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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Main Authors: Paola Malerba, Giri P Krishnan, Jean-Marc Fellous, Maxim Bazhenov
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-04-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC4836732?pdf=render
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author Paola Malerba
Giri P Krishnan
Jean-Marc Fellous
Maxim Bazhenov
author_facet Paola Malerba
Giri P Krishnan
Jean-Marc Fellous
Maxim Bazhenov
author_sort Paola Malerba
collection DOAJ
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 doaj.art-dccbaf24e56d46f385ca1a1af05170722022-12-22T02:10:27ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582016-04-01124e100488010.1371/journal.pcbi.1004880Hippocampal CA1 Ripples as Inhibitory Transients.Paola MalerbaGiri P KrishnanJean-Marc FellousMaxim BazhenovMemories 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.http://europepmc.org/articles/PMC4836732?pdf=render
spellingShingle Paola Malerba
Giri P Krishnan
Jean-Marc Fellous
Maxim Bazhenov
Hippocampal CA1 Ripples as Inhibitory Transients.
PLoS Computational Biology
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
url http://europepmc.org/articles/PMC4836732?pdf=render
work_keys_str_mv AT paolamalerba hippocampalca1ripplesasinhibitorytransients
AT giripkrishnan hippocampalca1ripplesasinhibitorytransients
AT jeanmarcfellous hippocampalca1ripplesasinhibitorytransients
AT maximbazhenov hippocampalca1ripplesasinhibitorytransients