Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation

Following learning, increased coupling between spindle oscillations in the medial prefrontal cortex (mPFC) and ripple oscillations in the hippocampus is thought to underlie memory consolidation. However, whether learning-induced increases in ripple-spindle coupling are necessary for successful memor...

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Main Authors: Frances Xia, Blake A Richards, Matthew M Tran, Sheena A Josselyn, Kaori Takehara-Nishiuchi, Paul W Frankland
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/27868
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spelling doaj-595af273dffd4e7591ab384a80940e792021-05-05T13:50:23ZengeLife Sciences Publications LtdeLife2050-084X2017-09-01610.7554/eLife.27868Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidationFrances Xia0https://orcid.org/0000-0001-7415-6620Blake A Richards1https://orcid.org/0000-0001-9662-2151Matthew M Tran2Sheena A Josselyn3https://orcid.org/0000-0001-5451-489XKaori Takehara-Nishiuchi4https://orcid.org/0000-0002-7282-7838Paul W Frankland5https://orcid.org/0000-0002-1395-3586Department of Physiology, University of Toronto, Toronto, Canada; Program in Neurosciences and Mental Health, Hospital for Sick Children, University Avenue, Toronto, CanadaDepartment of Biological Sciences, University of Toronto Scarborough, Toronto, Canada; Department of Cell and Systems Biology, University of Toronto, Toronto, CanadaDepartment of Biological Sciences, University of Toronto Scarborough, Toronto, Canada; Department of Cell and Systems Biology, University of Toronto, Toronto, CanadaDepartment of Physiology, University of Toronto, Toronto, Canada; Program in Neurosciences and Mental Health, Hospital for Sick Children, University Avenue, Toronto, Canada; Department of Psychology, University of Toronto, Toronto, Canada; Institute of Medical Sciences, University of Toronto, Toronto, CanadaDepartment of Cell and Systems Biology, University of Toronto, Toronto, Canada; Department of Psychology, University of Toronto, Toronto, Canada; Institute of Medical Sciences, University of Toronto, Toronto, CanadaDepartment of Physiology, University of Toronto, Toronto, Canada; Program in Neurosciences and Mental Health, Hospital for Sick Children, University Avenue, Toronto, Canada; Department of Psychology, University of Toronto, Toronto, Canada; Institute of Medical Sciences, University of Toronto, Toronto, CanadaFollowing learning, increased coupling between spindle oscillations in the medial prefrontal cortex (mPFC) and ripple oscillations in the hippocampus is thought to underlie memory consolidation. However, whether learning-induced increases in ripple-spindle coupling are necessary for successful memory consolidation has not been tested directly. In order to decouple ripple-spindle oscillations, here we chemogenetically inhibited parvalbumin-positive (PV+) interneurons, since their activity is important for regulating the timing of spiking activity during oscillations. We found that contextual fear conditioning increased ripple-spindle coupling in mice. However, inhibition of PV+ cells in either CA1 or mPFC eliminated this learning-induced increase in ripple-spindle coupling without affecting ripple or spindle incidence. Consistent with the hypothesized importance of ripple-spindle coupling in memory consolidation, post-training inhibition of PV+ cells disrupted contextual fear memory consolidation. These results indicate that successful memory consolidation requires coherent hippocampal-neocortical communication mediated by PV+ cells.https://elifesciences.org/articles/27868memoryconsolidationhippocampusanterior cingulate cortexripplespindle
collection DOAJ
language English
format Article
sources DOAJ
author Frances Xia
Blake A Richards
Matthew M Tran
Sheena A Josselyn
Kaori Takehara-Nishiuchi
Paul W Frankland
spellingShingle Frances Xia
Blake A Richards
Matthew M Tran
Sheena A Josselyn
Kaori Takehara-Nishiuchi
Paul W Frankland
Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
eLife
memory
consolidation
hippocampus
anterior cingulate cortex
ripple
spindle
author_facet Frances Xia
Blake A Richards
Matthew M Tran
Sheena A Josselyn
Kaori Takehara-Nishiuchi
Paul W Frankland
author_sort Frances Xia
title Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
title_short Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
title_full Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
title_fullStr Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
title_full_unstemmed Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
title_sort parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-09-01
description Following learning, increased coupling between spindle oscillations in the medial prefrontal cortex (mPFC) and ripple oscillations in the hippocampus is thought to underlie memory consolidation. However, whether learning-induced increases in ripple-spindle coupling are necessary for successful memory consolidation has not been tested directly. In order to decouple ripple-spindle oscillations, here we chemogenetically inhibited parvalbumin-positive (PV+) interneurons, since their activity is important for regulating the timing of spiking activity during oscillations. We found that contextual fear conditioning increased ripple-spindle coupling in mice. However, inhibition of PV+ cells in either CA1 or mPFC eliminated this learning-induced increase in ripple-spindle coupling without affecting ripple or spindle incidence. Consistent with the hypothesized importance of ripple-spindle coupling in memory consolidation, post-training inhibition of PV+ cells disrupted contextual fear memory consolidation. These results indicate that successful memory consolidation requires coherent hippocampal-neocortical communication mediated by PV+ cells.
topic memory
consolidation
hippocampus
anterior cingulate cortex
ripple
spindle
url https://elifesciences.org/articles/27868
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