Awake replay of remote experiences in the hippocampus

By Mattias P. Karlsson, Loren M. Frank. 2009

747 citations recorded by the source corpus.

Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal-neocortical networks. Replay is present during both sleep and waking behavior, but although sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here, we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was more robust when the rat had recently been in motion than during extended periods of quiescence. Our results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, 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): “Furthermore, many existing artificial replay implementations do not purge their memory buffer, which is not consistent with biology (Nádasdy et al., 1999; Karlsson & Frank, 2009) and do not have a notion of waking (streaming/online) learning.”
Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, neutral): “In contrast, as we argue below, awake replay is consistent with the patterns of activity necessary to support a hippocampal retrieval mechanism, indicating that hippocampal replay during the awake state could be a common neural mechanism for both consolidation and retrieva”
Lifelong Generative Modeling (2017, background): “While strongly motivated by biological rehearsal processes [119, 53, 58, 110], these generative replay strategies fail to efficiently use previous learning and simply re-learn each new joint task from scratch.”
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…”
About sleep's role in memory. (2013, background): “In addition to current learning experience, more remote learning experiences are also reactivated, indicating that wake reactivations do not depend on the actual perceptual input (621).”
Cellular and Systems Consolidation of Declarative Memory (2017, background): “NREM sleep is obviously one such period, but neural replay has also been found to occur during periods of quiet wake (Karlsson and Frank 2009).”
Human Replay Spontaneously Reorganizes Experience (2019, background): “The rest period was intended to be analogous to the awake resting periods in rodent studies in which hippocampal replay has been observed in spatial tasks (Davidson et al., 2009; Foster and Wilson, 2006; Karlsson and Frank, 2009).”
Generative Predictive Codes by Multiplexed Hippocampal Neuronal Tuplets. (2018, neutral): “This approach estimated a rather limited and rigid predictive and recall capacity of the hippocampal network for spatial navigation and memory (Azizi et al., 2013; Dragoi and Tonegawa, 2013b; Karlsson and Frank, 2009; Lee and Wilson, 2002; Silva et al., 2015), in apparent contrast with the increased”
Integrating memories to guide decisions (2015, background): “Indeed, similar retrospective ‘‘replay’’ phenomena have also been reported, in which place cells represent positions where the animal has been in the past, including reverse replay behind the animal [35], or replaying spatially remote routes while the animal is pausing or asleep [36,37].”
Hippocampal “time cells” bridge the gap in memory for discontiguous events (2011, positive): “…experimental studies on both humans (Gelbard-Sagiv et al., 2008; Paz et al., 2010) and animals (Louie and Wilson, 2001; Foster and Wilson, 2006; Karlsson and Frank, 2009; Davidson et al., 2009) have shown that hippocampal neuronal ensembles ''replay'' specific event representations following…”
The restless engram: consolidations never end. (2012, background): “Such replay is observed time locked either to an immediate experience (Foster & Wilson 2006, Csicsvari et al. 2007, Diba & Buzsaki 2007) or to a spatially and temporally remote one (Davidson et al. 2009, Karlsson & Frank 2009).”