Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice

Coordinated peri-ripple activity in the hippocampal-neocortical network is essential for mnemonic information processing in the brain. Hippocampal ripples likely serve different functions in sleep and awake states. Thus, the corresponding neocortical activity patterns may differ in important ways. W...

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Main Authors: Javad Karimi Abadchi, Zahra Rezaei, Thomas Knöpfel, Bruce L McNaughton, Majid H Mohajerani
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/79513
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author Javad Karimi Abadchi
Zahra Rezaei
Thomas Knöpfel
Bruce L McNaughton
Majid H Mohajerani
author_facet Javad Karimi Abadchi
Zahra Rezaei
Thomas Knöpfel
Bruce L McNaughton
Majid H Mohajerani
author_sort Javad Karimi Abadchi
collection DOAJ
description Coordinated peri-ripple activity in the hippocampal-neocortical network is essential for mnemonic information processing in the brain. Hippocampal ripples likely serve different functions in sleep and awake states. Thus, the corresponding neocortical activity patterns may differ in important ways. We addressed this possibility by conducting voltage and glutamate wide-field imaging of the neocortex with concurrent hippocampal electrophysiology in awake mice. Contrary to our previously published sleep results, deactivation and activation were dominant in post-ripple neocortical voltage and glutamate activity, respectively, especially in the agranular retrosplenial cortex (aRSC). Additionally, the spiking activity of aRSC neurons, estimated by two-photon calcium imaging, revealed the existence of two subpopulations of excitatory neurons with opposite peri-ripple modulation patterns: one increases and the other decreases firing rate. These differences in peri-ripple spatiotemporal patterns of neocortical activity in sleep versus awake states might underlie the reported differences in the function of sleep versus awake ripples.
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spelling doaj.art-924fdffa35ba468786103704aebc99062023-01-25T15:11:24ZengeLife Sciences Publications LtdeLife2050-084X2023-01-011210.7554/eLife.79513Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in miceJavad Karimi Abadchi0https://orcid.org/0000-0003-4175-7598Zahra Rezaei1Thomas Knöpfel2https://orcid.org/0000-0002-5718-0765Bruce L McNaughton3Majid H Mohajerani4https://orcid.org/0000-0003-0964-2977Canadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, CanadaCanadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, CanadaLaboratory for Neuronal Circuit Dynamics, Imperial College London, London, United Kingdom; Department of Physics, Hong Kong Baptist University, Kowloon Tong, Hong KongCanadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, Canada; Department of Neurobiology and Behavior, University of California, Irvine, United StatesCanadian Centre for Behavioral Neuroscience, University of Lethbridge, Lethbridge, CanadaCoordinated peri-ripple activity in the hippocampal-neocortical network is essential for mnemonic information processing in the brain. Hippocampal ripples likely serve different functions in sleep and awake states. Thus, the corresponding neocortical activity patterns may differ in important ways. We addressed this possibility by conducting voltage and glutamate wide-field imaging of the neocortex with concurrent hippocampal electrophysiology in awake mice. Contrary to our previously published sleep results, deactivation and activation were dominant in post-ripple neocortical voltage and glutamate activity, respectively, especially in the agranular retrosplenial cortex (aRSC). Additionally, the spiking activity of aRSC neurons, estimated by two-photon calcium imaging, revealed the existence of two subpopulations of excitatory neurons with opposite peri-ripple modulation patterns: one increases and the other decreases firing rate. These differences in peri-ripple spatiotemporal patterns of neocortical activity in sleep versus awake states might underlie the reported differences in the function of sleep versus awake ripples.https://elifesciences.org/articles/79513hippocampusneocortexhippocampal-neocortical interactionmemory consolidationsharp-wave ripplevoltage/glutamate/calcium imaging
spellingShingle Javad Karimi Abadchi
Zahra Rezaei
Thomas Knöpfel
Bruce L McNaughton
Majid H Mohajerani
Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
eLife
hippocampus
neocortex
hippocampal-neocortical interaction
memory consolidation
sharp-wave ripple
voltage/glutamate/calcium imaging
title Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
title_full Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
title_fullStr Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
title_full_unstemmed Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
title_short Inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
title_sort inhibition is a prevalent mode of activity in the neocortex around awake hippocampal ripples in mice
topic hippocampus
neocortex
hippocampal-neocortical interaction
memory consolidation
sharp-wave ripple
voltage/glutamate/calcium imaging
url https://elifesciences.org/articles/79513
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