Positive and Negative Symptoms in Schizophrenia Relate to Distinct Oscillatory Signatures of Sensory Gating

Abstract

Oscillatory activity in neural populations and temporal synchronization within these populations are important mechanisms contributing to perception and cognition. In schizophrenia, perception and cognition are impaired. Aberrant gating of irrelevant sensory information, which has been related to altered oscillatory neural activity, presumably contributes to these impairments. However, the link between schizophrenia symptoms and sensory gating deficits, as reflected in oscillatory activity, is not clear. In this electroencephalography study, we used a paired-stimulus paradigm to investigate frequency-resolved oscillatory activity in 22 schizophrenia patients and 22 healthy controls. We found sensory gating deficits in patients compared to controls, as reflected in reduced gamma-band power and alpha-band phase synchrony difference between the first and the second auditory stimulus. We correlated these markers of neural activity with a five-factor model of the Positive and Negative Syndrome Scale. Gamma-band power sensory gating was positively correlated with positive symptoms. Moreover, alpha-band phase synchrony sensory gating was negatively correlated with negative symptoms. A cluster analysis revealed three schizophrenia phenotypes, characterized by (i) aberrant gamma-band power and high positive symptoms, (ii) aberrant alpha-band phase synchrony, low positive, and low negative symptom scores or (iii) by intact sensory gating and high negative symptoms. Our study demonstrates that aberrant neural synchronization, as reflected in gamma-band power and alpha-band phase synchrony, relates to the schizophrenia psychopathology. Different schizophrenia phenotypes express distinct levels of positive and negative symptoms as well as varying degrees of aberrant oscillatory neural activity. Identifying the individual phenotype might improve therapeutic interventions in schizophrenia.

Beta/Gamma Oscillations and Event-Related Potentials Indicate Aberrant Multisensory Processing in Schizophrenia

“…For example, Leicht et al (2010) investigated auditory evoked gamma band oscillations in SCZ and found a significant reduction of power in SCZ compared to HC around 50 ms after stimulus presentation. Keil et al (2016) recently replicated this effect. Another study by Lenz et al (2011) examined evoked gamma band responses in SCZ during an auditory oddball-paradigm and reported diminished responses to standard and deviant stimuli in SCZ around 40 to 90 ms after stimulus onset.…”

“…It might be that the absence of significant main effects between groups relates to a lack of statistical power. Indeed, previous studies have reported diminished evoked beta band (13–30 Hz) and gamma band (>30 Hz) oscillations in SCZ (Gallinat et al, 2004; Leicht et al, 2010, 2015; Lenz et al, 2011; Keil et al, 2016). For example, Leicht et al (2010) investigated auditory evoked gamma band oscillations in SCZ and found a significant reduction of power in SCZ compared to HC around 50 ms after stimulus presentation.…”

“…Research has stated that primary cognitive disturbances in SCZ cause an inability to sufficiently filter and process sensory information, leading to disconnection of information and disrupted binding (McGhie and Chapman, 1961; Shakow, 1963; Freedman et al, 1991; Vlcek et al, 2014). Furthermore, electrophysiological studies have suggested that aberrant neural oscillations play a role for cognitive deficits in SCZ (Andreasen, 2000; Lee et al, 2003; Lisman, 2012; Pittman-Polletta et al, 2015; Senkowski and Gallinat, 2015; Uhlhaas and Singer, 2015; Keil et al, 2016). Thus far, sensory processing deficits have been most consistently observed in studies using setups with unisensory stimulation.…”

Spatiotemporal processing of somatosensory stimuli in schizotypy

“…Indeed, Heed and colleagues2 recently suggested that oscillatory brain activity seems to be optimally suited for implementing the transformation and integration of multiple coordinates. Interestingly, there is now plenty of evidence associating altered spontaneous brain oscillations with risk for psychosis6061626364, as well as abnormal multisensory perception in schizophrenia6566. Future research is warranted to determine a direct relationship between abnormal touch remapping and altered oscillatory brain activity in schizotypy.…”

Consistency of abnormal sensory gating in first‐admission and chronic schizophrenia across quantification methods

“…Thoma et al () and Smith et al () reported specific relationships between M50 gating and symptoms in schizophrenia, and others did so for P50 gating and symptoms (Arnfred & Chen, ; Erwin, Turetsky, Moberg, Gur, & Gur, ; Louchart‐de la Chapelle et al, ; Ringel et al, ; Yee, Nuechterlein, Morris, & White, ). In spectral analysis of a traditional EEG sensory gating paradigm, Keil and colleagues (Keil, Roa Romero, Balz, Henjes, & Senkowski, ) reported that SZ had less gamma‐band power reduction from S1 to S2, which correlated with Positive and Negative Syndrome Scale (PANSS) positive symptoms, and less alpha‐band phase coherence reduction from S1 to S2, which correlated with PANSS negative symptoms. These two spectral measures of gating were in turn correlated.…”