Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat

By J. J. Chrobak, G. Buzsáki. 1994

The coordinated activity of hippocampal neurons is reflected by macroscopic patterns, theta and sharp waves (SPW), evident in extracellular field recordings. The importance of these patterns is underscored by the ordered relation of specific neuronal populations to each pattern as well as the relation of each pattern to distinct behavioral states. During awake immobility, consummatory behavior, and slow wave sleep, CA3 and CA1 neurons participate in organized population bursts during SPW. In contrast, during theta-associated exploratory activity, the majority of principle cells are silent. Considerably less is known about the discharge properties of retrohippocampal neurons during theta, and particularly during SPW. These retrohippocampal neurons (entorhinal cortical, parasubicular, presubicular, and subicular) process and transmit information between the neocortex and the hippocampus. The present study examined the activity of these neurons in freely behaving rats during SPW (awake immobility) as well as theta (locomotion and REM sleep). A qualitative distinction between the activity of deep (V-VI) and superficial (II- III) layer retrohippocampal neurons was observed in relation to SPW as compared to theta. Deep layer retrohippocampal neurons exhibited a concurrent increase in activity during hippocampal SPW. In contrast, deep layer neurons were not modulated by the prominent theta oscillations observed throughout the hippocampus and entorhinal cortex. On the other hand, superficial layer retrohippocampal neurons were often phase-related to theta oscillations, but were surprisingly indifferent to the SPW-associated population bursting occurring within the deep layers. These findings indicate a concerted discharge of the hippocampal and retrohippocampal cortices during SPW that includes neurons within CA3, CA1, and subiculum as well as neurons in layers V- VI of the presubiculum, parasubiculum, and entorhinal cortex. Further, they suggest a temporal discontinuity in the input/output relations between the hippocampus and retrohippocampal structures. We suggest that SPW-associated population bursts in hippocampal and retrohippocampal cortices exert a powerful depolarizing effect on their postsynaptic neocortical targets and may represent a physiological mechanism for memory trace transfer from the hippocampus to the neocortex.

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Citations in the corpus

Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics (1999, background): “…with the idea that these events reflect convergence of the network onto “attractor” states representing stored memories (McNaughton, 1983; Chrobak and Buzsáki, 1994; Wilson and McNaughton, 1994; Shen and McNaughton, 1996); however, this conjecture requires verification from further analysis.”
Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory (2005, background): “…behaviors, a truly self-organized pattern, called sharp wave burst, emerges in the recursive networks of the CA3 region and sweeps through the entire hippocampal–entorhinal system at irregular intervals (Buzsáki et al., 1983; Buzsáki et al., 1992; Chrobak and Buzsaki, 1994; Ylinen et al., 1995).”
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).”
The role of acetylcholine in learning and memory. (2006, background): “High cholinergic levels during waking suppress feedback, providing dominant feedforward effects appropriate for encoding, and reducing the influence of hippocampus on entorhinal cortex [31].”
Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration (2014, background): “This evidence is often tied together with work suggesting that the dialogue between hippocampus and cortex may reverse in direction between wake and sleep (Buzsáki, 1998; Chrobak and Buzsáki, 1994), that the neuromodulatory milieu of sleep may favor outflow from hippocampus in some stages of sleep (”
On the methods for reactivation and replay analysis (2020, background): “SWRs entrain downstream targets of the hippocampus in the entorhinal cortex [10], confirming the original hypothesis that these physiological events may underlie a global phenomenon implied in memory formation.”
High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat (1996, background): “Previous findings demonstrated that the superficial layer (II– III) neurons within these regions do not seem to be influenced by hippocampal sharp waves (Chrobak and Buzsáki, 1994).”
Neural syntax: cell assemblies, synapsembles and readers (2010, unknown): “, 2008) and often grouped by slower oscillations (Bragin et al., 1995; Canolty et al., 2006; Chrobak and Buzsáki, 1998; Hasenstaub et al., 2005; Sirota et al., 2008; Steriade, 2006).”