Abstract

SummaryHumans are intrinsically social animals, forming enduring affiliative bonds [1]. However, a striking minority with psychopathic traits, who present with violent and antisocial behaviors, tend to value other people only insofar as they contribute to their own advancement [2, 3]. Extant research has addressed the neurocognitive processes associated with aggression in such individuals, but we know remarkably little about processes underlying their atypical social affiliation. This is surprising, given the importance of affiliation and bonding in promoting social order and reducing aggression [4, 5]. Human laughter engages brain areas that facilitate social reciprocity and emotional resonance, consistent with its established role in promoting affiliation and social cohesion [6, 7, 8]. We show that, compared with typically developing boys, those at risk for antisocial behavior in general (irrespective of their risk of psychopathy) display reduced neural response to laughter in the supplementary motor area, a premotor region thought to facilitate motor readiness to join in during social behavior [9, 10, 11]. Those at highest risk for developing psychopathy additionally show reduced neural responses to laughter in the anterior insula. This region is implicated in auditory-motor processing and in linking action tendencies with emotional experience and subjective feelings [10, 12, 13]. Furthermore, this same group reports reduced desire to join in with the laughter of others—a behavioral profile in part accounted for by the attenuated anterior insula response. These findings suggest that atypical processing of laughter could represent a novel mechanism that impoverishes social relationships and increases risk for psychopathy and antisocial behavior.

Highlights

  • In the supplementary motor area (SMA), differences were detected for typically developing boys versus disruptive boys with high callous-unemotional traits (MNI coordinates for peak voxel: x = À14, y = À9, z = 58; t(1,61) = 4.14, z = 3.87; p = 0.043, small-volume family-wise error correction (SVC FWE); cluster size = 64 voxels; Figure 1B) and for typically developing boys versus disruptive boys with low callous-unemotional traits (cluster 1, MNI coordinates for peak voxel: x = 15, y = 6, z = 52; t(1,59) = 4.42, z = 4.09; p = 0.02, SVC FWE; cluster size = 132 voxels; cluster 2, MNI coordinates for peak voxel: x = À14, y = À1, z = 52; t(1,59) = 4.24, z = 3.95; p = 0.03, SVC FWE; cluster size = 101 voxels)

  • We found a correlation between ratings of desire to join in with laughter and anterior insula (AI) responses to laughter across the two groups (r = 0.34, p < 0.01; Figure 2B); in addition, importantly, AI responses to laughter mediated the effect of group on ratings of desire to join in with laughter

  • There were no group differences in responses to laughter within primary auditory regions or within 10-mm spheres around auditory peaks revealed by the main effect of laughter across all participants, both for typically developing boys versus boys with high callous-unemotional traits and for typically developing boys versus boys with low callousunemotional traits, suggesting no differences in how the groups responded to laughter at a basic auditory processing level

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Summary

RESULTS AND DISCUSSION

Humans are intrinsically social animals, forming enduring affiliative bonds [1]. a striking minority with psychopathic traits, who present with violent and antisocial behaviors, tend to value other people only insofar as they contribute to their own advancement [2, 3]. There were no group differences in responses to laughter within primary auditory regions or within 10-mm spheres around auditory peaks revealed by the main effect of laughter across all participants (left: MNI coordinates: x = À46, y = À18, z = 1; right: MNI coordinates: x = 51, y = À10, z = À2), both for typically developing boys versus boys with high callous-unemotional traits and for typically developing boys versus boys with low callousunemotional traits, suggesting no differences in how the groups responded to laughter at a basic auditory processing level These findings provide the first empirical evidence that boys with disruptive behavior show atypical neural responses to laughter, a primitive and potent social cue that plays a major role in facilitating social affiliation and promoting and maintaining social bonds. D KEY RESOURCES TABLE d CONTACT FOR RESOURCE SHARING d EXPERIMENTAL MODEL AND SUBJECT DETAILS

B Participants d METHOD DETAILS
Findings
METHOD DETAILS
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