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Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model

Taxidis, Jiannis; Mizuseki, Kenji; Mason, Robert; Owen, Markus R.

Authors

Jiannis Taxidis

Kenji Mizuseki

Robert Mason

Markus R. Owen

Abstract

Hippocampal sharp wave-ripple complexes (SWRs) involve the synchronous discharge of thousands of cells throughout the CA3-CA1-subiculum-entorhinal cortex axis. Their strong
transient output affects cortical targets, rendering SWRs a possible means for memory transfer from the hippocampus to the neocortex for long-term storage. Neurophysiological
observations of hippocampal activity modulation by the cortical slow oscillation (SO) during deep sleep and anesthesia, and correlations between ripples and UP states, support the role of SWRs in memory consolidation through a cortico-hippocampal feedback loop. We couple a cortical network exhibiting SO with a hippocampal CA3-CA1 computational network model exhibiting SWRs, in order to model such cortico-hippocampal correlations and uncover important parameters and coupling mechanisms controlling them. The cortical oscillatory output entrains the CA3 network via connections representing the mossy fiber input, and the CA1 network via the temporoammonic pathway (TA). The
spiking activity in CA3 and CA1 is shown to depend on the excitation-to-inhibition ratio, induced by combining the two hippocampal inputs, with mossy fiber input controlling the UP-state correlation of CA3 population bursts and corresponding SWRs, whereas the temporoammonic input affects the overall CA1 spiking activity. Ripple characteristics and pyramidal spiking participation to SWRs are shaped by the strength of the Schaffer collateral drive. A set of in vivo recordings from the rat hippocampus confirms a model-predicted segregation of pyramidal cells into subgroups according to the SO state where they preferentially fire and their response to SWRs. These groups can potentially play distinct functional roles in the replay of spike sequences.

Journal Article Type Article
Publication Date Feb 5, 2013
Journal Frontiers in Computational Neuroscience
Electronic ISSN 1662-5188
Publisher Frontiers Media
Peer Reviewed Peer Reviewed
Volume 7
Issue Februa
Article Number 19
Institution Citation Taxidis, J., Mizuseki, K., Mason, R., & Owen, M. R. (2013). Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model. Frontiers in Computational Neuroscience, 7(Februa), doi:10.3389/fncom.2013.00003
DOI https://doi.org/10.3389/fncom.2013.00003
Publisher URL http://journal.frontiersin.org/Journal/10.3389/fncom.2013.00003/abstract
Copyright Statement Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0
Additional Information This Document is Protected by copyright and was first published by Frontiers. All rights reserved. It is reproduced with permission.

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