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SWRs were proposed to play an important role in memory consolidation ( Buzsáki, 1989). Hippocampal sharp wave-ripple complexes (SWRs) occur during behavioral immobility and non-REM sleep ( Buzsáki et al., 1983 Buzsáki, 1986) and consist of an aperiodically occurring field potential transient, the sharp wave, and a superimposed fast, periodic (150–200 Hz) oscillation, the ripples. These interneurons are thus essential in organizing pyramidal cell activity not only during gamma oscillation, but, in a different configuration, during SWRs.ĭifferent types of behavior are accompanied by distinct brain states, which are characterized by various EEG patterns that indicate unique underlying network dynamics. Local drug applications and modeling experiments confirmed that the activity of parvalbumin-positive perisomatic inhibitory neurons is both necessary and sufficient for ripple-frequency current and rhythm generation. Conversely, optogenetic silencing of parvalbumin-positive cells interrupted the SWRs or inhibited their occurrence. Even with excitation blocked, tonic driving of parvalbumin-positive cells evoked ripple oscillations.
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Optogenetic stimulation of parvalbumin-positive cells evoked full SWRs and EPSC sequences in pyramidal cells. The synchronized GABA A receptor-mediated currents give rise to a major component of the ripple-frequency oscillation in the local field potential and organize the phase-locked spiking of pyramidal cells. We showed that this tonic excitatory envelope drives reciprocally connected parvalbumin-positive basket cells, which start ripple-frequency spiking that is phase-locked through reciprocal inhibition. SWRs initiate when firing in a set of spontaneously active pyramidal cells triggers a gradual, exponential buildup of activity in the recurrent CA3 network.
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Our results suggest that SWRs are initiated through a combined refractory and stochastic mechanism. We recorded EPSCs and IPSCs to examine the buildup of neuronal activity preceding SWRs and analyzed the distribution of time intervals between subsequent SWR events.
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To understand the mechanisms underlying the initiation of irregularly occurring SWRs and the generation of periodic ripples, we selectively manipulated different components of the CA3 network in mouse hippocampal slices. Replay of neuronal activity during hippocampal sharp wave-ripples (SWRs) is essential in memory formation.