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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 and Mizuseki, Kenji and Mason, Robert and Owen, Markus 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 . Art. No. 3. ISSN 1662-5188. doi:10.3389/fncom.2013.00003. https://resolver.caltech.edu/CaltechAUTHORS:20130308-103322250

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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.


Item Type:Article
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URLURL TypeDescription
http://dx.doi.org/10.3389/fncom.2013.00003DOIUNSPECIFIED
http://www.frontiersin.org/Computational_Neuroscience/10.3389/fncom.2013.00003/abstractPublisherUNSPECIFIED
Additional Information:© 2013 Taxidis, Mizuseki, Mason and Owen. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc. Received: 28 November 2012; Accepted: 21 January 2013; Published online: 05 February 2013. The authors would like to warmly thank Albert Compte for his help and advice in implementing the cortical model, György Buzsáki, Christof Koch, Anton Sirota, and Erik Schomburg for helpful discussions, Steve Coombes for his valuable help in constructing our computational model, Uri Maoz for his help in statistical analysis and all reviewers for their constructive recommendations. This work was funded by the Marie Curie Network, MMBNOTT, Project No. MEST-CT-2005-020723).
Funders:
Funding AgencyGrant Number
Marie Curie Network MMBNOTTMEST-CT-2005-020723
Subject Keywords:hippocampus; slow oscillation; sharp waves; ripples; mossy fibers; temporoammonic pathway; correlations
DOI:10.3389/fncom.2013.00003
Record Number:CaltechAUTHORS:20130308-103322250
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130308-103322250
Official Citation:Taxidis J, Mizuseki K, Mason R and Owen MR (2013) Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model. Front. Comput. Neurosci. 7:3. doi: 10.3389/fncom.2013.00003
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:37417
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:08 Mar 2013 19:06
Last Modified:09 Nov 2021 23:28

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