Auditory cortex responsiveness during talking and listening: early illness schizophrenia and patients at clinical high-risk for psychosis

Abstract

Objective: The corollary discharge mechanism is theorized to dampen sensations resulting from our own actions and distinguish them from environmental events. Deficits in this mechanism in schizophrenia may contribute to misperceptions of self-generated sensations as originating from external stimuli. We previously found attenuated speech-related suppression of auditory cortex in chronic patients, consistent with such deficits. Whether this abnormality precedes psychosis onset, emerges early in the illness, and/or progressively worsens with illness chronicity, is unknown.

Methods: Event-related potentials (ERPs) were recorded from schizophrenia patients (SZ; n = 75) and age-matched healthy controls (HC; n = 77). A subsample of early illness schizophrenia patients (ESZ; n = 39) was compared with patients at clinical high-risk for psychosis (CHR; n = 35) and to a subgroup of age-matched HC (n = 36) during a Talk-Listen paradigm. The N1 ERP component was elicited by vocalizations as subjects talked (Talk) and heard them played back (Listen).

Results: As shown previously, SZ showed attenuated speech-related N1 suppression relative to HC. This was also observed in ESZ. N1 suppression values in CHR were intermediate to HC and ESZ and not statistically distinguishable from either comparison group. Age-corrected N1 Talk-Listen difference z scores were not correlated with illness duration in the full SZ sample.

Conclusions: Putative dysfunction of the corollary discharge mechanism during speech is evident early in the illness and is stable over its course. The intermediate effects in CHR patients may reflect the heterogeneity of this group, requiring longitudinal follow-up data to address if speech-related N1 suppression abnormalities are a risk marker for conversion to psychosis.

Fig. 1.

Grand average event-related potential (ERP) waveforms for Talk and Listen conditions. ERP waveforms for Talk and Listen conditions show the N1 component during the Talk (dotted line) and Listen (solid line) conditions. (a) The N1 amplitude during Talk is reduced relative to Listen in healthy controls. (b) This effect is attenuated in the schizophrenia patients. (c) The N1 amplitude during Talk is reduced relative to Listen in a healthy control group age matched to (d) clinical high-risk, and (e) early illness schizophrenia patients.

Fig. 2.

N1 amplitude (mean and SE) for Talk and Listen conditions. Line graphs show group means and SEs for N1 amplitude assessed during Talk and Listen conditions. (a) Normal speech-related N1 suppression is shown in healthy controls (HC; solid line; Talk: M = −1.1, SE = 0.4; Listen: M = −4.3, SE = 0.3), while the flatter slope indicates reduced N1 suppression in schizophrenia patients (SZ; dashed line; Talk: M = −1.7, SE = 0.6; Listen: M = −2.9, SE = 0.2). In (b), clinical high-risk patients (CHR; dotted line; Talk: M = −2.4, SE = 0.6; Listen: M = −3.7, SE = 0.4) show a slope that is intermediate to age-matched healthy controls (HC; solid line; Talk: M = −1.1, SE = 0.7; Listen: M = −4.3, SE = 0.6) and early illness schizophrenia patients (ESZ; dashed line; Talk: M = −2.5, SE = 0.9; Listen: M = −3.0, SE = 0.3). All amplitude values are given in microvolts (μV).

Fig. 3.

N1 Talk-Listen difference scores. Mean (±SE) N1 Talk-Listen difference scores (in microvolts) for the age-matched healthy control group, clinical high-risk, and early illness schizophrenia patients.