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

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

doi:10.3389/fncom.2013.00003

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.

Highlights

The standard model for memory consolidation assumes that new memories are stored temporarily in hippocampal and parahippocampal areas, and are later transferred to the neocortex, during slow wave sleep (SWS), for long-term storage (Buzsáki, 1989, 2006; Eichenbaum, 2000)
We first explore the role of the mossy fiber input on CA3 population bursts and the oscillatory responses in CA1 resulting from the Schaffer collaterals
The main results from our simulations can be summarized as follows: (1) The correlation of CA3 population bursts, and corresponding CA1 sharp wave-ripple complexes (SWRs), with the cortical slow oscillation (SO) are controlled by the feedforward excitation-to-inhibition ratio induced by the mossy fiber input

Summary

Introduction

The standard model for memory consolidation assumes that new memories are stored temporarily in hippocampal and parahippocampal areas, and are later transferred to the neocortex, during slow wave sleep (SWS), for long-term storage (Buzsáki, 1989, 2006; Eichenbaum, 2000). A series of recent observations suggest a general drive from cortex to hippocampus during SWS (Siapas and Wilson, 1998; Sirota et al, 2003; Hahn et al, 2006, 2007; Isomura et al, 2006; Mölle et al, 2006). These studies focus on the temporal relationships between intrinsic rhythmic oscillations found in the cortex and hippocampus, the slow oscillation (SO) and the sharp wave-ripple complexes (SWRs) respectively. Various theoretical and computational approaches of different architectures and complexities have addressed potential cellular and/or network mechanisms underlying such oscillations (Bazhenov et al, 2002; Compte et al, 2003; Hill and Tononi, 2005; Holcman and Tsodyks, 2006; Parga and Abbott, 2007)

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