High-frequency neural oscillations and visual processing deficits in schizophrenia

Abstract

Visual information is fundamental to how we understand our environment, make predictions, and interact with others. Recent research has underscored the importance of visuo-perceptual dysfunctions for cognitive deficits and pathophysiological processes in schizophrenia. In the current paper, we review evidence for the relevance of high frequency (beta/gamma) oscillations towards visuo-perceptual dysfunctions in schizophrenia. In the first part of the paper, we examine the relationship between beta/gamma band oscillations and visual processing during normal brain functioning. We then summarize EEG/MEG-studies which demonstrate reduced amplitude and synchrony of high-frequency activity during visual stimulation in schizophrenia. In the final part of the paper, we identify neurobiological correlates as well as offer perspectives for future research to stimulate further inquiry into the role of high-frequency oscillations in visual processing impairments in the disorder.

Keywords: evoked and induced neural activity; high-frequency neural oscillations; neural synchrony; neurobiology; schizophrenia; visual perception.

Figure 1

(A) Visual steady-state potentials (SSP) in patients with schizophrenia and controls: Average signal power for the two groups during resting state and photic stimulation at different frequencies recorded at Oz. (Legend: HC-PS, healthy control subjects during Photic Stimulation; SZ-PS, Schizophrenia subjects during Photic Stimulation; HC-BL, Healthy control subjects during Baseline; SZ-BL, Schizophrenia subjects during Baseline). Error bars indicate standard error. Significant differences between groups on ANOVAs are marked with “^*” for the photic stimulation condition and “x” for the resting condition. Adapted from Krishnan et al. (2005). (B) Sensory evoked oscillations during a visual oddball task in patients with schizophrenia. The colored scale indicates the phase locking factor (PLF) of oscillations in the 20–100 Hz frequency range in the occipital cortex (electrode O1) for healthy controls and patients with schizophrenia. Control participants show an increase in phase locking for gamma oscillations ~100 ms after stimulus presentation. However, this is significantly smaller in patients with schizophrenia, indicating a dysfunction in early sensory processes. Adapted from Spencer et al. (2008). (C) High-Frequency Oscillations during Perceptual Organization in ScZ. Left-Panel: Time-frequency representations and topographies of gamma-band spectral power of MEG-data in response to Mooney faces for controls (top) and chronic ScZ patients (bottom). The gamma-band signal is expressed as relative power change in the post-stimulus time window compared to baseline, averaged across all channels. The topographies (middle panels) display the results for a non-Parametric ANOVA indicating the main effects of group for both low (top) and high (bottom) gamma-band oscillations at the sensor level. Intensity of red indexes increased activity in controls while stronger blue intensities suggest increased gamma-band power in schizophrenia patients relative to controls. The topographies depict corrected t-values and the channels that form a statistically significant cluster are indicated (^*p < 0.001; ^xp < 0.05). Right panel: Correlation between high gamma-band power and disorganization. The scatter-plot shows the relationship between high (60–120 Hz) gamma-band power in the 50–350 ms time window over positive channels and the disorganization component of the positive and negative syndrome scale. Adapted from Grützner et al. (2013).

Figure 2

(A) Left: visually induced gamma-band activity in MEG data in a monozygotic (MZ) and a dyzygotic (DZ) twin pair. Time-frequency representations (TFRs) of activity in the gamma-band range relative to prestimulus baseline levels in two twins of a MZ pair, averaged across 74 parieto-occipital MEG sensors. Time 0s denotes stimulus onset. Right: correlation between gamma-peak frequencies in MZ twins [A] and DZ twins [B]. Each data point represents the peak frequency of one twin vs. that of his or her co-twin (random axis assignment). Slope values are estimated by random permutations of x and y values. The data suggest a heritability of the gamma-band frequency of 91%. Adapted from van Pelt et al. (2012). (B) Evoked oscillatory activity in schizophrenia patients and their unaffected co-twins. EEG time-frequency analyses of evoked gamma-band power during an auditory oddball task for responses to the standard stimuli at electrode Cz in healthy twins, MZ twins concordant with schizophrenia, MZ twins discordant with schizophrenia, and unaffected co-twin members. Impaired evoked gamma-band power was significantly associated with schizophrenia and unaffected co-twins exhibited significantly reduced 30–60 Hz power as well-compared with controls, highlighting the genetic contribution toward impairments in high-frequency oscillations in the disorder. Adapted from Hall et al. (2011) by permission of Oxford University Press.