During non-REM sleep, memory consolidation is driven by a dialogue between hippocampus and cortex involving the reactivation of specific neural activity sequences ('replay'). In the hippocampus, replay occurs during sharp-wave ripples (SWRs), short bouts of excitatory activity in area CA3 which induce high frequency oscillations in the inhibitory interneurons of area CA1. Despite growing evidence for the functional importance of replay, its neural mechanisms remain poorly understood. Here, we develop a novel theoretical model of hippocampal spiking during SWRs. In our model, noise-induced activation of CA3 pyramidal cells triggered an excitatory cascade capable of inducing local ripple events in CA1.Ripples occurred stochastically, with Schaffer Collaterals driving their coordination, so that localized sharp waves in CA3 produced consistently localized CA1 ripples. In agreement with experimental data, the majority of pyramidal cells in the model showed low reactivation probabilities across SWRs. We found, however, that a subpopulation of pyramidal cells had high reactivation probabilities, which derived from fine-tuning of the network connectivity. In particular, the excitatory inputs along synaptic pathway(s) converging onto cells and cell pairs controlled emergent single cell and cell pair reactivation, with inhibitory inputs and intrinsic cell excitability playing differential roles in CA3 vs. CA1. Our model predicts (1) that the hippocampal network structure driving the emergence of SWR is also able to generate and modulate reactivation, (2) inhibition plays a particularly prominent role in CA3 reactivation and (3) CA1 sequence reactivation is reliant on CA3-CA1 interactions rather than an intrinsic CA1 process.. CC-BY-NC-ND4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/164699 doi: bioRxiv preprint first posted online Jul. 18, 2017; New and NoteworthyWe develop a new biophysical model of hippocampal sharp-wave ripple activity to study determinants of pyramidal cell reactivation during sleep. The majority of pyramidal cells revealed low reactivation probabilities arising from stationary network properties. Highly reactivating subpopulations were driven by cell-specific synaptic inputs, with CA3 excitatory recurrents and CA3-CA1 Schaffer Collaterals interacting to promote reliable CA1 sequence reactivation. The model recapitulates experimental data and highlights mechanisms by which experience-dependent inputs can tune memory consolidation.
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