Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics

By Hemant S. Kudrimoti, C. A. Barnes, Bruce L. McNaughton. 1999

During slow wave sleep (SWS), traces of neuronal activity patterns from preceding behavior can be observed in rat hippocampus and neocortex. The spontaneous reactivation of these patterns is manifested as the reinstatement of the distribution of pairwise firing-rate correlations within a population of simultaneously recorded neurons. The effects of behavioral state [quiet wakefulness, SWS, and rapid eye movement (REM)], interactions between two successive spatial experiences, and global modulation during 200 Hz electroencephalographic (EEG) “ripples” on pattern reinstatement were studied in CA1 pyramidal cell population recordings. Pairwise firing-rate correlations during often repeated experiences accounted for a significant proportion of the variance in these interactions in subsequent SWS or quiet wakefulness and, to a lesser degree, during SWS before the experience on a given day. The latter effect was absent for novel experiences, suggesting that a persistent memory trace develops with experience. Pattern reinstatement was strongest during sharp wave–ripple oscillations, suggesting that these events may reflect system convergence onto attractor states corresponding to previous experiences. When two different experiences occurred in succession, the statistically independent effects of both were evident in subsequent SWS. Thus, the patterns of neural activity reemerge spontaneously, and in an interleaved manner, and do not necessarily reflect persistence of an active memory (i.e., reverberation). Firing-rate correlations during REM sleep were not related to the preceding familiar experience, possibly as a consequence of trace decay during the intervening SWS. REM episodes also did not detectably influence the correlation structure in subsequent SWS, suggesting a lack of strengthening of memory traces during REM sleep, at least in the case of familiar experiences.

Subfields: Neuroscience

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Citations in the corpus

Lifelong Learning of Spatiotemporal Representations With Dual-Memory Recurrent Self-Organization (2018, positive): “This is conceptually consistent with neurophysiological studies evidencing that hippocampal replay consists of the reactivation of previously stored patterns of neural activity occurring predominantly after an experience (Kudrimoti et al., 1999; Karlsson and Frank, 2009).”
Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “While the majority of replay studies are from NREM sleep, some studies have shown replay during REM sleep (Louie & Wilson, 2001; Eckert et al., 2020; Kudrimoti et al., 1999).”
Hippocampal Replay is Not a Simple Function of Experience (2010, background): “Whereas previous studies (Wil- son and McNaughton, 1994; Jackson et al., 2006; O’Neill et al., 2006; Karlsson and Frank, 2009) have found increasing replay with experience, these studies did not compare tasks with different behavioral requirements in which parts of the environment were experienced m”
About sleep's role in memory. (2013, methodology): “The slow oscillations during SWS drive the repeated reactivation of hippocampal memory representations during sharp wave-ripples (SW-Rs; FIGURE 1B) in the hippocampus together with thalamo-cortical spindles, which are involved in inducing enduring plastic changes in cortical areas (FIGURE 3B).”
ReviewMemory Consolidation in Sleep: Dream or Reality (2004, background): “As noted above, Walker et sleep in rats (Kudrimoti et al., 1999) and primates (Hoff-al.”
On the methods for reactivation and replay analysis (2020, background): “One caveat with EV is that it is not compared to a proper control but is simply expected to be stronger than wake-PRE coherence [12].”
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus (2009, unknown): “Previous reports of reactivation during pauses in behavior have documented increased coordinated activity of pairs of CA1 place cells during SWRs (Kudrimoti et al., 1999; Cheng and Frank, 2008) as well as sequential replay of CA3 and CA1 place cells during SWRs (Foster and Wilson, 2006; Diba and Buz”
Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans (2010, background): “Such replay phenomena have been found to occur during sleep (9, 18–20) but also during postencoding waking states (16, 17).”
Are spatial memories strengthened in the human hippocampus during slow wave sleep? (2004, unknown): “Here, using regional cerebral blood flow meation in their firing during NREM sleep when the animal surements, we show that, in humans, hippocampal is spatially confined to the relevant location during the areas that are activated during route learning in a virpreceding waking periods (Kudrimoti et a”