Cortical Reactivation of Non-Spatial and Spatial Memory Representations Coordinate with Hippocampus to Form a Memory Dialogue

Abstract

Episodic memory depends on the association of diverse attribute representations that are distributed across the neocortex, and evidence suggests that these attributes are linked, at least initially, by the hippocampus, which orchestrates retrieval and the offline replay of experience during memory consolidation. The dynamics that characterize this hippocampal-cortical dialogue, however, are only partly understood. Although it was originally proposed that replay is initiated in CA3, with the spontaneous emission of sharp-wave ripple (SWR) bursts, increasing evidence suggests that cortex may seed the process with partial information, leading to pattern completion in CA3 and subsequent global reactivation of the episode. A recent study has shown that the secondary motor cortex (M2), among other areas, carries two distinct types of representations: place cell-like activity, which relies on an intact hippocampus for its development, and responses tied to visuo-tactile cues — the 'attributes' of the experience, which do not require the hippocampus. Using two-photon Ca2+imaging, while simultaneously acquiring LFP from the ipsilateral CA1, we assessed the interactions among cortical retrieval of visuo-tactile attributes of previous experiences in a virtual environment, hippocampal SWR, and the cortical reinstatement of the spatial aspects of the same experiences. During rest after the experience, two types of reactivation events occurred, which separately conveyed information about spatial trajectories and visuo-tactile attributes. Reactivation of attribute information preceded that of trajectories in relation to hippocampal SWRs. Furthermore, paired reactivations of cue and trajectory information supported similar features of previous experiences. These results are consistent with the hypothesis that cortical retrieval of non-spatial attributes of recent experience seeds hippocampal reactivation of associated spatial sequences, which is followed by retrieval of episodic memory traces.

Replay without sharp wave ripples in a spatial memory task

“…This is consistent with the finding that individual neurons in the prefrontal cortex exhibit activity during hippocampal ripples that is selective for which arm of a Y-maze is being replayed but not for individual locations within the arm (Berners-Lee et al, 2021). Likewise, VTA neurons have been shown to selectively fire at replayed reward locations during ripples (Gomperts et al, 2015), while both the retrosplenial and secondary motor cortices show selective activation to landmarks and cues during reactivations during rest (Chang et al, 2020; Chang et al, 2023). Taken together, these results suggest that what is broadcast from the hippocampus during ripples is a more narrowly restricted set of experiential content than replay, which could explain selective memory for salient experiences (LaBar & Phelps, 1998; Kensinger, 2009).…”

“…The copyright holder for this preprint (which this version posted May 14, 2024. ; https://doi.org/10.1101/2024.05. 13.593931 doi: bioRxiv preprint was not certified by peer review) is the author/funder. All rights reserved.…”

“…The copyright holder for this preprint (which this version posted May 14, 2024. ; https://doi.org/10.1101/2024.05. 13.593931 doi: bioRxiv preprint…”

“…Berners-Lee et al, 2021). Likewise, VTA neurons have been shown to selectively fire at replayed reward locations during ripples(Gomperts et al, 2015), while both the retrosplenial and secondary motor cortices show selective activation to landmarks and cues during reactivations during rest(Chang et al, 2020;Chang et al, 2023). Taken together, these results suggest that what is broadcast from the hippocampus during ripples is a more narrowly restricted set of experiential content than replay, which could explain selective memory for salient experiences (LaBar & Phelps, 1998;Kensinger, 2009).Our unique behavioral paradigm using repeated spatial and reward manipulations allowed us to probe the relationship between ripple fields and behavioral context.…”