Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples
- University of Lethbridge, Canada
- University of California, Irvine, United States
Abstract
A prevalent model is that sharp-wave ripples (SWR) arise 'spontaneously' in CA3 and propagate recent memory traces outward to the neocortex to facilitate memory consolidation there. Using voltage and extracellular glutamate transient recording over widespread regions of mice dorsal neocortex in relation to CA1 multiunit activity (MUA) and SWR, we find that the largest SWR-related modulation occurs in retrosplenial cortex; however, contrary to the unidirectional hypothesis, neocortical activation exhibited a continuum of activation timings relative to SWRs, varying from leading to lagging. Thus, contrary to the model in which SWRs arise 'spontaneously' in the hippocampus, neocortical activation often precedes SWRs and may thus constitute a trigger event in which neocortical information seeds associative reactivation of hippocampal 'indices'. This timing continuum is consistent with a dynamics in which older, more consolidated memories may in fact initiate the hippocampal-neocortical dialog, whereas reactivation of newer memories may be initiated predominantly in the hippocampus.
Data availability
All data analyzed and used to produce the main findings of this study have been deposited on Dryad. Source data files have been provided for Figures 2, 3, 5, and 7.
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Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripplesDryad Digital Repository, doi:10.5061/dryad.qnk98sfbb.
Article and author information
Author details
Edgar Bermudez-Contreras
Majid H Mohajerani
Funding
Natural Sciences and Engineering Research Council of Canada (40352)
- Majid H Mohajerani
Natural Sciences and Engineering Research Council of Canada (1631465)
- Bruce L McNaughton
Alberta Innovates - Health Solutions
- Majid H Mohajerani
Canadian Institutes of Health Research (390930)
- Majid H Mohajerani
Canadian Institutes of Health Research (156040)
- Bruce L McNaughton
Defense Advanced Research Projects Agency (HR0011-18-2-0021)
- Bruce L McNaughton
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: The animal housing, handling, and surgery protocols (#1812) were approved by the University of Lethbridge Animal Care Committee and were in accordance with guidelines set forth by the Canadian Council for Animal Care.
Copyright
© 2020, Karimi Abadchi 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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Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples
eLife 9:e51972.
https://doi.org/10.7554/eLife.51972
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