Inner speech and the neurobiology of psychosis

Abstract

Aberrations of inner speech have been linked to psychotic symptoms such as thought insertion and auditory verbal hallucinations. These symptoms may reflect failures of prediction and source monitoring. Normally, efference copies of speech motor commands are sent to auditory cortices and suppressed, helping distinguish self-generated from external input. If suppression malfunctions, predicted auditory input may become perceptually salient. Further, if self-monitoring or error detection-related regions are also impaired (e.g., anterior cingulate cortex, ACC), inner speech may be misattributed as external. We tested this proposal using neuroimaging meta-analyses, examining how the brain systems in overt and inner speech production in neurotypical participants overlap with findings from psychosis-spectrum participants performing a range of tasks. They showed increased activity in motor-related regions associated with inner speech (e.g., ventral premotor cortices) and decreased grey matter in bilateral auditory cortices and ACC, in regions specific to overt speech. Coactivation-based network analyses revealed that these ventral premotor and auditory regions form distinct, inversely coupled audiomotor networks. Classification suggests the ventral premotor network supports higher-level language processing, while the audiomotor network supports lower-level speech and self-referential processing. Overall, results accord with the proposal that psychotic symptoms like auditory verbal hallucinations derive from phenotypic hyperactivation in inner speech-related regions that yield affectively salient efference copy signals that are insufficiently suppressed and monitored as self-produced. In line with a hierarchical predictive-processing account, disruption of a distributed recurrent system distorts self-awareness and conscious experience.