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Theta-phase-specific modulation of dentate gyrus memory neurons

The theta rhythm, a quasi-periodic 4–10 Hz oscillation, is observed during memory processing in the hippocampus, with different phases of theta hypothesized to separate independent streams of information related to the encoding and recall of memories. At the cellular level, the discovery of hippocam...

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Autores principales: Rahsepar, Bahar, Norman, Jacob F, Noueihed, Jad, Lahner, Benjamin, Quick, Melanie H, Ghaemi, Kevin, Pandya, Aashna, Fernandez, Fernando R, Ramirez, Steve, White, John A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10361715/
https://www.ncbi.nlm.nih.gov/pubmed/37401757
http://dx.doi.org/10.7554/eLife.82697
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author Rahsepar, Bahar
Norman, Jacob F
Noueihed, Jad
Lahner, Benjamin
Quick, Melanie H
Ghaemi, Kevin
Pandya, Aashna
Fernandez, Fernando R
Ramirez, Steve
White, John A
author_facet Rahsepar, Bahar
Norman, Jacob F
Noueihed, Jad
Lahner, Benjamin
Quick, Melanie H
Ghaemi, Kevin
Pandya, Aashna
Fernandez, Fernando R
Ramirez, Steve
White, John A
author_sort Rahsepar, Bahar
collection PubMed
description The theta rhythm, a quasi-periodic 4–10 Hz oscillation, is observed during memory processing in the hippocampus, with different phases of theta hypothesized to separate independent streams of information related to the encoding and recall of memories. At the cellular level, the discovery of hippocampal memory cells (engram neurons), as well as the modulation of memory recall through optogenetic activation of these cells, has provided evidence that certain memories are stored, in part, in a sparse ensemble of neurons in the hippocampus. In previous research, however, engram reactivation has been carried out using open-loop stimulation at fixed frequencies; the relationship between engram neuron reactivation and ongoing network oscillations has not been taken into consideration. To address this concern, we implemented a closed-loop reactivation of engram neurons that enabled phase-specific stimulation relative to theta oscillations in the local field potential in CA1. Using this real-time approach, we tested the impact of activating dentate gyrus engram neurons during the peak (encoding phase) and trough (recall phase) of theta oscillations. Consistent with previously hypothesized functions of theta oscillations in memory function, we show that stimulating dentate gyrus engram neurons at the trough of theta is more effective in eliciting behavioral recall than either fixed-frequency stimulation or stimulation at the peak of theta. Moreover, phase-specific trough stimulation is accompanied by an increase in the coupling between gamma and theta oscillations in CA1 hippocampus. Our results provide a causal link between phase-specific activation of engram cells and the behavioral expression of memory.
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spelling pubmed-103617152023-07-22 Theta-phase-specific modulation of dentate gyrus memory neurons Rahsepar, Bahar Norman, Jacob F Noueihed, Jad Lahner, Benjamin Quick, Melanie H Ghaemi, Kevin Pandya, Aashna Fernandez, Fernando R Ramirez, Steve White, John A eLife Neuroscience The theta rhythm, a quasi-periodic 4–10 Hz oscillation, is observed during memory processing in the hippocampus, with different phases of theta hypothesized to separate independent streams of information related to the encoding and recall of memories. At the cellular level, the discovery of hippocampal memory cells (engram neurons), as well as the modulation of memory recall through optogenetic activation of these cells, has provided evidence that certain memories are stored, in part, in a sparse ensemble of neurons in the hippocampus. In previous research, however, engram reactivation has been carried out using open-loop stimulation at fixed frequencies; the relationship between engram neuron reactivation and ongoing network oscillations has not been taken into consideration. To address this concern, we implemented a closed-loop reactivation of engram neurons that enabled phase-specific stimulation relative to theta oscillations in the local field potential in CA1. Using this real-time approach, we tested the impact of activating dentate gyrus engram neurons during the peak (encoding phase) and trough (recall phase) of theta oscillations. Consistent with previously hypothesized functions of theta oscillations in memory function, we show that stimulating dentate gyrus engram neurons at the trough of theta is more effective in eliciting behavioral recall than either fixed-frequency stimulation or stimulation at the peak of theta. Moreover, phase-specific trough stimulation is accompanied by an increase in the coupling between gamma and theta oscillations in CA1 hippocampus. Our results provide a causal link between phase-specific activation of engram cells and the behavioral expression of memory. eLife Sciences Publications, Ltd 2023-07-04 /pmc/articles/PMC10361715/ /pubmed/37401757 http://dx.doi.org/10.7554/eLife.82697 Text en © 2023, Rahsepar, Norman et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Rahsepar, Bahar
Norman, Jacob F
Noueihed, Jad
Lahner, Benjamin
Quick, Melanie H
Ghaemi, Kevin
Pandya, Aashna
Fernandez, Fernando R
Ramirez, Steve
White, John A
Theta-phase-specific modulation of dentate gyrus memory neurons
title Theta-phase-specific modulation of dentate gyrus memory neurons
title_full Theta-phase-specific modulation of dentate gyrus memory neurons
title_fullStr Theta-phase-specific modulation of dentate gyrus memory neurons
title_full_unstemmed Theta-phase-specific modulation of dentate gyrus memory neurons
title_short Theta-phase-specific modulation of dentate gyrus memory neurons
title_sort theta-phase-specific modulation of dentate gyrus memory neurons
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10361715/
https://www.ncbi.nlm.nih.gov/pubmed/37401757
http://dx.doi.org/10.7554/eLife.82697
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