Abstract
Executing memory-guided behavior requires storage of information about experience and later recall of that information to inform choices. Awake hippocampal replay, when hippocampal neural ensembles briefly reactivate a representation related to prior experience, has been proposed to critically contribute to these memory-related processes. However, it remains unclear whether awake replay contributes to memory function by promoting the storage of past experiences, facilitating planning based on evaluation of those experiences, or both. We designed a dynamic spatial task that promotes replay before a memory-based choice and assessed how the content of replay related to past and future behavior. We found that replay content was decoupled from subsequent choice and instead was enriched for representations of previously rewarded locations and places that had not been visited recently, indicating a role in memory storage rather than in directly guiding subsequent behavior.
Highlights
Central to cognition, memory allows us to store representations of experience and to later use those representations to inform our future actions
Most sharp-wave ripples (SWRs) contain interpretable spatial content Because replay events tend to coincide with SWRs, we identified SWRs using a permissive threshold to ensure that we were examining a large fraction of the actual replay events in the dorsal hippocampus (STAR Methods)
We found that more than 90% of SWRs decoded to the same maze segment, and our main results were unchanged with the use of this simplified decoding approach
Summary
Memory allows us to store representations of experience and to later use those representations to inform our future actions. Both of these processes engage a brain structure called the hippocampus (Buckner, 2010; Milner et al, 1998; Squire, 1992), and both have been hypothesized to rely on a pattern of neural activity known as hippocampal replay. The pattern of neural activity corresponding to a past experience can be reactivated in a time-compressed manner (Buzsaki, 2015; Carr et al, 2011; Joo and Frank, 2018). The role of replay during waking is less clear, : while awake SWRs have been linked to learning (Fernandez-Ruiz et al, 2019; Igata et al, 2021; Jadhav et al, 2012; Nokia et al, 2012), how the content of those SWRs contributes to memoryrelated information processing remains controversial
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