Neurophysiological Evidence of Motor Preparation Dysfunction during Inner Speech and its Association with Auditory Verbal Hallucinations in Schizophrenia Spectrum Disorders

Background and Hypothesis Auditory verbal hallucinations (AVH) are hypothesized to result from failures in corollary discharge mechanisms to correctly predict self-initiated inner speech. However, the role of motor preparation in inner speech, during which sensorimotor predictions are formed, remains unclear. This study aimed to test the hypothesis by examining the relationship between AVH and an electrophysiological marker of action preparation: the contingent negative variation (CNV). Study Design Participants completed an electroencephalographic paradigm. In the Active condition, they imagined an inner syllable at a cued moment coinciding with the presentation of an audible syllable. In the Passive condition, participants passively listened to audible syllables. The amplitude of the late CNV preceding inner speech production was compared with that associated with passive listening across 3 groups: (1) schizophrenia spectrum patients with current AVH (SZAVH+, n = 58), (2) schizophrenia spectrum patients without current AVH (SZAVH-, n = 50), and (3) healthy controls (HC, n = 49). Study Results The HC group showed a more negative late CNV in the Active condition compared with the Passive condition. In contrast, the SZAVH+ and SZAVH- groups showed positive-going slow cortical potentials in both conditions, with less positivity in the Active condition in the former. This pattern significantly predicted AVH status. Conclusions These findings provide evidence of motor preparation dysfunction during inner speech in schizophrenia spectrum disorders. The distinct pattern of deficits observed in hallucinators may reflect imprecise corollary discharges theorized to underlie some AVH. Premovement neural indices may provide a novel window into abnormalities in prediction formation.