Psychopathic and autistic traits differentially influence the neural mechanisms of social cognition from communication signals

Abstract

Psychopathy is associated with severe deviations in social behavior and cognition. While previous research described such cognitive and neural alterations in the processing of rather specific social information from human expressions, some open questions remain concerning central and differential neurocognitive deficits underlying psychopathic behavior. Here we investigated three rather unexplored factors to explain these deficits, first, by assessing psychopathy subtypes in social cognition, second, by investigating the discrimination of social communication sounds (speech, non-speech) from other non-social sounds, and third, by determining the neural overlap in social cognition impairments with autistic traits, given potential common deficits in the processing of communicative voice signals. The study was exploratory with a focus on how psychopathic and autistic traits differentially influence the function of social cognitive and affective brain networks in response to social voice stimuli. We used a parametric data analysis approach from a sample of 113 participants (47 male, 66 female) with ages ranging between 18 and 40 years (mean 25.59, SD 4.79). Our data revealed four important findings. First, we found a phenotypical overlap between secondary but not primary psychopathy with autistic traits. Second, primary psychopathy showed various neural deficits in neural voice processing nodes (speech, non-speech voices) and in brain systems for social cognition (mirroring, mentalizing, empathy, emotional contagion). Primary psychopathy also showed deficits in the basal ganglia (BG) system that seems specific to the social decoding of communicative voice signals. Third, neural deviations in secondary psychopathy were restricted to social mirroring and mentalizing impairments, but with additional and so far undescribed deficits at the level of auditory sensory processing, potentially concerning deficits in ventral auditory stream mechanisms (auditory object identification). Fourth, high autistic traits also revealed neural deviations in sensory cortices, but rather in the dorsal auditory processing streams (communicative context encoding). Taken together, social cognition of voice signals shows considerable deviations in psychopathy, with differential and newly described deficits in the BG system in primary psychopathy and at the neural level of sensory processing in secondary psychopathy. These deficits seem especially triggered during the social cognition from vocal communication signals.

The relationship between psychopathy and autism: a systematic review and narrative synthesis

“…In terms of limitations of the included research, only two studies ( 67 , 74 ) differentiated between primary and secondary psychopathy and none considered the impact of adverse childhood experiences. In psychopathy research, children with CUTs showed strongest deficits in emotion recognition when there was no history of maltreatment, suggesting that this may be a feature of the primary variant only ( 108 ).…”

“…Skjegstad et al. ( 74 ) reported deficits in both trait groups for socio-affective processing, but again these showed different areas of association; autistic traits were associated with deficits in dorsal auditory processing streams (used for communication context encoding), whilst psychopathic traits were associated with hypoactivity in socio-affective processing networks. This study was exploratory and lacked an a priori power calculation, but both studies suggested distinct neural mechanisms across these constructs.…”

“…No correlation between autistic traits and factor one (interpersonal) was found. Only one study differentiated primary and secondary psychopathy, reporting a positive correlation between autistic traits and secondary psychopathy traits only ( 74 ). All the aforementioned studies measured autistic traits, and only one study recruited adults with a diagnosis of autism and intellectual disability, observing a small but significant positive relationship between autism and CUTs ( 65 ).…”