The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia

Abstract

Neural oscillations and their synchronization may represent a versatile signal to realize flexible communication within and between cortical areas. By now, there is extensive evidence to suggest that cognitive functions depending on coordination of distributed neural responses, such as perceptual grouping, attention-dependent stimulus selection, subsystem integration, working memory, and consciousness, are associated with synchronized oscillatory activity in the theta-, alpha-, beta-, and gamma-band, suggesting a functional mechanism of neural oscillations in cortical networks. In addition to their role in normal brain functioning, there is increasing evidence that altered oscillatory activity may be associated with certain neuropsychiatric disorders, such as schizophrenia, that involve dysfunctional cognition and behavior. In the following article, we aim to summarize the evidence on the role of neural oscillations during normal brain functioning and their relationship to cognitive processes. In the second part, we review research that has examined oscillatory activity during cognitive and behavioral tasks in schizophrenia. These studies suggest that schizophrenia involves abnormal oscillations and synchrony that are related to cognitive dysfunctions and some of the symptoms of the disorder. Perspectives for future research will be discussed in relationship to methodological issues, the utility of neural oscillations as a biomarker, and the neurodevelopmental hypothesis of schizophrenia.

Fig. 1.

Synchronous Gamma Oscillations and Perceptual Binding. Responses are recorded for a pair of multiunit (MUA) activity with nonoverlapping receptive fields in primary visual cortex of an anesthetized cat. In the 2 different visual stimulation conditions, the stimuli consisted either of a single long moving bar (A) or of 2 small bars moving in different directions (C). In both conditions, the receptive fields were stimulated near optimally and simultaneously, and consequently, no changes in neurons' firing rates were observed (results not shown). In contrast, neuronal synchronization between the 2 MUAs changed strongly, as estimated by the cross-correlation histograms (CCHs) in (B) and (D). The high center peak and the good fit of a Gabor function in (B) indicate that the stimulus in (A) evoked strong neuronal synchrony, while the flat CCH in (D) indicates lack of synchronization between the responses to stimuli in (C).

Fig. 2.

Neural Synchrony During Gestalt Perception in Schizophrenia. Group average of phase synchrony for all electrodes and for correct trials during a Gestalt perception task in controls (A). Phase synchrony during Gestalt perception in controls exhibited 2 maxima over an average frequency range of 20–30 Hz (A). The increase in phase synchrony between 200 and 300 ms has been related to the construction of coherent object representations, whereas the second peak indexes the preparation and execution of the motor response. In patients with schizophrenia (B), the onset of the first peak in the face condition was delayed and occurred between 350 and 400 ms in the frequency range of 20–25 Hz. In addition, a second, weaker peak was found around 600 ms. Compared with controls, the reduction in phase synchrony in patients with schizophrenia in the frequency range of 20–30 Hz was significant (frequency range: 20–30 Hz, time interval: 200–280 ms, t(36) = 2.96, P = .005). (C) This shows the topography of phase synchrony between 20 and 30 Hz. Synchrony between pairs of electrodes is indicated by connecting lines, which were drawn only if the synchrony value is beyond a 2-tailed probability of P < .0005. Differences between groups are displayed in the bottom row. Red lines indicate a decrease in synchrony in schizophrenia patients compared with controls. Green lines indicate increase in synchrony for patients with schizophrenia relative to controls. The decrease in phase synchrony between 200 and 300 ms indexes a deficit in the long-range synchronization during Gestalt perception in schizophrenia. Adapted with permission from Uhlhaas et al. Copyright 2006 Society for Neuroscience.