Parvalbumin-positive interneurons mediate cortical-hippocampal interactions that are necessary for memory consolidation
Abstract
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.
Article and author information
Author details
Funding
Canadian Institutes of Health Research (FDN143227)
- Paul W Frankland
Canadian Institutes of Health Research (MOP74650)
- Sheena A Josselyn
Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-05458)
- Kaori Takehara-Nishiuchi
Natural Sciences and Engineering Research Council of Canada (RGPIN-2014-04947)
- Blake A Richards
Natural Sciences and Engineering Research Council of Canada
- Frances Xia
Natural Sciences and Engineering Research Council of Canada
- Matthew M Tran
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All procedures in this study were approved by the Canadian Council for Animal Care (CCAC) and the Animal Care Committees at the Hospital for Sick Children and the University of Toronto.
Reviewing Editor
- Marlene Bartos, University of Freiburg, Germany
Version history
- Received: April 17, 2017
- Accepted: September 28, 2017
- Accepted Manuscript published: September 29, 2017 (version 1)
- Version of Record published: October 24, 2017 (version 2)
Copyright
© 2017, Xia et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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