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

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

Voice-Identity Processing Deficit - The Cognitive and Neural Mechanisms of Phonagnosia

Die Stimme ist reich an grundlegenden Kommunikationselementen: Sie transportiert Sprache, sowie auch paralinguistische Informationen, wie den emotionale Zustand und die Identität des Sprechers. Im Vergleich zur Sprach- und Emotionsverarbeitung ist die Stimmerkennung bei weitem weniger gut erforscht. Dies ist erstaunlich, angesichts der allgegenwärtigen Relevanz der stimmbasierten Personenerkennung. Ein Ansatz neue Erkenntnisse zur Stimmerkennung zu erlangen, ist die Untersuchung von Personen, die ein selektives Defizit in der Stimmerkennung aufweisen. Dieses Defizit wird Phonagnosie bezeichnet. In der vorliegenden Dissertation untersuche ich Personen, bei denen Phonagnosie nach einer Hirnschädigung aufgetreten ist (i.e. erworbene Phonagnosie) und Personen, bei denen Phonagnosie entwicklungsbedingt und nicht durch eine offensichtliche Hirnschädigung bedingt ist (i.e. entwicklungsbedingte Phonagnosie). Die zugrunde liegenden kognitiven, neuro-funktionalen und neuro-anatomischen Mechanismen der Phonagnosie habe ich detailliert mit Hilfe von umfangreichen Verhaltensuntersuchungen sowie funktionaler und struktureller Magnetresonanztomographie charakterisiert. Die Ergebnisse der Dissertation bereichern das derzeitige Stimmerkennungsmodel durch: (i) Neue Erkenntnisse darüber welche Gehirnregionen notwendig sind, um eine Stimme zu erkennen. (ii) Und durch die empirische Bekräftigung der Annahme, dass Stimmerkennung ein mehrstufiger kognitiver Prozess ist, der verschiedene Subformen der Phonagnosie bedingt. Darüber hinaus tragen neue wissenschaftliche Erkenntnisse zur Stimmerkennung maßgeblich dazu bei, praktische Anwendungsbereiche wie klinische Therapieprogramme und künstliche Stimmerkennungprogramme weiterzuentwickeln.The voice contains elementary social communication cues: it conveys speech, as well as paralinguistic information pertaining to the emotional state or the identity of the speaker. In contrast to neuroscientific research on vocal-speech and vocal-emotion processing, voice-identity processing has been less explored. This seems surprising, given the day-to-day significance of person recognition by voice. A valuable approach to unravel how voice-identity processing is accomplished is to investigate people who have a selective deficit in voice recognition. Such a deficit has been termed phonagnosia. In the present dissertation, I investigate phonagnosia following brain damage (i.e. acquired phonagnosia), as well as phonagnosia cases without apparent brain lesion (i.e. developmental phonagnosia). I in-depth characterise the underlying cognitive, neural-functional, and neuro-anatomical mechanisms of phonagnosia by means of comprehensive behavioural testing as well as functional and structural magnetic resonance imaging. The findings of this dissertation inform the current model of voice-identity processing by (i) delivering novel evidence of brain regions that crucially contribute to voice-identity processing, and by (ii) emphasising the multistage nature of voice-identity processing. We showed that dysfunction at different cognitive stages results in behaviourally distinct phonagnosia sub-types. Generally, advanced scientific knowledge about voice-identity processing as provided in the current dissertation also propels practical applications such as clinical treatment programs and artificial voice-recognition systems

Categorizing human vocal signals depends on an integrated auditory‐frontal cortical network

Voice signals are relevant for auditory communication and suggested to be processed in dedicated auditory cortex (AC) regions. While recent reports highlighted an additional role of the inferior frontal cortex (IFC), a detailed description of the integrated functioning of the AC–IFC network and its task relevance for voice processing is missing. Using neuroimaging, we tested sound categorization while human participants either focused on the higher‐order vocal‐sound dimension (voice task) or feature‐based intensity dimension (loudness task) while listening to the same sound material. We found differential involvements of the AC and IFC depending on the task performed and whether the voice dimension was of task relevance or not. First, when comparing neural vocal‐sound processing of our task‐based with previously reported passive listening designs we observed highly similar cortical activations in the AC and IFC. Second, during task‐based vocal‐sound processing we observed voice‐sensitive responses in the AC and IFC whereas intensity processing was restricted to distinct AC regions. Third, the IFC flexibly adapted to the vocal‐sounds' task relevance, being only active when the voice dimension was task relevant. Forth and finally, connectivity modeling revealed that vocal signals independent of their task relevance provided significant input to bilateral AC. However, only when attention was on the voice dimension, we found significant modulations of auditory‐frontal connections. Our findings suggest an integrated auditory‐frontal network to be essential for behaviorally relevant vocal‐sounds processing. The IFC seems to be an important hub of the extended voice network when representing higher‐order vocal objects and guiding goal‐directed behavior

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

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.ISSN:2158-318