Disrupted auditory N1, theta power and coherence suppression to willed speech in people with schizophrenia

Abstract

The phenomenon of sensory self-suppression - also known as sensory attenuation - occurs when a person generates a perceptible stimulus (such as a sound) by performing an action (such as speaking). The sensorimotor control system is thought to actively predict and then suppress the vocal sound in the course of speaking, resulting in lowered cortical responsiveness when speaking than when passively listening to an identical sound. It has been hypothesized that auditory hallucinations in schizophrenia result from a reduction in self-suppression due to a disruption of predictive mechanisms required to anticipate and suppress a specific, self-generated sound. It has further been hypothesized that this suppression is evident primarily in theta band activity. Fifty-one people, half of whom had a diagnosis of schizophrenia, were asked to repeatedly utter a single syllable, which was played back to them concurrently over headphones while EEG was continuously recorded. In other conditions, recordings of the same spoken syllables were played back to participants while they passively listened, or were played back with their onsets preceded by a visual cue. All participants experienced these conditions with their voice artificially shifted in pitch and also with their unaltered voice. Suppression was measured using event-related potentials (N1 component), theta phase coherence and power. We found that suppression was generally reduced on all metrics in the patient sample, and when voice alteration was applied. We additionally observed reduced theta coherence and power in the patient sample across all conditions. Visual cueing affected theta coherence only. In aggregate, the results suggest that sensory self-suppression of theta power and coherence is disrupted in schizophrenia.

Keywords: EEG; Electrophysiology; Psychosis; Schizophrenia; Sensorimotor control; Sensory perception.

Fig. 1

Event-related potentials across conditions and groups, measured in microvolts. The upper row shows the performance of the control sample, and the lower row shows the performance of the patient sample (labelled SZ). The left-hand column shows performance on the unaltered voice trials, the right-hand column shows performance on the pitch-shifted trials. The grey shaded area shows the time window used for N1 quantification. Each coloured line depicts mean performance, and the shaded area represents the standard error of the mean.

Fig. 2

Mean baseline-corrected theta power across conditions and groups, measured as signal-to-noise-ratio (SNR) in decibels averaged across all 64 scalp channels. The upper row shows the performance of the control sample, and the lower row shows the performance of the patient sample (labelled SZ). The left-hand column shows performance on the unaltered voice trials, the right-hand column shows performance on the pitch-shifted trials. The grey shaded area shows the time window used for theta power quantification. Each coloured line depicts mean performance, and the shaded area represents the standard error of the mean.

Fig. 3

Intertrial coherence across conditions and groups. The upper, middle and lower sections depict intertrial coherence in the Talk, Listen and Cued conditions, respectively. Within each section the left-hand images depict coherence during the unaltered voice trials, and the right hand images show coherence during pitch-shifted trials. Within each section, the upper row depicts the performance of the control group, and the lower row depicts performance of the patient group (labelled SZ). Time frequency plots show coherence distributed across time (-700 to 700 ms) and frequency (2–50 Hz), and averaged across all 64 scalp channels. The topoplots show mean coherence across at each channel, averaged across theta (4–7 Hz) and between 60 and 160 ms after stimulus onset. All panels used the same colour axis, which refers to the degree to which measured amplitudes are phase aligned across trials (0–1).

Fig. 4

Mean N1 magnitudes (Panel A), inter-trial phase coherence (Panel B) and theta power (Panel C). Mean N1 magnitude was obtained from 9 channels centered on FCz, between 85 and 135 ms post-stimulus onset. Phase coherence was quantified between 4 and 7 Hz, averaged across all scalp channels, between 60 and 160 ms after stimulus onset. Theta power was taken over a broad window (0–250 ms post onset), averaged across all channels, after a narrow bandpass filter was applied (see text for details). Error bars indicated standard error of the mean.