Abstract
SummaryHippocampal place cells encode an animal’s current position in space during exploration [1]. During sleep, hippocampal network activity recapitulates patterns observed during recent experience: place cells with overlapping spatial fields show a greater tendency to co-fire (“reactivation”) [2], and temporally ordered and compressed sequences of place cell firing observed during wakefulness are reinstated (“replay”) [3, 4, 5]. Reactivation and replay may underlie memory consolidation [6, 7, 8, 9, 10]. Compressed sequences of place cell firing also occur during exploration: during each cycle of the theta oscillation, the set of active place cells shifts from those signaling positions behind to those signaling positions ahead of an animal’s current location [11, 12]. These “theta sequences” have been linked to spatial planning [13]. Here, we demonstrate that, before weaning (post-natal day [P]21), offline place cell activity associated with sharp-wave ripples (SWRs) reflects predominantly stationary locations in recently visited environments. By contrast, sequential place cell firing, describing extended trajectories through space during exploration (theta sequences) and subsequent rest (replay), emerge gradually after weaning in a coordinated fashion, possibly due to a progressive decrease in the threshold for experience-driven plasticity. Hippocampus-dependent learning and memory emerge late in altricial mammals [14, 15, 16, 17], appearing around weaning in rats and slowly maturing thereafter [14, 15]. In contrast, spatially localized firing is observed 1 week earlier (with reduced spatial tuning and stability) [18, 19, 20, 21]. By examining the development of hippocampal reactivation, replay, and theta sequences, we show that the coordinated maturation of offline consolidation and online sequence generation parallels the late emergence of hippocampal memory in the rat.
Highlights
We first investigated the development of reactivation, defined as changes in cell pair firing correlations following exploration (Figure 1A; see STAR Methods)
We recorded 1,566 complex spike (CS) cells from region CA1 from 24 animals aged between post-natal day 17 (P17) and P32 as they ran in a familiar square open field environment (RUN) and during the rest phase immediately preceding (PRE-sleep) and following (POST-sleep) exploration, yielding a total dataset of 19,334 cell pairs
From P17 onward, the similarity of the place fields of CS cell pairs during RUN was significantly correlated with their co-activity during sharp-wave ripples (SWRs), selectively during POSTsleep
Summary
From P17 onward, the similarity of the place fields of CS cell pairs during RUN was significantly correlated with their co-activity during sharp-wave ripples (SWRs) (see STAR Methods), selectively during POSTsleep (but not during PRE-sleep; Figures 1B and 1C). Similar results are obtained when the similarity of cell pair RUN co-firing is assessed at the finer timescale of single theta cycles (Figure 1D). These results demonstrate that Hebbian plasticity between hippocampal CS cell pairs is present from the earliest ages tested in the rat: neurons that fire together during RUN show an increased propensity to closely timed co-firing during post-experience rest
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