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Hippocampal CA1 Ripples as Inhibitory Transients

Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation....

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Autores principales: Malerba, Paola, Krishnan, Giri P, Fellous, Jean-Marc, Bazhenov, Maxim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4836732/
https://www.ncbi.nlm.nih.gov/pubmed/27093059
http://dx.doi.org/10.1371/journal.pcbi.1004880
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author Malerba, Paola
Krishnan, Giri P
Fellous, Jean-Marc
Bazhenov, Maxim
author_facet Malerba, Paola
Krishnan, Giri P
Fellous, Jean-Marc
Bazhenov, Maxim
author_sort Malerba, Paola
collection PubMed
description Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation. In the hippocampus, replay occurs within sharp wave-ripples: short bouts of high-frequency activity in area CA1 caused by excitatory activation from area CA3. In this work, we develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential inter-arrival times and yet highly non-variable durations. Our study predicts that ripples are not persistent oscillations but result from a transient network behavior, induced by input from CA3, in which the high frequency synchronous firing of perisomatic interneurons does not depend on the time scale of synaptic inhibition. We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration. Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network.
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spelling pubmed-48367322016-04-29 Hippocampal CA1 Ripples as Inhibitory Transients Malerba, Paola Krishnan, Giri P Fellous, Jean-Marc Bazhenov, Maxim PLoS Comput Biol Research Article Memories are stored and consolidated as a result of a dialogue between the hippocampus and cortex during sleep. Neurons active during behavior reactivate in both structures during sleep, in conjunction with characteristic brain oscillations that may form the neural substrate of memory consolidation. In the hippocampus, replay occurs within sharp wave-ripples: short bouts of high-frequency activity in area CA1 caused by excitatory activation from area CA3. In this work, we develop a computational model of ripple generation, motivated by in vivo rat data showing that ripples have a broad frequency distribution, exponential inter-arrival times and yet highly non-variable durations. Our study predicts that ripples are not persistent oscillations but result from a transient network behavior, induced by input from CA3, in which the high frequency synchronous firing of perisomatic interneurons does not depend on the time scale of synaptic inhibition. We found that noise-induced loss of synchrony among CA1 interneurons dynamically constrains individual ripple duration. Our study proposes a novel mechanism of hippocampal ripple generation consistent with a broad range of experimental data, and highlights the role of noise in regulating the duration of input-driven oscillatory spiking in an inhibitory network. Public Library of Science 2016-04-19 /pmc/articles/PMC4836732/ /pubmed/27093059 http://dx.doi.org/10.1371/journal.pcbi.1004880 Text en © 2016 Malerba et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Malerba, Paola
Krishnan, Giri P
Fellous, Jean-Marc
Bazhenov, Maxim
Hippocampal CA1 Ripples as Inhibitory Transients
title Hippocampal CA1 Ripples as Inhibitory Transients
title_full Hippocampal CA1 Ripples as Inhibitory Transients
title_fullStr Hippocampal CA1 Ripples as Inhibitory Transients
title_full_unstemmed Hippocampal CA1 Ripples as Inhibitory Transients
title_short Hippocampal CA1 Ripples as Inhibitory Transients
title_sort hippocampal ca1 ripples as inhibitory transients
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4836732/
https://www.ncbi.nlm.nih.gov/pubmed/27093059
http://dx.doi.org/10.1371/journal.pcbi.1004880
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