Hippocampal Replay is Not a Simple Function of Experience

By Anoopum S. Gupta, Matthijs A. A. van der Meer, David S. Touretzky, A. David Redish. 2010

688 citations recorded by the source corpus.

Summary Replay of behavioral sequences in the hippocampus during sharp-wave-ripple-complexes (SWRs) provides a potential mechanism for memory consolidation and the learning of knowledge structures. Current hypotheses imply that replay should straightforwardly reflect recent experience. However, we find these hypotheses to be incompatible with the content of replay on a task with two distinct behavioral sequences (A&B). We observed forward and backward replay of B even when rats had been performing A for >10 minutes. Furthermore, replay of non-local sequence B occurred more often when B was infrequently experienced. Neither forward nor backward sequences preferentially represented highly-experienced trajectories within a session. Additionally, we observed the construction of never-experienced novel-path sequences. These observations challenge the idea that sequence activation during SWRs is a simple replay of recent experience. Instead, replay reflected all physically available trajectories within the environment, suggesting a potential role in active learning and maintenance of the cognitive map.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Neuroscience

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Citations in the corpus

Selective Experience Replay for Lifelong Learning (2018, background): “Neuroscience literature suggests that replay occurs most often when events are infrequent, and the breadth of replayed experiences are not limited to the most recent events experienced nor the current task being undertaken (Gupta et al. 2010).”
Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “An explicit demonstration of this effect was shown in a two-choice maze task, where replay in rats corresponded to paths that were experienced and shortcuts that were never experienced (Gupta, van der Meer, Touretzky, & Redish, 2010).”
Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, background): “The presence of both forward and reverse replay was verified in a recent study in which the animal's direction of travel along the track was restricted, resulting in experience almost exclusively in one directio”
About sleep's role in memory. (2013, background): “In a task requiring the rat to run back and forth on the same elevated linear track, replay in the reverse order occurred mainly at the end of a run, whereas replay in a forward direction transpired in the anticipatory period before a new run (288, 492).”
The successor representation in human reinforcement learning (2016, background): “Hippocampal replay processes help capture the topological structure of novel environments 33 and sequentially simulate and construct path to future goals 50 - beyond the animal’s direct experience - via forward and reverse replay 51 .”
Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility (2017, neutral): “…activity patterns correspond to representations of trajectories through space (Csicsvari et al., 2007; Davidson et al., 2009; Diba and Buzsáki, 2007; Foster and Wilson, 2006; Gupta et al., 2010; Jackson et al., 2006; Karlsson and Frank, 2009; Pfeiffer and Foster, 2013; Wu and Foster, 2014).”
DREAM Architecture: a Developmental Approach to Open-Ended Learning in Robotics (2020, neutral): “They may involve the replay of past events to consolidate learning [55, 56] or the exploration of new problem solving strategies [57, 58, 59].”
Sparse Attentive Backtracking: Long-Range Credit Assignment in Recurrent Networks (2017, background): “In particular, hippocampal recordings in rats indicate that brief sequences of prior experience are replayed both in the awake resting state and during sleep, both of which conditions are linked to memory consolidation and learning (Foster & Wilson, 2006; Davidson et al., 2009; Gupta et al., 2010).”
Episodic-like memory trace in awake replay of hippocampal place cell activity sequences (2015, background): “Contradicting with this hypothesis, growing evidence suggests that replays are not a simple function of experience (Gupta et al., 2010), but rather that reward outcomes enhance the reactivation of experiences (Singer and Frank, 2009) and that replays can depict future paths to remembered goals…”
The content of hippocampal “replay” (2018, background): “Powerful evidence in support of this notion came from experiments examining replay in rats exploring a two-choice maze (Gupta et al., 2010).”
Sparse Attentive Backtracking: Temporal CreditAssignment Through Reminding (2018, background): “…recordings in rats indicate that brief sequences of prior experience are replayed both in the awake resting state and during sleep, both of which conditions are linked to memory consolidation and learning (Foster & Wilson, 2006; Davidson et al., 2009; Gupta et al., 2010; Ambrose et al., 2016).”
The restless engram: consolidations never end. (2012, background): “As noted above, replay is not a simple function of experience (Gupta et al. 2010, Dragoi & Tonegawa 2011).”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “This view is compatible with the idea that a main function of SPW-Rs is to maintain the “matches” between world events and neuronal sequences (Gupta et al., 2010) and in the process snippets of brain computation breach into consciousness.”