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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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 |
work_keys_str_mv |
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