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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Main Authors: Benjamin J. Griffiths, María Carmen Martín-Buro, Bernhard P. Staresina, Simon Hanslmayr
Format: Article
Language:English
Published: Elsevier 2021-11-01
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.
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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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