Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes

By C. Pavlides, J. Winson. 1989

Rat hippocampal (CA1) complex spike “place cells” of freely behaving rats were recorded in pairs continuously during a series of waking (exploration and still-alert), drowsy (quiet-awake), and sleeping (slow- wave, pre-rapid-eye-movement and rapid-eye-movement sleep) behaviors. Pairs of units were selected that had nonoverlapping place fields. The rats were restricted from entering the place field of either cell overnight, and on the day of recording cells were exposed to their individual place fields independently and in a counterbalanced manner. Following exposure, recordings were made in the subsequent sleep episodes and the firing characteristics of both cells were analyzed. Following exposure, significant increases in the spiking activity of the exposed cell were observed in the subsequent sleeping states that were not evident in the unexposed cell. The increased activity was observed in the rate of firing (spikes/sec), the rate of occurrence of bursts with multiple spikes, as well as the number of bursts displaying short (2–4 msec) interspike intervals. The findings suggest that neuronal activity of hippocampal place cells in the awake states may influence the firing characteristics of these cells in subsequent sleep episodes. The increased firing rates along with the greater number of multiple spike bursts and the shorter interspike intervals within the burst, following exposure to a cell's place field, may represent possible information processing during sleep.

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Citations in the corpus

Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “The first evidence of replay in the hippocampus was observed in the firing patterns of pairs of neurons (Pavlides & Winson, 1989; Wilson & McNaughton, 1994).”
Awake replay of remote experiences in the hippocampus (2009, positive): “During these periods hippocampal place cells that fire together during exploration tend to fire together afterwards Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://w”
Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics (1999, background): “In support of these ideas, Pavlides and Winson (1989) demonstrated that hippocampal CA1 neurons that were highly active during behavior exhibited increased firing rates during subsequent sleep, relative to previous sleep.”
Retrieval and reconsolidation: toward a neurobiology of remembering. (2000, background): “Pavlides and Winson (1989) reported that particular hippocampal place cells that fired during exploratory behavior were selectively more active during the SWS episode following this behavior.”
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. (2001, background): “To investigate the structure of neural (Pavlides and Winson, 1989; Poe et al., 2000), efforts to detect short-timescale mnemonic activity like thatactivity during REM sleep, we simultaneously re- corded the activity of multiple neurons in the rat hippo- observed during SWS have failed to detect…”
The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples (2004, background): “Postbehavioral firing rates of hippocampal cells, which were first activated by exposure to their place fields, can be enhanced with respect to prebehavioral firing rates (Pavlides and Winson 1989), but apparently only if the previous waking episode was restricted to a small space encompassing the p”
Replay and Time Compression of Recurring Spike Sequences in the Hippocampus (1999, background): “In a previous study, Pavlides and Winson (1989) examined pairs of putative pyramidal cells recorded by the same single wire.”
Replay Comes of Age. (2017, background): “An early study reported that those place cells active in an environment, which typically comprise 30–50% of all place cells (Guzowski et al. 1999, Wilson & McNaughton 1993), were more active in subsequent sleep than those that had not been active in the environment (Pavlides & Winson 1989).”
Hebbian learning, its correlation catastrophe, and unlearning (1997, background): “So some of the neurons must become active again [1, 14, 15] during a ‘dream’—the more so, since the network always starts with the elimination of global correlations, such as common aspects of different patterns.”