Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation
To form an episodic memory, we must first process a vast amount of sensory information about the to-be-encoded event and then bind these sensory representations together to form a coherent memory trace. While these two cognitive capabilities are thought to have two distinct neural origins, with neoc...
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Format: | Article |
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Elsevier
2021-11-01
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Series: | NeuroImage |
Online Access: | http://www.sciencedirect.com/science/article/pii/S105381192100728X |
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author | Benjamin J. Griffiths María Carmen Martín-Buro Bernhard P. Staresina Simon Hanslmayr |
author_facet | Benjamin J. Griffiths María Carmen Martín-Buro Bernhard P. Staresina Simon Hanslmayr |
author_sort | Benjamin J. Griffiths |
collection | DOAJ |
description | To form an episodic memory, we must first process a vast amount of sensory information about the to-be-encoded event and then bind these sensory representations together to form a coherent memory trace. While these two cognitive capabilities are thought to have two distinct neural origins, with neocortical alpha/beta oscillations supporting information representation and hippocampal theta-gamma phase-amplitude coupling supporting mnemonic binding, evidence for a dissociation between these two neural markers is conspicuously absent. To address this, seventeen human participants completed an associative memory task that first involved processing information about three sequentially-presented stimuli, and then binding these stimuli together into a coherent memory trace, all the while undergoing MEG recordings. We found that decreases in neocortical alpha/beta power during sequence perception, but not mnemonic binding, correlated with enhanced memory performance. Hippocampal theta/gamma phase-amplitude coupling, however, showed the opposite pattern; increases during mnemonic binding (but not sequence perception) correlated with enhanced memory performance. These results demonstrate that memory-related decreases in neocortical alpha/beta power and memory-related increases in hippocampal theta/gamma phase-amplitude coupling arise at distinct stages of the memory formation process. We speculate that this temporal dissociation reflects a functional dissociation in which neocortical alpha/beta oscillations could support the processing of incoming information relevant to the memory, while hippocampal theta-gamma phase-amplitude coupling could support the binding of this information into a coherent memory trace. |
first_indexed | 2024-12-22T05:57:30Z |
format | Article |
id | doaj.art-dbb5d85588b241d3b219c318b36f05c1 |
institution | Directory Open Access Journal |
issn | 1095-9572 |
language | English |
last_indexed | 2024-12-22T05:57:30Z |
publishDate | 2021-11-01 |
publisher | Elsevier |
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series | NeuroImage |
spelling | doaj.art-dbb5d85588b241d3b219c318b36f05c12022-12-21T18:36:40ZengElsevierNeuroImage1095-95722021-11-01242118454Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formationBenjamin J. Griffiths0María Carmen Martín-Buro1Bernhard P. Staresina2Simon Hanslmayr3Department of Psychology, Ludwig-Maximilians-University, Munich, Germany; School of Psychology, University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK; Corresponding authors at: Department of Psychology, Ludwig-Maximilians-University, Munich, Germany and Institute for Neuroscience and Psychology, University of Glasgow, UK.Department of Psychology, Rey Juan Carlos University, Alcorcón, Madrid 28922, SpainSchool of Psychology, University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK; Department of Experimental Psychology, University of Oxford, UKSchool of Psychology, University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK; Institute for Neuroscience and Psychology, University of Glasgow, UK; Corresponding authors at: Department of Psychology, Ludwig-Maximilians-University, Munich, Germany and Institute for Neuroscience and Psychology, University of Glasgow, UK.To form an episodic memory, we must first process a vast amount of sensory information about the to-be-encoded event and then bind these sensory representations together to form a coherent memory trace. While these two cognitive capabilities are thought to have two distinct neural origins, with neocortical alpha/beta oscillations supporting information representation and hippocampal theta-gamma phase-amplitude coupling supporting mnemonic binding, evidence for a dissociation between these two neural markers is conspicuously absent. To address this, seventeen human participants completed an associative memory task that first involved processing information about three sequentially-presented stimuli, and then binding these stimuli together into a coherent memory trace, all the while undergoing MEG recordings. We found that decreases in neocortical alpha/beta power during sequence perception, but not mnemonic binding, correlated with enhanced memory performance. Hippocampal theta/gamma phase-amplitude coupling, however, showed the opposite pattern; increases during mnemonic binding (but not sequence perception) correlated with enhanced memory performance. These results demonstrate that memory-related decreases in neocortical alpha/beta power and memory-related increases in hippocampal theta/gamma phase-amplitude coupling arise at distinct stages of the memory formation process. We speculate that this temporal dissociation reflects a functional dissociation in which neocortical alpha/beta oscillations could support the processing of incoming information relevant to the memory, while hippocampal theta-gamma phase-amplitude coupling could support the binding of this information into a coherent memory trace.http://www.sciencedirect.com/science/article/pii/S105381192100728X |
spellingShingle | Benjamin J. Griffiths María Carmen Martín-Buro Bernhard P. Staresina Simon Hanslmayr Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation NeuroImage |
title | Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation |
title_full | Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation |
title_fullStr | Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation |
title_full_unstemmed | Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation |
title_short | Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation |
title_sort | disentangling neocortical alpha beta and hippocampal theta gamma oscillations in human episodic memory formation |
url | http://www.sciencedirect.com/science/article/pii/S105381192100728X |
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