Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum

Cognitive deficits in people with schizophrenia are among the hardest to treat and strongly predict functional outcome. The ability to maintain sensory precepts in memory over a short delay is impacted early in the progression of schizophrenia and has been linked to reliable neurophysiological marke...

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Main Authors: Brian A. Coffman, Gretchen Haas, Carl Olson, Raymond Cho, Avniel Singh Ghuman, Dean F. Salisbury
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-08-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpsyt.2020.00743/full
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spelling doaj-5a59392ba5fb4727a79e1fd6161ccb522020-11-25T02:55:03ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402020-08-011110.3389/fpsyt.2020.00743549845Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia SpectrumBrian A. Coffman0Gretchen Haas1Carl Olson2Raymond Cho3Raymond Cho4Avniel Singh Ghuman5Dean F. Salisbury6Clinical Neurophysiology Research Laboratory, Western Psychiatric Hospital of UPMC, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United StatesWestern Psychiatric Hospital of UPMC, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United StatesCenter for Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, PA, United StatesWestern Psychiatric Hospital of UPMC, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United StatesDepartment of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, United StatesLaboratory of Cognitive Neurodynamics, Department of Neurosurgery, Presbyterian Hospital, University of Pittsburgh School of Medicine, Pittsburgh, PA, United StatesClinical Neurophysiology Research Laboratory, Western Psychiatric Hospital of UPMC, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United StatesCognitive deficits in people with schizophrenia are among the hardest to treat and strongly predict functional outcome. The ability to maintain sensory precepts in memory over a short delay is impacted early in the progression of schizophrenia and has been linked to reliable neurophysiological markers. Yet, little is known about the mechanisms of these deficits. Here, we investigated possible neurophysiological mechanisms of impaired visual short-term memory (vSTM, aka working memory maintenance) in the first-episode schizophrenia spectrum (FESz) using magnetoencephalography (MEG). Twenty-eight FESz and 25 matched controls performed a lateralized change detection task where they were cued to selectively attend and remember colors of circles presented in either the left or right peripheral visual field over a 1 s delay. Contralateral alpha suppression (CAS) during the delay period was used to assess selective attention to cued visual hemifields held in vSTM. Delay-period CAS was compared between FESz and controls and between trials presenting one vs three items per visual hemifield. CAS in dorsal visual cortex was reduced in FESz compared to controls in high-load trials, but not low-load trials. Group differences in CAS were found beginning 100 ms after the disappearance of the memory set, suggesting deficits were not due to the initial deployment of attention to the cued visual hemifield prior to stimulus presentation. CAS was not greater for high-load vs low-load trials in FESz subjects, although this effect was prominent in controls. Further, lateralized gamma (34–40 Hz) power emerged in dorsal visual cortex prior to the onset of CAS in controls but not FESz. Gamma power in this cluster differed between groups at both high and low load. CAS deficits observed in FESz were correlated with change detection accuracy, working memory function, estimated IQ, and negative symptoms. Our results implicate deficits in CAS in trials requiring broad, but not narrow, focus of attention to spatially distributed objects maintained in vSTM in FESz, possibly due to reduced ability to broadly distribute visuospatial attention (alpha) or disruption of object-location binding (gamma) during encoding/consolidation. This early pathophysiology may shed light upon mechanisms of emerging working memory deficits that are intrinsic to schizophrenia.https://www.frontiersin.org/article/10.3389/fpsyt.2020.00743/fullfirst-episode schizophreniamagnetoencephalographyvisual short-term memoryworking memoryalphagamma
collection DOAJ
language English
format Article
sources DOAJ
author Brian A. Coffman
Gretchen Haas
Carl Olson
Raymond Cho
Raymond Cho
Avniel Singh Ghuman
Dean F. Salisbury
spellingShingle Brian A. Coffman
Gretchen Haas
Carl Olson
Raymond Cho
Raymond Cho
Avniel Singh Ghuman
Dean F. Salisbury
Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum
Frontiers in Psychiatry
first-episode schizophrenia
magnetoencephalography
visual short-term memory
working memory
alpha
gamma
author_facet Brian A. Coffman
Gretchen Haas
Carl Olson
Raymond Cho
Raymond Cho
Avniel Singh Ghuman
Dean F. Salisbury
author_sort Brian A. Coffman
title Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum
title_short Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum
title_full Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum
title_fullStr Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum
title_full_unstemmed Reduced Dorsal Visual Oscillatory Activity During Working Memory Maintenance in the First-Episode Schizophrenia Spectrum
title_sort reduced dorsal visual oscillatory activity during working memory maintenance in the first-episode schizophrenia spectrum
publisher Frontiers Media S.A.
series Frontiers in Psychiatry
issn 1664-0640
publishDate 2020-08-01
description Cognitive deficits in people with schizophrenia are among the hardest to treat and strongly predict functional outcome. The ability to maintain sensory precepts in memory over a short delay is impacted early in the progression of schizophrenia and has been linked to reliable neurophysiological markers. Yet, little is known about the mechanisms of these deficits. Here, we investigated possible neurophysiological mechanisms of impaired visual short-term memory (vSTM, aka working memory maintenance) in the first-episode schizophrenia spectrum (FESz) using magnetoencephalography (MEG). Twenty-eight FESz and 25 matched controls performed a lateralized change detection task where they were cued to selectively attend and remember colors of circles presented in either the left or right peripheral visual field over a 1 s delay. Contralateral alpha suppression (CAS) during the delay period was used to assess selective attention to cued visual hemifields held in vSTM. Delay-period CAS was compared between FESz and controls and between trials presenting one vs three items per visual hemifield. CAS in dorsal visual cortex was reduced in FESz compared to controls in high-load trials, but not low-load trials. Group differences in CAS were found beginning 100 ms after the disappearance of the memory set, suggesting deficits were not due to the initial deployment of attention to the cued visual hemifield prior to stimulus presentation. CAS was not greater for high-load vs low-load trials in FESz subjects, although this effect was prominent in controls. Further, lateralized gamma (34–40 Hz) power emerged in dorsal visual cortex prior to the onset of CAS in controls but not FESz. Gamma power in this cluster differed between groups at both high and low load. CAS deficits observed in FESz were correlated with change detection accuracy, working memory function, estimated IQ, and negative symptoms. Our results implicate deficits in CAS in trials requiring broad, but not narrow, focus of attention to spatially distributed objects maintained in vSTM in FESz, possibly due to reduced ability to broadly distribute visuospatial attention (alpha) or disruption of object-location binding (gamma) during encoding/consolidation. This early pathophysiology may shed light upon mechanisms of emerging working memory deficits that are intrinsic to schizophrenia.
topic first-episode schizophrenia
magnetoencephalography
visual short-term memory
working memory
alpha
gamma
url https://www.frontiersin.org/article/10.3389/fpsyt.2020.00743/full
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