specifier in the classification of children with conduct problems."
American Journal of Psychiatry, 2008
Objective: Extensive 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.
Because youth with aggressive conduct disorder (CD) often inflict pain on others, it is important to determine if they exhibit atypical empathic responses to viewing others in pain. In this initial functional magnetic resonance imaging (fMRI) study, 8 adolescents with aggressive CD and 8 matched controls were scanned while watching animated visual stimuli depicting other people experiencing pain or not experiencing pain. Furthermore, these situations involved either an individual whose pain was caused by accident or an individual whose pain was inflicted on purpose by another person. After scanning, participants rated how painful the situations were. In both groups the perception of others in pain was associated with activation of the pain matrix, including the ACC, insula, somatosensory cortex, supplementary motor area and periaqueductal gray. The pain matrix was activated to a significantly greater extent in participants with CD, who also showed strong amygdala, ventral striatum, and temporal pole activation. When watching situations in which pain was intentionally inflicted, control youth also exhibited signal increase in the medial prefrontal frontal cortex, lateral obitofrontal cortex, and temporoparietal junction, whereas youth with CD only exhibited activation in the insula. Furthermore, connectivity analyses demonstrated that youth with CD exhibited less amygdala/prefrontal coupling when watching pain inflicted by another than did control youth. These preliminary findings suggest that youth with aggressive CD exhibit an atypical pattern of neural response to viewing others in pain that should be explored in further studies.
The presence of elevated callous unemotional (CU) traits seems to designate a distinct group of children and adolescents with serious conduct problems. However, the extent to which CU traits impact the aversive reaction to harm is still a contentious issue. Here, we examined the effective connectivity seeded in the anterior insula and anterior cingulate cortex in a large number of children (N = 123, age 9–11, 60 females) with various levels of conduct disorder (CD) symptoms in response to visual stimuli depicting other people being physically injured. Perceiving others being harmed was associated with increased hemodynamic activity in the left amygdala and right temporoparietal junction (rTPJ). Children with higher callous traits showed less functional connectivity seeded in anterior cingulate with left amygdala and anterior insula. Conversely, CD symptoms were positively related to connectivity of insula with rTPJ. Overall, these results suggest that callousness is marked by the disruption of widespread cortical networks responsible for detecting and appropriately responding to important environmental cues, such as the distress of others. Children who exhibit conduct problems (CP), such as aggression, cruelty, and theft, are more likely to behave antisocially and immorally as adults, are at a higher risk of developing psychopathy and present a serious public health challenge 1,2. Moreover, scholars working to extend the specific personality traits which characterize adult psychopathy to younger populations have identified callous-unemotional (CU) traits as another important risk factor for serious conduct problems 3,4. These affective and interpersonal aspects, such as the lack of guilt, remorse, and empathy, are associated with greater delinquency, both in children with and without CP, predictive of adult psychopathy, and are relatively stable across development 5–7. Thus, identifying the impact of CU traits on neural processing during empathy-eliciting tasks in children could provide important insights into the neural mechanisms underlying the development of adult antisocial behaviors 8. Examining the neural response to the observation or imagination of others in distress or physical pain provides one of the most useful models of empathy 9. Perceiving another individual in distress triggers an harm aversion response, which can be coupled with feelings of concern for that person, two basic elements of empathy 10. Neuroscientific investigations, using functional MRI, magnetoencephalography, and electrophysiology have employed this paradigm in adult populations to identify associations between psychopathic traits and atypi-cal neural activation and connectivity when viewing harm to others, both in forensic and nonforensic populations 10–14. However, this work has only recently been extended to children with behavioral problems 15–19 , and it remains unclear to which extent CU traits influence functional connectivity during the perception of pain in preadolescents. Early functional neuroimaging studies of empathy have utilized pain perception tasks, and demonstrated overlapping neural activation in anterior insula (aINS), dorsal anterior cingulate (dACC), brainstem, and cere-bellum, both for the experience of somatic pain and the observation of another in pain or emotional distress 20 (for a meta-analysis). While these regions are reliably recruited in studies of empathy for pain, greater activity in these regions during these tasks may not reflect empathic processing per se, but rather pain recognition 9 and
Mapping the developmental pathways of child conduct problems through the neurobiology of empathy
Neuroscience & Biobehavioral Reviews, 2017
The notion that antisocial behavior reflects failures of empathy has a long history in the clinical literature, yet only recently has evidence emerged to support neuroscientific accounts of empathy and the development of child conduct problems. Much of this evidence has come from research into callous-unemotional traits, which correspond to the affective component of psychopathy and therefore encompass deficits in empathy within a broader cluster of emotional impairments. In this review we integrate current evidence concerning the biobehavioral bases of empathy and callous-unemotional traits, and discuss how it may inform models of heterogeneous subgroups of individuals with early onset conduct problems. We argue that somewhat distinct failures of empathy map onto distinct risk pathways to early onset conduct problems, and that these pathways may be best understood by examining empathy in terms of cognitive and environmental prerequisites and the various neurochemical systems implicated therein.
Neural Abnormalities in Early-Onset and Adolescence-Onset Conduct Disorder
Archives of General Psychiatry, 2010
Context: Conduct disorder (CD) is characterized by severe antisocial behavior that emerges in childhood (early-onset CD [EO-CD]) or adolescence (adolescenceonset CD [AO-CD]). Early-onset CD is proposed to have a neurodevelopmental basis, whereas AO-CD is thought to emerge owing to social mimicry of deviant peers. However, this developmental taxonomic theory is debated after reports of neuropsychological impairments in both CD subtypes. A critical, although unaddressed, issue is whether these subtypes present similar or distinct neurophysiological profiles. Hence, we investigated neurophysiological responses to emotional and neutral faces in regions associated with antisocial behavior (ie, the amygdala, ventromedial prefrontal cortex, insula, and orbitofrontal cortex) in individuals with EO-CD and AO-CD and in healthy control subjects.