Disrupted Modulation of Alpha and Low Beta Oscillations Mediates Temporal Sequence Memory Deficits in People With Schizophrenia

People with schizophrenia (SZ) exhibit impaired episodic memory when relating objects to each other in time and space. Empirical studies and computational models suggest that low-frequency neural oscillations may be a mechanism by which the brain keeps track of temporal relationships during encoding...

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Published inBiological psychiatry : cognitive neuroscience and neuroimaging Vol. 6; no. 12; pp. 1157 - 1164
Main Authors Zheng, Yicong, Liu, Xiaonan L., Hsieh, Liang-Tien, Hurtado, Mitzi, Wang, Yan, Niendam, Tara A., Carter, Cameron S., Ranganath, Charan, Ragland, J. Daniel
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.12.2021
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ISSN2451-9022
2451-9030
2451-9030
DOI10.1016/j.bpsc.2021.04.002

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Abstract People with schizophrenia (SZ) exhibit impaired episodic memory when relating objects to each other in time and space. Empirical studies and computational models suggest that low-frequency neural oscillations may be a mechanism by which the brain keeps track of temporal relationships during encoding and retrieval, with modulation of oscillatory power as sequences are learned. It is unclear whether sequence memory deficits in SZ are associated with altered neural oscillations. Using electroencephalography, this study examined neural oscillations in 51 healthy control subjects and 37 people with SZ during a temporal sequence learning task. Multiple 5-object picture sequences were presented across 4 study-test blocks in either fixed or random order. Participants answered semantic questions for each object (e.g., living/nonliving), and sequence memory was operationalized as faster responses for fixed versus random sequences. Differences in oscillatory power between fixed versus random sequences provided a neural index of temporal sequence memory. Although both groups showed reaction time differences in late blocks (blocks 3 and 4), this evidence of sequence memory was reduced in people with SZ relative to healthy control subjects. Decreases in globally distributed prestimulus alpha (8–12 Hz) and beta 1 (13–20 Hz) power for fixed versus random sequences in late blocks were also attenuated in people with SZ relative to healthy control subjects. Moreover, changes in oscillatory power predicted individual reaction time differences and fully mediated the relationship between group and sequence memory. Disrupted modulation of alpha and beta 1 electroencephalography oscillations is a candidate mechanism of temporal sequence memory deficits in people with SZ.
AbstractList People with schizophrenia (SZ) exhibit impaired episodic memory when relating objects to each other in time and space. Empirical studies and computational models suggest that low-frequency neural oscillations may be a mechanism by which the brain keeps track of temporal relationships during encoding and retrieval, with modulation of oscillatory power as sequences are learned. It is unclear whether sequence memory deficits in SZ are associated with altered neural oscillations. Using electroencephalography, this study examined neural oscillations in 51 healthy control subjects and 37 people with SZ during a temporal sequence learning task. Multiple 5-object picture sequences were presented across 4 study-test blocks in either fixed or random order. Participants answered semantic questions for each object (e.g., living/nonliving), and sequence memory was operationalized as faster responses for fixed versus random sequences. Differences in oscillatory power between fixed versus random sequences provided a neural index of temporal sequence memory. Although both groups showed reaction time differences in late blocks (blocks 3 and 4), this evidence of sequence memory was reduced in people with SZ relative to healthy control subjects. Decreases in globally distributed prestimulus alpha (8-12 Hz) and beta 1 (13-20 Hz) power for fixed versus random sequences in late blocks were also attenuated in people with SZ relative to healthy control subjects. Moreover, changes in oscillatory power predicted individual reaction time differences and fully mediated the relationship between group and sequence memory. Disrupted modulation of alpha and beta 1 electroencephalography oscillations is a candidate mechanism of temporal sequence memory deficits in people with SZ.
People with schizophrenia (SZ) exhibit impaired episodic memory when relating objects to each other in time and space. Empirical studies and computational models suggest that low-frequency neural oscillations may be a mechanism by which the brain keeps track of temporal relationships during encoding and retrieval, with modulation of oscillatory power as sequences are learned. It is unclear whether sequence memory deficits in SZ are associated with altered neural oscillations.BACKGROUNDPeople with schizophrenia (SZ) exhibit impaired episodic memory when relating objects to each other in time and space. Empirical studies and computational models suggest that low-frequency neural oscillations may be a mechanism by which the brain keeps track of temporal relationships during encoding and retrieval, with modulation of oscillatory power as sequences are learned. It is unclear whether sequence memory deficits in SZ are associated with altered neural oscillations.Using electroencephalography, this study examined neural oscillations in 51 healthy control subjects and 37 people with SZ during a temporal sequence learning task. Multiple 5-object picture sequences were presented across 4 study-test blocks in either fixed or random order. Participants answered semantic questions for each object (e.g., living/nonliving), and sequence memory was operationalized as faster responses for fixed versus random sequences. Differences in oscillatory power between fixed versus random sequences provided a neural index of temporal sequence memory.METHODSUsing electroencephalography, this study examined neural oscillations in 51 healthy control subjects and 37 people with SZ during a temporal sequence learning task. Multiple 5-object picture sequences were presented across 4 study-test blocks in either fixed or random order. Participants answered semantic questions for each object (e.g., living/nonliving), and sequence memory was operationalized as faster responses for fixed versus random sequences. Differences in oscillatory power between fixed versus random sequences provided a neural index of temporal sequence memory.Although both groups showed reaction time differences in late blocks (blocks 3 and 4), this evidence of sequence memory was reduced in people with SZ relative to healthy control subjects. Decreases in globally distributed prestimulus alpha (8-12 Hz) and beta 1 (13-20 Hz) power for fixed versus random sequences in late blocks were also attenuated in people with SZ relative to healthy control subjects. Moreover, changes in oscillatory power predicted individual reaction time differences and fully mediated the relationship between group and sequence memory.RESULTSAlthough both groups showed reaction time differences in late blocks (blocks 3 and 4), this evidence of sequence memory was reduced in people with SZ relative to healthy control subjects. Decreases in globally distributed prestimulus alpha (8-12 Hz) and beta 1 (13-20 Hz) power for fixed versus random sequences in late blocks were also attenuated in people with SZ relative to healthy control subjects. Moreover, changes in oscillatory power predicted individual reaction time differences and fully mediated the relationship between group and sequence memory.Disrupted modulation of alpha and beta 1 electroencephalography oscillations is a candidate mechanism of temporal sequence memory deficits in people with SZ.CONCLUSIONSDisrupted modulation of alpha and beta 1 electroencephalography oscillations is a candidate mechanism of temporal sequence memory deficits in people with SZ.
Author Liu, Xiaonan L.
Carter, Cameron S.
Zheng, Yicong
Ranganath, Charan
Hsieh, Liang-Tien
Hurtado, Mitzi
Niendam, Tara A.
Ragland, J. Daniel
Wang, Yan
AuthorAffiliation 2 Department of Psychology, University of California at Davis, Davis, CA, USA
3 Department of Psychology, University of California at Berkeley, Berkeley, CA, USA
5 Department of Psychiatry and Behavioral Sciences, University of California at Davis, Davis, CA, USA
1 Center for Neuroscience, University of California at Davis, Davis, CA, USA
4 Helen Wills Neuroscience Institute, University of California at Berkeley, Berkeley, CA, USA
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Snippet People with schizophrenia (SZ) exhibit impaired episodic memory when relating objects to each other in time and space. Empirical studies and computational...
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SubjectTerms Alpha
Beta
Brain - physiology
Electroencephalography
Electrophysiology
Episodic memory
Humans
Memory Disorders - etiology
Neural oscillations
Reaction Time
Schizophrenia
Schizophrenia - complications
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Title Disrupted Modulation of Alpha and Low Beta Oscillations Mediates Temporal Sequence Memory Deficits in People With Schizophrenia
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