Social cognition deficits are prominent in several psychiatric disorders and personality dimensions, particularly in individuals exhibiting high psychopathic traits. These deficits often manifest as deviant brain activity within the social brain network, encompassing cortical and subcortical subsystems like the mirror neuron system (MNS), mentalizing system, empathy system, and limbic system. Previous research on the neural correlates of psychopathy has yielded inconsistent findings, potentially due to several factors. Firstly, psychopathy encompasses diverse subtypes (primary and secondary) with varying phenotypic and neurofunctional characteristics. Primary psychopathy is characterized by low anxiety, manipulativeness, and callousness, with deficits in responding to others' distress and dysfunction in the amygdala and anterior insula (aINS). Secondary psychopathy, however, involves high anxiety, impulsivity, and emotional reactivity, demonstrating a different pattern of social cognitive abilities and deficits. A second factor is the common focus on visual stimuli in previous research, neglecting the crucial role of auditory communication (speech and non-speech vocalizations) in social interaction. Voice signals are embedded within complex social contexts and carry temporal structural properties that may influence the detection and processing of social information. This necessitates investigation beyond the often-studied visual social recognition tasks. A third factor involves the unexplored overlap between psychopathy and other conditions, especially autism spectrum disorder (ASD) and autistic traits. Both psychopathy and ASD share some social cognitive deficits and neurofunctional impairments, particularly within the empathy and limbic networks. However, individuals with ASD often exhibit challenges with cognitive empathy but maintain affective empathy. Furthermore, a high percentage of individuals with ASD also experience sensory processing difficulties. This study aimed to address these limitations by employing a parametric neuroimaging approach to investigate the differential influence of psychopathic and autistic traits on the neurofunctional mechanisms underlying social perception, specifically focusing on responses to social voice stimuli. The researchers hypothesized that these traits would differentially correlate with neurofunctional diversity across the social cognitive and affective brain networks.

The literature review extensively covers studies on the neural underpinnings of social cognition deficits in psychopathy and autism. Studies focusing on the neural correlates of psychopathy highlight dysfunctional brain activity in the cognitive social brain nodes and their connections, but results have been inconsistent. The authors explain that this inconsistency could be due to a lack of consideration of psychopathy subtypes (primary and secondary), a focus on visual stimuli instead of auditory communication signals, and a lack of comparative studies with other conditions like autism. They review studies highlighting the distinct phenotypic and neurofunctional differences between primary and secondary psychopathy. The review also examines the importance of auditory communication in social interaction, including the role of nonverbal and speech communication in conveying social information. Finally, existing literature on the overlap between psychopathy and autistic traits is presented, emphasizing shared and unique cognitive, neurofunctional, and genetic links. A significant finding highlighted is the 90% prevalence of sensory processing symptoms in ASD patients, often correlating with auditory voice area activation. The review sets the stage for the current study, which aims to address the limitations of previous research by employing a parametric neuroimaging approach with auditory stimuli, and comparing the influence of both psychopathic and autistic traits.

This study used functional magnetic resonance imaging (fMRI) to investigate brain activity during auditory communication sound processing in 113 participants (47 male, 66 female; aged 18-40, mean age 25.59). Participants underwent fMRI while performing a one-back task with 500 ms sound recordings, including 70 human voice sounds (speech and non-speech), and 70 non-voice sounds (animal, artificial, and natural sounds). Behavioral data (reaction times and accuracy) were analyzed using a one-way repeated-measures ANOVA. Psychopathic traits were assessed using the Levenson Self-Report Psychopathy Scale (LSRP), measuring primary and secondary psychopathy, and autistic traits were assessed with the Autism-Spectrum Quotient (AQ). Additional personality traits (Big Five Inventory, PANAS, STAI, BDI) were also measured. fMRI data were preprocessed using SPM12, with a GLM analysis including regressors for each sound condition and motion correction parameters. Contrasts were performed to identify brain activity patterns associated with general and specific voice processing. Region-of-interest (ROI) analysis focused on significant clusters from the initial analysis. Finally, whole-brain analyses investigated the association between neural effects of voice processing and psychopathic/autistic trait scores. Parametric regression analysis was used to determine the influence of personality traits on brain activity, and multiple regression analyses accounted for other personality traits and demographic variables.

The study yielded four key findings. First, a phenotypic overlap was observed between secondary, but not primary, psychopathy and autistic traits. Second, primary psychopathy was associated with various neural deficits in voice processing regions (including the basal ganglia) and social cognition networks (mirroring, mentalizing, empathy). Third, neural deviations in secondary psychopathy were limited to social mirroring and mentalizing impairments, but included novel findings of deficits in auditory sensory processing, possibly involving the ventral auditory stream. Fourth, high autistic traits correlated with neural deviations in sensory cortices, specifically in the dorsal auditory processing streams. Specifically, the LSRP total and primary scores negatively correlated with hit rates in the sound repetition task, suggesting difficulties in detecting sound repetitions in individuals with high psychopathic traits. fMRI analysis revealed that across participants, voice sounds elicited higher activity in bilateral auditory cortices, frontal cortices, and motor cortex. Specific voice categories (speech vs. non-speech) elicited similar activity, with non-speech sounds activating amygdala regions, reflecting their socio-affective nature. Correlations between personality traits and brain activity showed that LSRP total and primary scores correlated positively with activity in the right planum temporale (PTe) and mid-superior temporal cortex (mST) during sound processing. Contrasting voice versus non-voice sound processing, negative correlations were found between psychopathy scores and activity in the infero-orbital frontal cortex (ioFC), amygdala, and anterior cingulate cortex (ACC), highlighting hypoactivity in these regions during voice processing. Multiple regression analysis, controlling for other personality traits and demographic factors, showed that increasing psychopathic traits were negatively associated with activity in widespread brain networks involved in social cognition (MNS, mentalizing, empathy, limbic), and the basal ganglia (BG). The basal ganglia involvement is a novel finding. In contrast, the effect of autistic traits on neural voice processing was relatively limited, with negative correlations in higher-order auditory cortices, ventral premotor cortex, and ACC.

The findings demonstrate that psychopathic and autistic traits differentially influence the neural processing of social communication signals. Primary psychopathy displays widespread hypoactivity across social brain networks, including a novel finding of BG involvement, suggesting a profound deficit in processing the social relevance and meaning of voice signals, consistent with affective empathy deficits and reduced motivation to engage socially. Secondary psychopathy exhibits more specific impairments in social cognitive networks (mirroring, mentalizing), coupled with novel sensory processing deficits. These results suggest that these subtypes may have distinct underlying neural mechanisms. The less extensive neural deficits associated with autistic traits highlight more subtle impairments in social voice processing, predominantly affecting higher-order auditory processing and the encoding of communicative context. The lack of significant overlap between the neural effects of psychopathic and autistic traits reinforces the distinct nature of these phenotypes and their unique impact on social brain functioning. The study's results underscore the importance of considering psychopathy subtypes, employing auditory stimuli in social cognition research, and the unique contributions of sensory processing to social deficits in psychopathy and ASD. Future research should explore the longitudinal development of these neural patterns and investigate potential therapeutic targets based on these distinct neurocognitive profiles.

This study provides novel insights into the differential neural mechanisms underlying social cognition deficits in psychopathy and autism. The findings highlight the importance of considering psychopathy subtypes and incorporating auditory stimuli into future research. The distinct neural profiles identified may inform the development of targeted interventions. Future studies should investigate longitudinal development and explore potential therapeutic targets based on these unique neurocognitive profiles. This could involve more detailed analysis of the distinct contributions of different amygdala subnuclei, investigating potential sensory processing deficits in larger samples of primary psychopathy and secondary psychopathy, and exploring the interplay between these distinct neurocognitive profiles with various behavioral and affective measures.

The study's cross-sectional design limits causal inferences. The use of self-report measures for personality traits introduces potential biases. The sample, while large, might not fully represent the diversity of psychopathic and autistic traits in the general population. The focus on auditory stimuli limits the generalizability to other modalities. The relatively limited diversity of non-social sounds used warrants consideration for future studies.