Boys at risk of psychopathy have reduced neural/behavioral responses to laughter

Psychopathic traits are associated with a lack of enduring affiliative bonds

Humans are intrinsically social animals, forming enduring affiliative bonds []. 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 []. 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 []. Human laughter engages brain areas that facilitate social reciprocity and emotional resonance, consistent with its established role in promoting affiliation and social cohesion []. 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 []. 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 []. 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.

How do you feel--now? The anterior insula and human awareness.

The evolution and functions of laughter and humor: a synthetic approach.

It is not always tickling: distinct cerebral responses during perception of different laughter types.

Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity.

Importance of cooperation and affiliation in the evolution of primate sociality.

Annual research review: A developmental psychopathology approach to understanding callous-unemotional traits in children and adolescents with serious conduct problems.

Results and Discussion

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Wilson D.S. The evolution and functions of laughter and humor: a synthetic approach. 10 Warren J.E.

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Scott S.K. Positive emotions preferentially engage an auditory-motor “mirror” system. Laughter is a universal expression of emotion [] used to maintain social bonds []. It is a highly contagious behavior: it can be primed simply by listening to others’ laughter []. Such emotional contagion has been posited as a mechanism for facilitating the coupling of emotions and behavior within groups, increasing cooperation, cohesiveness, and social connectedness []. The social nature of laughter is evident in that an individual is up to 30 times more likely to laugh when with others than when alone []. Laughter also plays a role in the vicarious experience of positive emotions, and it triggers the endogenous opioid system, argued to be key for prosocial communication and social bonding in primates and other mammals []. Neuroimaging studies demonstrate that listening to laughter automatically recruits motor and premotor regions involved in the production of emotional expressions [], including the precentral gyrus, supplementary motor area, inferior frontal gyrus, and anterior insula []. This preparatory motor response is thought to facilitate joining in with others’ positive vocalizations during social behavior, representing a neural mechanism for experiencing these emotions vicariously and promoting social connectedness []. These findings from typical individuals have established laughter as an ideal probe for examining atypical social affiliation and connectedness.

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Scott S. Callous-unemotional traits in children and mechanisms of impaired eye contact during expressions of love: a treatment target?. Individuals with psychopathy show a reduced capacity to develop social relationships founded on an enjoyment of prosocial interaction or concern for others’ well-being []. More broadly, individuals with persistent antisocial behavior show reduced prosocial functioning and act in way that violates the rights of other people []. Investigating potential mechanisms underpinning impoverished social connectedness in individuals at risk of psychopathy and persistent antisocial behavior has the potential to inform the design of therapeutic approaches to foster prosocial behavior in these individuals who incur substantial societal costs []. Remarkably, there has been no systematic neurocognitive investigation of potential mechanisms of impaired social connectedness in this group of people. Instead, research has focused on how individuals with psychopathic traits and persistent antisocial behavior process other people’s distress []. For example, extant research shows that adults with psychopathy and children at increased risk for psychopathy (those with disruptive behaviors and “callous-unemotional traits” []) show reduced neural and physiological responses to others’ fear and pain []. However, unlike individuals with autism, they do not have difficulties taking the perspective of other people []. Knowing what other people think but not resonating with their feelings facilitates the ability to manipulate and deceive others, in line with one’s own self-interest []. While prosocial emotions likely evolved to promote mutualistic social investment and collaboration within groups [], their absence may represent an alternative adaptive strategy involving promotion of oneself at others’ expense []. Although previous research has addressed the underpinnings of increased behavioral aggression in those at risk for psychopathy and persistent antisocial behavior [], it fails to fully account for the impoverished social affiliation also evident in this group of people [].

7 McGettigan C.

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et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 7 McGettigan C.

Walsh E.

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Sauter D.A.

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Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 10 Warren J.E.

Sauter D.A.

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Dresner M.A.

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Rosen S.

Scott S.K. Positive emotions preferentially engage an auditory-motor “mirror” system. 11 Lima C.F.

Krishnan S.

Scott S.K. Roles of supplementary motor areas in auditory processing and auditory imagery. 20 Lima C.F.

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Evans S.

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Meekings S.

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et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 12 Wattendorf E.

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Celio M.R. Insular cortex activity and the evocation of laughter. 13 Craig A.D.B. How do you feel--now? The anterior insula and human awareness. 36 Carr L.

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Ochsner K.N. Overlapping activity in anterior insula during interoception and emotional experience. We hypothesized that boys with disruptive behaviors would be less responsive to others’ laughter at the neural and behavioral levels, reflecting a potential mechanism underpinning impoverished social connectedness. Specifically, we hypothesized that compared to typically developing controls, boys with disruptive behaviors would show an attenuated subjective desire to join in with the laughter of others and reduced neural activation across premotor and motor areas involved in processing laughter and positive vocalizations: the precentral gyrus, supplementary motor area (SMA), inferior frontal gyrus (IFG), and anterior insula (AI) []. These regions are implicated in auditory-motor integration and motor readiness to join in []. We hypothesized that attenuated responsiveness to laughter across these regions would be particularly characteristic of boys with high levels of callous-unemotional traits and disruptive behaviors who show the most impoverished patterns of social affiliation. Finally, we hypothesized that neural responses to laughter across our regions of interest would in part explain differences in the subjective desire to join in with laughter. This could particularly be the case in the AI, given that, in addition to showing auditory-motor properties, the insular cortex is thought to play a role in linking action information with emotional or motivational experience [] and in representing interoceptive information, providing the basis for subjective emotional awareness [].

7 McGettigan C.

Walsh E.

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Sauter D.A.

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Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 10 Warren J.E.

Sauter D.A.

Eisner F.

Wiland J.

Dresner M.A.

Wise R.J.S.

Rosen S.

Scott S.K. Positive emotions preferentially engage an auditory-motor “mirror” system. 20 Lima C.F.

Lavan N.

Evans S.

Agnew Z.

Halpern A.R.

Shanmugalingam P.

Meekings S.

Boebinger D.

Ostarek M.

McGettigan C.

et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 7 McGettigan C.

Walsh E.

Jessop R.

Agnew Z.K.

Sauter D.A.

Warren J.E.

Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. Here we investigated behavioral and neural responses to laughter in 11- to 16-year-old boys with (1) disruptive behaviors and high callous-unemotional traits (N = 32); (2) disruptive behaviors and low callous-unemotional traits (N = 30); and (3) matched typically developing controls (N = 31). Groups were matched for IQ, age, handedness, ethnicity, and socioeconomic status (demographic information reported in STAR Methods ). We recorded fMRI responses while participants listened to genuine laughter, interleaved with posed laughter and distractor crying sounds. Participants were instructed simply to attend to the stimuli to ensure that potential responses seen in premotor and motor systems could not be accounted for by task-related motor or decisional processes []. To assess whether group differences reflected reactivity to genuine laughter as a basic emotional cue, rather than higher-level processing of the social meaning of laughter, we also included posed laughter (which is more volitional, rather than spontaneous/involuntary []). After scanning, participants completed a behavioral task in which they evaluated each sound on two dimensions (presented in separate blocks) using a seven-point scale: (1) “How much does hearing the sound make you feel like joining in and/or feeling the emotion?” (a behavioral measure of subjective laughter contagion) and (2) “How much does the sound reflect a genuinely felt emotion?” (a behavioral measure of the ability to infer laughter authenticity). Measuring the discrimination between the two types of laughter at behavioral and neural levels allowed us to index the ability to infer the authenticity of the emotional state of the speaker (“emotional authenticity”) (see STAR Methods ).

7 McGettigan C.

Walsh E.

Jessop R.

Agnew Z.K.

Sauter D.A.

Warren J.E.

Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 10 Warren J.E.

Sauter D.A.

Eisner F.

Wiland J.

Dresner M.A.

Wise R.J.S.

Rosen S.

Scott S.K. Positive emotions preferentially engage an auditory-motor “mirror” system. 20 Lima C.F.

Lavan N.

Evans S.

Agnew Z.

Halpern A.R.

Shanmugalingam P.

Meekings S.

Boebinger D.

Ostarek M.

McGettigan C.

et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 38 (1,61) = 4.14, z = 3.87; p = 0.035, SVC FWE; cluster size = 46 voxels) ( (1,61) = 4.14, z = 3.87; p = 0.043, SVC FWE; cluster size = 64 voxels; (1,59) = 4.42, z = 4.09; p = 0.02, SVC FWE; cluster size = 132 voxels; cluster 2, MNI coordinates for peak voxel: x = −14, y = −1, z = 52; t (1,59) = 4.24, z = 3.95; p = 0.03, SVC FWE; cluster size = 101 voxels). For disruptive boys with low callous-unemotional traits, no group differences compared with typically developing boys were found in the remaining ROIs: the precentral gyrus, AI, and IFG. Follow-up analyses also indicated that the two groups of disruptive boys, those with high versus low callous-unemotional traits, did not significantly differ from each other in those ROIs that differentiated either group from the typically developing boys (all p > 0.16), and no additional group differences emerged in whole-brain comparisons. Figure 1 Neural Responses to Laughter across All Participants and Differences between Groups Show full caption (A) Responses to genuine laughter versus rest across all participants, N = 93, p < 0.001 peak level uncorrected, family-wise error (FWE) corrected (p < 0.05) at cluster level. See also Table S1 (B) Responses to genuine laughter (versus rest) in typically developing (TD) boys versus boys with disruptive behavior and high callous-unemotional traits (DB/HCU) (thresholded at p < 0.05 small-volume corrected FWE). See also Table S3 . Error bars represent the standard error of the mean. Whole-brain analyses of responses to genuine laughter across all participants revealed activity across auditory, motor, and premotor, as well as limbic, medial pre-frontal and anterior temporal areas ( Figure 1 A; Table S1 ), consistent with previous studies []. When we compared responses for typically developing boys versus boys with disruptive behavior and high callous-unemotional traits, ROI analyses using small-volume family-wise error correction (SVC FWE) [] revealed the predicted pattern of reduced response in boys with high callous-unemotional traits in the left AI (MNI coordinates for peak voxel: x = −34, y = 3, z = −15; t= 4.14, z = 3.87; p = 0.035, SVC FWE; cluster size = 46 voxels) ( Figure 1 B). In the SMA, differences were detected for typically developing boys versus disruptive boys with high callous-unemotional traits (MNI coordinates for peak voxel: x = −14, y = −9, z = 58; t= 4.14, z = 3.87; p = 0.043, SVC FWE; cluster size = 64 voxels; Figure 1 B) 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= 4.42, z = 4.09; p = 0.02, SVC FWE; cluster size = 132 voxels; cluster 2, MNI coordinates for peak voxel: x = −14, y = −1, z = 52; t= 4.24, z = 3.95; p = 0.03, SVC FWE; cluster size = 101 voxels). For disruptive boys with low callous-unemotional traits, no group differences compared with typically developing boys were found in the remaining ROIs: the precentral gyrus, AI, and IFG. Follow-up analyses also indicated that the two groups of disruptive boys, those with high versus low callous-unemotional traits, did not significantly differ from each other in those ROIs that differentiated either group from the typically developing boys (all p > 0.16), and no additional group differences emerged in whole-brain comparisons.

39 Hayes A.F. Introduction to Mediation, Moderation and Conditional Process Analysis: A Regression-Based Approach. 40 Miller G.A.

Chapman J.P. Misunderstanding analysis of covariance. Table 1 Participant Characteristics and Questionnaire Data TD Controls DB/HCU DB/LCU TD versus DB/HCU TD versus DB/LCU DB/HCU versus DB/LCU (N = 31) (N = 32) (N = 30) p Value a a All p values are Bonferroni corrected and obtained from t tests, except for ethnicity and handedness (Bonferroni-corrected Fisher’s exact tests used). p Value a a All p values are Bonferroni corrected and obtained from t tests, except for ethnicity and handedness (Bonferroni-corrected Fisher’s exact tests used). p Value a a All p values are Bonferroni corrected and obtained from t tests, except for ethnicity and handedness (Bonferroni-corrected Fisher’s exact tests used). Characteristics and Questionnaires Age 13.92 (1.80) 14.66 (1.37) 14.42 (1.61) p = 0.213 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 p > 0.3 Socio-economic status c c Missing data from three DB/LCU participants. 2.83 (1.12) 3.08 (0.82) 2.70 (1.17) p > 0.3 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 p > 0.3 b b Welch’s t test used due to inhomogeneity of variance between groups. F-IQ d d Missing data from two participants (one DB/LCU and one DB/HCU). 101.23 (12.37) 96.90 (11.36) 101.55 (14.18) p > 0.3 p > 0.3 p > 0.3 b b Welch’s t test used due to inhomogeneity of variance between groups. Verbal T score d d Missing data from two participants (one DB/LCU and one DB/HCU). 50.42 (8.54) 46.29 (9.31) 52.97 (11.19) p = 0.221 p > 0.3 b b Welch’s t test used due to inhomogeneity of variance between groups. p = 0.044 Performance T score d d Missing data from two participants (one DB/LCU and one DB/HCU). 50.61 (10.63) 49.71 (7.74) 48.24 (7.76) p > 0.3 p > 0.3 p > 0.3 Ethnicity 18 white, 4 black, 9 mixed 17 white, 6 black, 9 mixed 20 white, 3 black, 7 mixed p > 0.3 p > 0.3 p > 0.3 Handedness 26 right, 5 left 28 right, 4 left 29 right, 1 left p > 0.3 p > 0.3 p > 0.3 Inventory of callous-unemotional traits e e Measures taken at screening phase, comprising parent and teacher report. 24.81 (6.81) 51.19 (6.76) 32.75 (7.43) p < 0.001 p < 0.001 p < 0.001 Conduct disorder symptoms e e Measures taken at screening phase, comprising parent and teacher report. 0.68 (0.79) 11.44 (4.98) 5.43 (2.22) p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. ADHD symptoms f f Measures taken at scanning session: parent report. , g g Missing data from one DB/HCU participant. 12.60 (7.68) 25.60 (11.75) 22.94 (11.38) p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 Generalized anxiety disorder symptoms f f Measures taken at scanning session: parent report. , g g Missing data from one DB/HCU participant. 3.66 (1.96) 9.25 (4.17) 8.43 (4.89) p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 Major depressive symptoms f f Measures taken at scanning session: parent report. , h h Missing data from two DB/LCU participants. 3.19 (1.83) 6.89 (4.37) 5.79 (3.54) p < 0.001 b b Welch’s t test used due to inhomogeneity of variance between groups. p < 0.003 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 Alcohol use and disorders i i Child self-report at scanning session. 0.51 (1.47) 2.42 (3.92) 2.98 (5.46) p = 0.041 b b Welch’s t test used due to inhomogeneity of variance between groups. p = 0.068 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 Drug use and disorders i i Child self-report at scanning session. , j j Missing data from one DB/LCU participant. 0.13 (0.72) 2.13 (4.43) 3.34 (4.92) p = 0.051 b b Welch’s t test used due to inhomogeneity of variance between groups. p < 0.005 b b Welch’s t test used due to inhomogeneity of variance between groups. p > 0.3 Self-rated pubertal development i i Child self-report at scanning session. , k k Missing data from one TD and one DB/LCU participant. 8.90 (2.86) 10.31 (2.87) 8.80 (3.87) p = 0.171 p > 0.3 b b Welch’s t test used due to inhomogeneity of variance between groups. p = 0.261 Behavioral Responses to Laughter Desire to join in with genuine laughter l l Assessed using a behavioral task at scanning session. 4.15 (1.20) 3.26 (1.14) 3.54 (1.20) p = 0.011 p = 0.161 p > 0.3 Authenticity detection l l Assessed using a behavioral task at scanning session. 1.13 (0.83) 0.96 (0.76) 0.87 (0.79) p > 0.3 p > 0.3 p > 0.3 Abbreviations: F-IQ, full IQ score calculated on two-subset Wechsler Abbreviated Scale of Intelligence; ADHD, attention-deficit/hyperactivity disorder; DB/HCU, boys with disruptive behavior and high callous-unemotional traits; DB/LCU, boys with disruptive behavior and low callous-unemotional traits. Figure 2 Group Differences on Perceived Contagiousness of Laughter and Relationship with Neural Responses in the Anterior Insula Show full caption (A) Behavioral data on reported desire to join in with genuine laughter for TD versus DB/HCU boys (significant group difference: t(61) = 3.02, p < 0.01). Error bars represent the standard error of the mean. (B) Anterior insula response for genuine laughter versus rest (beta values extracted from a 10-mm sphere around the peak of the cluster) plotted against reported desire to join in with genuine laughter across TD and DB/HCU boys. Behaviorally, boys with high callous-unemotional traits reported less desire to join in with genuine laughter compared to typically developing boys ( Table 1 Figure 2 A), whereas those with low callous-unemotional traits did not differ from typically developing boys or boys with high callous-unemotional traits ( Table 1 ). Given the behavioral differences between typically developing boys and boys with high callous-unemotional traits, we also examined the relationship between their behavioral and brain data. We found a correlation between ratings of desire to join in with laughter and AI responses to laughter across the two groups (r = 0.34, p < 0.01; Figure 2 B); in addition, importantly, AI responses to laughter mediated the effect of group on ratings of desire to join in with laughter. The total effect of group on ratings of desire to join in was −0.89 (95% confidence interval [CI]: −1.48, −0.30), and the indirect (mediated) effect through AI responses was −0.24 (95% CI: −0.57, −0.05), indicating that approximately 27% of the effect of group on desire to join in was mediated by AI responses [] (full mediation model in Figure S1 ). No such mediation effect was detected in the SMA. Main analyses did not include covariates such as ADHD symptoms, on the basis that it is problematic to covary for variables intrinsically related to group assignment []. However, when analyses were re-run including ADHD symptoms as covariates, all group comparisons remained significant.

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Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 42 Bryant G.A.

Atkipis C.A. The animal nature of spontaneous human laughter. 43 Frühholz S.

Grandjean D. Processing of emotional vocalizations in bilateral inferior frontal cortex. Finally, to examine whether reductions in brain responses related to affiliative rather than higher-level socio-cognitive processes, we contrasted cortical and behavioral discrimination between genuine and posed laughter. Across all participants, whole-brain analyses indicated that genuine laughter elicited stronger responses than posed laughter in the right temporal pole, right IFG, and left superior temporal gyrus ( Table S2 ). These areas are consistent with previous studies on emotional authenticity processing in the auditory domain []. They might be key for processing the prominent acoustic hallmarks that signal genuine laughter (e.g., higher pitch []) and for the higher-order socio-emotional and evaluative processes [] needed to infer whether laughter is posed or genuine. Of the ROIs, increased responses to genuine laughter were only found in the IFG. No supra-threshold clusters were found for the contrast posed laughter > genuine laughter. At the set statistical thresholds, neural and behavioral discrimination between genuine and posed laughter was similar between typically developing boys versus boys with high callous-unemotional traits and between typically developing boys versus boys with low callous-unemotional traits (for behavioral discrimination, see Table 1 ; for neural discrimination, see Tables S3 and S4 , which for completeness report results at p < 0.001 uncorrected, cluster size ≥ 10 voxels). Thus, the capacity to detect emotional authenticity at the neural and behavioral levels did not differ across the three groups.

As an additional control measure, we examined whether differences in basic auditory responses to laughter could account for the observed group differences in response to genuine 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 (left: MNI coordinates: x = −46, y = −18, z = 1; right: MNI coordinates: x = 51, y = −10, z = −2), both for typically developing boys versus boys with high callous-unemotional traits and for typically developing boys versus boys with low callous-unemotional traits, suggesting no differences in how the groups responded to laughter at a basic auditory processing level.

10 Warren J.E.

Sauter D.A.

Eisner F.

Wiland J.

Dresner M.A.

Wise R.J.S.

Rosen S.

Scott S.K. Positive emotions preferentially engage an auditory-motor “mirror” system. 20 Lima C.F.

Lavan N.

Evans S.

Agnew Z.

Halpern A.R.

Shanmugalingam P.

Meekings S.

Boebinger D.

Ostarek M.

McGettigan C.

et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 12 Wattendorf E.

Westermann B.

Lotze M.

Fiedler K.

Celio M.R. Insular cortex activity and the evocation of laughter. 13 Craig A.D.B. How do you feel--now? The anterior insula and human awareness. 36 Carr L.

Iacoboni M.

Dubeau M.-C.

Mazziotta J.C.

Lenzi G.L. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. 6 Scott S.K.

Lavan N.

Chen S.

McGettigan C. The social life of laughter. 7 McGettigan C.

Walsh E.

Jessop R.

Agnew Z.K.

Sauter D.A.

Warren J.E.

Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 11 Lima C.F.

Krishnan S.

Scott S.K. Roles of supplementary motor areas in auditory processing and auditory imagery. 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. Boys with disruptive behavior and high callous-unemotional traits showed reduced responses in the AI, a region associated with automatic facilitation of motor responses to emotional vocalizations [], as well as with the experience of emotions and with linking action information with emotional and motivational processes []. Reduced AI responses to genuine laughter partially explained the lower subjective desire to join in with others’ laughter in boys with high callous-unemotional traits compared with typically developing boys. This suggests a link between AI response and the perceived contagiousness of laughter, which reflects its socio-emotional and motivational salience. More broadly, both groups of boys with disruptive behavior (irrespective of level of callous-unemotional traits) showed reduced responses in the SMA—also part of the network thought to facilitate the automatic priming of laughter when one hears other people laughing [].

27 Blair R.J.R. Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations. Our findings suggest that group differences in responses to genuine laughter were not attributable to difficulties in processing laughter at a basic auditory level or in discriminating different types of laughter (i.e., the capacity to infer social meaning). The latter finding is consistent with evidence of intact theory of mind ability in boys with disruptive behaviors [], although it remains unclear which precise mechanism the boys with disruptive behaviors relied upon to infer authenticity: more basic detection of the acoustic markers that signal authenticity, higher-order socio-emotional and evaluative processes, or both combined. Additionally, the posed stimuli used here were generated by regular (untrained) speakers in a relatively artificial setting. These stimuli are typically perceived as natural and positive, but more research will be needed to determine whether similar findings would be obtained if we had used contextually appropriate posed laughter deployed by trained actors, for example.

Notably, in the present study, direct comparisons between disruptive boys with high and low callous-unemotional traits revealed no significant differences in neural response across ROIs that differentiated either group from typically developing boys. Although significantly reduced AI responses were only seen for the comparison between typically developing boys and boys with high callous-unemotional traits (and, as such, we ran mediation analysis on this group comparison only), we cannot firmly establish the selectivity of this finding to the high callous-unemotional group. It is, of course, possible that different developmental histories underlie atypical laughter processing in boys with high versus low callous-unemotional traits, something that warrants further investigation. Development of social connectedness is a bidirectional process, and the degree to which neural responses to laughter and subjective desire to join in with laughter are a consequence of atypical social connectedness versus experience-independent factors is unclear. This may also vary between children with high versus low callous-unemotional traits. Indeed, potential causes of reduced social connectedness that could give rise to atypical laughter processing might include the canalized development of an alternative social strategy centered on self-interested rather than collaborative behaviors, or various early life experiences or caregiver behaviors.

7 McGettigan C.

Walsh E.

Jessop R.

Agnew Z.K.

Sauter D.A.

Warren J.E.

Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 20 Lima C.F.

Lavan N.

Evans S.

Agnew Z.

Halpern A.R.

Shanmugalingam P.

Meekings S.

Boebinger D.

Ostarek M.

McGettigan C.

et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 7 McGettigan C.

Walsh E.

Jessop R.

Agnew Z.K.

Sauter D.A.

Warren J.E.

Scott S.K. Individual differences in laughter perception reveal roles for mentalizing and sensorimotor systems in the evaluation of emotional authenticity. 11 Lima C.F.

Krishnan S.

Scott S.K. Roles of supplementary motor areas in auditory processing and auditory imagery. 20 Lima C.F.

Lavan N.

Evans S.

Agnew Z.

Halpern A.R.

Shanmugalingam P.

Meekings S.

Boebinger D.

Ostarek M.

McGettigan C.

et al. Feel the noise: relating individual differences in auditory imagery to the structure and function of sensorimotor systems. 13 Craig A.D.B. How do you feel--now? The anterior insula and human awareness. 37 Zaki J.

Davis J.I.

Ochsner K.N. Overlapping activity in anterior insula during interoception and emotional experience. Limitations of the current study include the use of a research diagnosis of conduct disorder as a basis for identifying boys with disruptive behavior, as well as a focus on males. Replication of these findings in a clinically diagnosed sample is important, as well as investigation of potential gender differences. Additionally, our task did not allow us to investigate whether reductions in behavioral contagion and anterior insula response in boys at risk for psychopathy and persistent antisocial behavior were present for other positive emotional expressions. Future studies should address whether these findings are specific to laughter or extend to other types of positive vocalizations, for example sounds of achievement or pleasure [], or to non-vocal social gestures. Furthermore, future studies could include objective indices of contagion responses (e.g., facial electromyography), in addition to the self-report measure of motivation to join in with laughter that we used here. This could help elucidate whether the observed profile of behavioral responses reflects abnormalities in automatic motor contagion responses to laughter, in more subjective (conscious) components of emotional contagion, or both. The combined pattern of brain and behavioral results we obtained suggests that both might be involved. The areas where atypical responses were found, SMA and AI, are both part of the auditory-motor network that has been argued to support the automatic impulse to respond to the emotional expressions of others []. However, we could link perceived emotional contagion with activity in the AI only, not with SMA activity. Given that AI has been additionally implicated in emotional experience and subjective feelings [], this could mean that our behavioral measure is capturing conscious aspects of contagion better than more automatic motor resonance. Objective indices of motor resonance would potentially provide the additional sensitivity needed to detect whether the reduced SMA activity in boys with disruptive behaviors reflects atypical automatic motor contagion. Future studies could also include physiological responses such as heart rate and respiration to index arousal in response to laughter stimuli.