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 in | Biological psychiatry : cognitive neuroscience and neuroimaging Vol. 6; no. 12; pp. 1157 - 1164 |
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| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.12.2021
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2451-9022 2451-9030 2451-9030 |
| DOI | 10.1016/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. |
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| 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 |
| AuthorAffiliation_xml | – name: 4 Helen Wills Neuroscience Institute, University of California at Berkeley, Berkeley, CA, USA – name: 3 Department of Psychology, University of California at Berkeley, Berkeley, CA, USA – name: 5 Department of Psychiatry and Behavioral Sciences, University of California at Davis, Davis, CA, USA – name: 2 Department of Psychology, University of California at Davis, Davis, CA, USA – name: 1 Center for Neuroscience, University of California at Davis, Davis, CA, USA |
| Author_xml | – sequence: 1 givenname: Yicong orcidid: 0000-0003-4925-6069 surname: Zheng fullname: Zheng, Yicong organization: Center for Neuroscience, University of California, Davis, Davis, California – sequence: 2 givenname: Xiaonan L. surname: Liu fullname: Liu, Xiaonan L. organization: Center for Neuroscience, University of California, Davis, Davis, California – sequence: 3 givenname: Liang-Tien surname: Hsieh fullname: Hsieh, Liang-Tien organization: Department of Psychology, University of California, Berkeley, Berkeley, California – sequence: 4 givenname: Mitzi surname: Hurtado fullname: Hurtado, Mitzi organization: Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, California – sequence: 5 givenname: Yan surname: Wang fullname: Wang, Yan organization: Department of Psychology, University of California, Davis, Davis, California – sequence: 6 givenname: Tara A. surname: Niendam fullname: Niendam, Tara A. organization: Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, California – sequence: 7 givenname: Cameron S. surname: Carter fullname: Carter, Cameron S. organization: Department of Psychology, University of California, Davis, Davis, California – sequence: 8 givenname: Charan surname: Ranganath fullname: Ranganath, Charan organization: Center for Neuroscience, University of California, Davis, Davis, California – sequence: 9 givenname: J. Daniel surname: Ragland fullname: Ragland, J. Daniel email: jdragland@ucdavis.edu organization: Department of Psychiatry and Behavioral Sciences, University of California, Davis, Davis, California |
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| Keywords | Neural oscillations Alpha Electrophysiology Schizophrenia Episodic memory Beta |
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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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