Interneuronal gap junctions increase synchrony and robustness of hippocampal ripple oscillations

Abstract

Sharp wave‐ripples (SWRs) are important for memory consolidation. Their signature in the hippocampal extracellular field potential can be decomposed into a ≈ 100 ms long sharp wave superimposed by ≈ 200 Hz ripple oscillations. How ripple oscillations are generated is currently not well understood. A promising model for the genesis of ripple oscillations is based on recurrent interneuronal networks (INT‐INT). According to this hypothesis, the INT‐INT network in CA1 receives a burst of excitation from CA3 that generates the sharp wave, and recurrent inhibition leads to an ultrafast synchronization of the CA1 network causing the ripple oscillations; fast‐spiking parvalbumin‐positive basket cells (PV+BCs) may constitute the ripple‐generating interneuronal network. PV+BCs are also coupled by gap junctions (GJs) but the function of GJs for ripple oscillations has not been quantified. Using simulations of CA1 hippocampal networks of PV+BCs, we show that GJs promote synchrony beyond a level that could be obtained by only inhibition. GJs also increase the neuronal firing rate of the interneuronal ensemble, while they affect the ripple frequency only mildly. The promoting effect of GJs on ripple oscillations depends on fast GJ transmission (≲ 0.5 ms), which requires proximal GJ coupling (≲ 100 μm from soma), but is robust to variability of the delay and the amplitude of GJ coupling.

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