Abstract

Gamma rhythms are known to contribute to the process of memory encoding. However, little is known about the underlying mechanisms at the molecular, cellular and network levels. Using local field potential recording in awake behaving mice and concomitant field potential and whole-cell recordings in slice preparations we found that gamma rhythms lead to activity-dependent modification of hippocampal networks, including alterations in sharp wave-ripple complexes. Network plasticity, expressed as long-lasting increases in sharp wave-associated synaptic currents, exhibits enhanced excitatory synaptic strength in pyramidal cells that is induced postsynaptically and depends on metabotropic glutamate receptor-5 activation. In sharp contrast, alteration of inhibitory synaptic strength is independent of postsynaptic activation and less pronounced. Further, we found a cell type-specific, directionally biased synaptic plasticity of two major types of GABAergic cells, parvalbumin- and cholecystokinin-expressing interneurons. Thus, we propose that gamma frequency oscillations represent a network state that introduces long-lasting synaptic plasticity in a cell-specific manner.

Highlights

  • Neural oscillations are thought to play an important role in learning and memory processing (Axmacher et al, 2006; Duzel et al, 2010; Nyhus and Curran, 2010)

  • Using local field potential (LFP) recordings from dorsal hippocampus we found spontaneous sharp wave-ripple activity (SWR) in resting states of quietly sitting mice, while running behavior was accompanied by theta-nested gamma oscillations (Figure 1A)

  • The altered post-gamma SWR (p-SWR) could reflect a change of the animals internal state including the contribution of a different set of cell assembles (Buzsaki, 2015), which is difficult to control in vivo

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Summary

Introduction

Neural oscillations are thought to play an important role in learning and memory processing (Axmacher et al, 2006; Duzel et al, 2010; Nyhus and Curran, 2010). Neuroscience eLife digest Changes in the strength of synapses – the connections between neurons – form the basis of learning and memory This process, which is known as synaptic plasticity, incorporates transient experiences into persistent memory traces. In stark contrast to excitation, alteration of inhibitory synaptic strength was independent of postsynaptic activation and less pronounced, reflecting an IN-specific, directionally biased synaptic plasticity, as demonstrated in our study for two major GABAergic inhibitory cell types, PV- and CCK-expressing INs. Our results suggest that gamma frequency oscillations represent a network state that promotes the formation of long-lasting synaptic plasticity in the hippocampal area CA3, leading to modification of synaptic strengths in a cell-specific manner

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