High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat

By J. J. Chrobak, György Buzsáki. 1996

Population bursts of the CA3 network, which occur during eating, drinking, awake immobility, and slow-wave sleep, produce a large field excitatory postsynaptic potential throughout stratum radiatum of the CA1 field (sharp wave). The CA3 burst sets into motion a short-lived, dynamic interaction between CA1 pyramidal cells and interneurons, the product of which is a 200 Hz oscillatory field potential (ripple) and phase-related discharge of the CA1 network. Although many CA1 pyramidal neurons discharge during the time frame (50–100 msec) of each sharp wave, each wave of a ripple (∼5 msec) reflects the synchronization of more discrete subsets of CA1 neurons. When we used multi-site recordings in freely behaving rats, we observed ripples throughout the longitudinal extent (∼4–5 mm) of the dorsal CA1 region that were coherent for multiple cycles of each ripple. High-frequency ripples were also observed throughout the hippocampal–entorhinal output pathway that were concurrent but less coherent on a cycle-by-cycle basis. Single and multiunit neuronal activity was phase-related to local ripples throughout the hippocampal–entorhinal output pathway. Entorhinal ripples occurred 5–30 msec after the CA1 ripples and were related to the occurrence of an entorhinal sharp wave. Thus, during each hippocampal sharp wave, there is a powerful synchronization among the neuronal networks that connect the hippocampus to the neocortex. We suggest that this population interaction (1) biologically constrains theoretical models of hippocampal function and dysfunction and (2) has the capacity to support an “off-line” memory consolidation process.

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Citations in the corpus

Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, background): “Activity during SWRs propagates from CA3 to CA1, one of the main output areas of the hippocampus, and then out to neocorte”
Hippocampal replay of extended experience (2009, neutral): “During pauses in locomotion and during slow-wave sleep, many place cells are recruited in intermittent population bursts, which are accompanied by ripples in the hippocampal local field potential (Buzsáki et al., 1992; Chrobak and Buzsáki, 1996).”
About sleep's role in memory. (2013, neutral): “, high-frequency local field potential oscillations (100– 300 Hz) originating in CA1] to form SW-R events (159, 162, 196, 241, 459, 832, 1342).”
The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples (2004, background): “In concert with CA1, the subiculum and entorhinal cortex may well contribute to ripple modulation of VS firing rate (Chrobak and Buzsáki, 1996).”
Sleep to Remember (2006, background): “They are superimposed upon ripple activity, which is a high-frequency local field potential oscillation (100–300 Hz) originating in CA1 (Buzsáki 1986; Chrobak and Buzsáki 1994, 1996).”
New experiences enhance coordinated neural activity in the hippocampus. (2008, unknown): “Ripple-like events can also be detected using a variety of thresholds (Chrobak and Buzsaki, 1996; Csicsvari et al., 2000).”
Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. (1998, background): “These highfrequency oscillations constitute a major mode of hippocampal activity (Buzsaki et al., 1992; Ylinen et al., 1995; Chrobak and Buzsaki, 1996), and they provide ideal physiological conditions for the induction of the longAthanassios G.”
Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience (1998, background): “These ripples are a consequence of synchronous discharges of CA3 pyramidal cell populations (BuzsaÂ ki et al. 1992; BuzsaÂ ki et al. 1983; BuzsaÂ ki 1986; Ylinen et al. 1995b).”
Regional slow waves and spindles in human sleep. (2011, unknown): “Since the entorhinal cortex provides both the major input to and receives output from the hippocampus, our results support the notion that ripples reflect hippocampal output (Chrobak and Buzsaki, 1996).”
Correlated neuronal activity and the flow of neural information (2001, background): “Direct measurement of field potentials from the cortex reveals even higher-frequency components in the 40–200-Hz rang”
Memory consolidation. (2015, unknown): “Cite this article as Cold Spring Harb Perspect Biol 2015;7:a021766 17”