Neural synchrony indexes disordered perception and cognition in schizophrenia

Abstract

Current views of schizophrenia suggest that it results from abnormalities in neural circuitry, but empirical evidence in the millisecond range of neural activity has been difficult to obtain. In pursuit of relevant evidence, we previously demonstrated that schizophrenia is associated with abnormal patterns of stimulus-evoked phaselocking of the electroencephalogram in the gamma band (30-100 Hz). These patterns may reflect impairments in neural assemblies, which have been proposed to use gamma-band oscillations as a mechanism for synchronization. Here, we report the unique finding that, in both healthy controls and schizophrenia patients, visual Gestalt stimuli elicit a gamma-band oscillation that is phase-locked to reaction time and hence may reflect processes leading to conscious perception of the stimuli. However, the frequency of this oscillation is lower in schizophrenics than in healthy individuals. This finding suggests that, although synchronization must occur for perception of the Gestalt, it occurs at a lower frequency because of a reduced capability of neural networks to support high-frequency synchronization in the brain of schizophrenics. Furthermore, the degree of phase locking of this oscillation is correlated with visual hallucinations, thought disorder, and disorganization in the schizophrenia patients. These data provide support for linking dysfunctional neural circuitry and the core symptoms of schizophrenia.

Fig. 1.

Gestalt perception task. (A) Stimuli. The ratio of inducer radius to square length is 0.2. (B) RT and error data (bars indicate SE). (C) Grand average VEPs (Upper) and stimulus-locked phase-locking values (Lower; 34.1–40.5 Hz) at electrode O1. Arrows indicate the latency of the response-locked oscillation in the square condition relative to stimulus onset for each group.

Fig. 2.

Grand average stimulus-locked time-frequency maps of phase-locking values for NC and SZ. The left parietal (P3) and occipital (O1) sites are shown. Color scales indicate phase-locking values. The frequency and stimulus-locked latency of the response-locked oscillations are indicated by the arrows.

Fig. 3.

Grand average response-locked phase-locking maps, as in Fig. 2. The RT on each trial is shifted to 0 ms.

Fig. 4.

SZ symptom analyses. (A) Correlations between symptom scales (y axis) and the occipital response-locked effect (x axis) for SZ. (B) VEPs for the VH and NVH patients at O1.