Auditory verbal hallucinations in non-clinical populations: the contribution of language hemispheric lateralization, personality traits, affectivity, and mood factors (C.A.T.C.H. IN. HE.AD. project).

Background: Auditory verbal hallucinations (AVHs) are core symptoms of psychosis, yet only ~25% of AVH hearers meet criteria for a psychotic disorder. AVHs lie on a continuum from clinical to non-clinical populations, but the underlying psychological and neurophysiological factors remain unclear. According to Crow’s hypothesis (1997), a reduced left-hemispheric language lateralization may represent a vulnerability factor for AVHs, as the absence of contralateral inhibition might determine confusion between inner thoughts and external voices. This project aims to develop a standardized protocol to assess electroencephalographic (EEG) language-related laterality mechanisms, together with personality traits, affectivity, and mood factors associated with AVHs in non-clinical individuals. Methods: The complete protocol has been applied to 30 non-clinical individuals with AVHs (recruited via the Italian national association of voice-hearers) and 30 healthy controls (HC), similar for gender, age, and educational level. All participants were adults, right-handed, and Italian native speakers. Participants first completed a set of validated scales assessing psychotic-like experiences (CAPE-15), schizotypal traits (SCID-5-PD), repetitive thinking (PTQ), mood and stress (DASS-21), and regulation strategies (CERQ). AVHs characteristics were assessed with PSYRATS. Next, participants performed a Rhyme Judgment task (selected based on a previous protocol validation study) while the EEG activity was recorded with a 128-channel High-Density EEG. After preprocessing the data, analyses of the event-related potentials (ERP) components and neural generators were performed. Behavioural performances were compared between groups in terms of accuracy and response time. Results: Non-clinical individuals with AVHs reported infrequent, short-lasting, internally located, non-distressing, and highly controllable voices. Compared to HC, they reported more psychotic-like experiences (p<.00001), including persecutory ideation (p<.005), bizarre experiences (p<.00005), and perceptual abnormalities (p<.00001). They also differed from HC in terms of higher schizotypal traits (p<.00001) and higher levels of anxiety (p=.01) and stress (p=.01), while they did not diverge in terms of depressive symptoms and repetitive negative thinking. The cognitive and emotional regulation strategies used by the two groups were mostly similar. EEG results revealed a more bilateral activation pattern in AVH participants across early (P100, N150, N350) ERP components and slow waves (CNV), and source analysis suggested less hemispheric specialization of the linguistic network. Behavioural performance was optimal in both groups (~94% accuracy, ~1000 ms response time) and was not statistically different. Discussion: Non-clinical individuals with AVHs were characterized by higher psychotic-like experiences, schizotypal traits, anxiety and stress levels compared to HC. These differences were accompanied by infrequent, non-distressing, and highly controllable AVHs, which might suggest the presence of a selective psychological profile rather than a global dysfunction. EEG results seem to support Crow's hypothesis, suggesting that a reduced left hemispheric lateralization for language may be a vulnerability factor for AVHs also in non-clinical populations. Bilateral activation patterns in the absence of behavioural deficits might indicate preserved performance through compensatory mechanisms. Albeit based on preliminary results, this protocol provides a promising framework for future investigations along AVHs continuum from non-clinical to psychopathological populations.