Abstract
The mammalian hippocampus expresses highly organized patterns of neuronal activity which form a neuronal correlate of spatial memories. These memory-encoding neuronal ensembles form on top of different network oscillations which entrain neurons in a state- and experience-dependent manner. The mechanisms underlying activation, timing and selection of participating neurons are incompletely understood. Here we studied the synaptic mechanisms underlying one prominent network pattern called sharp wave-ripple complexes (SPW-R) which are involved in memory consolidation during sleep. We recorded SPW-R with extracellular electrodes along the different layers of area CA1 in mouse hippocampal slices. Contribution of glutamatergic excitation and GABAergic inhibition, respectively, was probed by local application of receptor antagonists into s. radiatum, pyramidale and oriens. Laminar profiles of field potentials show that GABAergic potentials contribute substantially to sharp waves and superimposed ripple oscillations in s. pyramidale. Inhibitory inputs to s. pyramidale and s. oriens are crucial for action potential timing by ripple oscillations, as revealed by multiunit-recordings in the pyramidal cell layer. Glutamatergic afferents, on the other hand, contribute to sharp waves in s. radiatum where they also evoke a fast oscillation at ~200 Hz. Surprisingly, field ripples in s. radiatum are slightly slower than ripples in s. pyramidale, resulting in a systematic shift between dendritic and somatic oscillations. This complex interplay between dendritic excitation and perisomatic inhibition may be responsible for the precise timing of discharge probability during the time course of SPW-R. Together, our data illustrate a complementary role of spatially confined excitatory and inhibitory transmission during highly ordered network patterns in the hippocampus.
Highlights
The hippocampus expresses a variety of highly ordered spatiotemporal activity patterns which are believed to underlie memory formation and memory consolidation (Buzsáki, 1989; Harris et al, 2003; Buzsáki and Draguhn, 2004)
In order to dissect the laminar profile of sharp wave-ripple complexes (SPW-R) we used a linear array of eight equidistant extracellular electrodes which were placed perpendicularly to the pyramidal cell layer of CA1 between s. lacunosum-moleculare and the alveus (Figure 1A)
The underlying cellular mechanisms have been studied both in vivo (Buzsáki et al, 1992) and the in vitro slice preparation (Maier et al, 2003). These studies have shown that perisomatic inhibition is of key importance (Ylinen et al, 1995; Ellender et al, 2010) and that, at the same time, glutamatergic inputs from upstream projection neurons mediate synaptic excitation and propagation of activity (Buzsáki, 1986; Csicsvari et al, 2000; Both et al, 2008; Maier et al, 2011)
Summary
The hippocampus expresses a variety of highly ordered spatiotemporal activity patterns which are believed to underlie memory formation and memory consolidation (Buzsáki, 1989; Harris et al, 2003; Buzsáki and Draguhn, 2004). In extracellular field potential recordings, these sharp wave-ripple complexes (SPW-R) appear as monophasic synaptic potentials superimposed by a fast “ripple” oscillation at ∼200 Hz (Ylinen et al, 1995). SPW-R provide a template for sequential activation of selected neurons which repeat previously acquired representations of space- or context-dependent experience (O’Keefe, 1976; Wilson and McNaughton, 1994; Harris et al, 2003). Several studies show that individual cells or units are activated with astonishing temporal precision within individual ripple cycles, which last only ∼5 ms (Buzsáki et al, 1992; Ylinen et al, 1995; Csicsvari et al, 1999b). The mechanisms mediating selective and temporally precise activation of hippocampal neurons during such fast oscillations are, only partly understood. The intense activation of fast spiking interneurons during SPW-R suggests a role for phasic GABAergic inhibition (Csicsvari et al, 1999b; Klausberger et al, 2003; Ellender et al, 2010; Hájos et al, 2013)
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