Impaired Speaking-Induced Suppression Predicts Degraded Agency and Hallucination Severity in Schizophrenia

Agency is the awareness of being the originator of one's own thoughts and actions. Patients with schizophrenia (SZ) show deficits in agency that contribute to distortions in reality monitoring (RM) (distinguishing self-generated from externally produced information) and psychotic symptoms. Agency is also critical for speech monitoring (SM) (monitoring what we hear ourselves say while speaking). For example, disruptions in agency that manifest as hallucinations are thought to result from the misattribution of the source of patients' inner thoughts/speech as external voices.

We used magnetoencephalography (MEG) to assess agency during RM and SM tasks. In healthy control participants (HCs) during SM, the auditory cortical (A1) response is smaller while speaking (speak condition) compared with listening to the same speech (listen condition). This is known as the speaking-induced suppression (SIS) M100 response, which is measured using MEG 100 ms after speech onset.

During RM, patients with SZ (N = 30) showed impairments in both self-agency (identification of self-generated information) and external agency (identification of externally produced information) compared with HCs (N = 30). During SM, patients with SZ failed to enhance M100 responses during the listen condition, resulting in weakened SIS-that is, smaller M100 listen minus speak differences. Weakened SIS predicted worsening hallucination severity.

Patients with SZ showed degraded neural M100 responses in A1 during the listen condition, which drove impaired SIS (i.e., smaller M100 listen minus speak differences). Impaired SIS indicated degraded auditory sensory predictions, making it more likely for patients with SZ to misattribute the source of inner thoughts/speech as externally derived, giving rise to disruptions in agency during RM and more severe hallucinations.