Abstract
Encoding of information by hippocampal neurons is defined by the number and the timing of action potentials generated relative to ongoing network oscillations in the theta (5–14 Hz), gamma (30–80 Hz) and ripple frequency range (150–200 Hz). The exact mechanisms underlying the temporal coupling of action potentials of hippocampal cells to the phase of rhythmic network activity are not fully understood. One critical determinant of action potential timing is synaptic inhibition provided by a complex network of Gamma-amino-hydroxy-butyric acid releasing (GABAergic) interneurons. Among the various GABAergic cell types, particularly Parvalbumin-expressing cells are powerful regulators of neuronal activity. Here we silenced Parvalbumin-expressing interneurons in hippocampal areas CA1 and the dentate gyrus in freely moving mice using the optogenetic silencing tool eNpHR to determine their influence on spike timing in principal cells. During optogenetic inhibition of Parvalbumin-expressing cells, local field potential recordings revealed no change in power or frequency of CA1 or dentate gyrus network oscillations. However, CA1 pyramidal neurons exhibited significantly reduced spike-phase coupling to CA1 theta, but not gamma or ripple oscillations. These data suggest that hippocampal Parvalbumin-expressing interneurons are particularly important for an intact theta-based temporal coding scheme of hippocampal principal cell populations.
Highlights
Encoding of information by hippocampal neurons is defined by the number and the timing of action potentials generated relative to ongoing network oscillations in the theta (5–14 Hz), gamma (30–80 Hz) and ripple frequency range (150–200 Hz)
To and efficiently silence hippocampal Parvalbumin expressing INs (PVIs), we injected adeno-associated viruses (AAVs) carrying a Cre-dependent genetic construct encoding for eNpHR-eYFP23 in the hippocampal subfields CA1 and dentate gyrus (DG) of seven PV-Cre mice
To examine the effect of PVI silencing on the level of individual cells and neuronal populations, we implanted an optrode coupled to a microdrive (Supplementary Fig. S1) in the dorsal hippocampus and simultaneously recorded single units and the local field potential (LFP) at different radial layers ranging from CA1 alveus/stratum oriens (AO), pyramidal cell layer (PCL), stratum radiatum/lacunosum-moleculare (RLM) to the DG
Summary
Encoding of information by hippocampal neurons is defined by the number and the timing of action potentials generated relative to ongoing network oscillations in the theta (5–14 Hz), gamma (30–80 Hz) and ripple frequency range (150–200 Hz). CA1 pyramidal neurons exhibited significantly reduced spike-phase coupling to CA1 theta, but not gamma or ripple oscillations These data suggest that hippocampal Parvalbumin-expressing interneurons are important for an intact theta-based temporal coding scheme of hippocampal principal cell populations. In vivo whole-cell voltage-clamp recordings from hippocampal PCs showed that inhibitory synaptic activity is temporally and spatially modulated by simultaneous neuronal network oscillations in different frequency r anges[15,16]. The differential contribution of PVIs to the generation of hippocampal network oscillations and to phase coupling of principal neuron activity to the different frequency bands is not clear We addressed these questions by optogenetic silencing of PVIs in the hippocampal subfields CA1 and the dentate gyrus (DG) in freely moving mice
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