Preplay of future place cell sequences by hippocampal cellular assemblies

By George Dragoi, S. Tonegawa. Nature, 2010

666 citations recorded by the source corpus.

During spatial exploration, hippocampal neurons show a sequential firing pattern in which individual neurons fire specifically at particular locations along the animal’s trajectory (place cells). According to the dominant model of hippocampal cell assembly activity, place cell firing order is established for the first time during exploration, to encode the spatial experience, and is subsequently replayed during rest or slow-wave sleep for consolidation of the encoded experience. Here we report that temporal sequences of firing of place cells expressed during a novel spatial experience occurred on a significant number of occasions during the resting or sleeping period preceding the experience. This phenomenon, which is called preplay, occurred in disjunction with sequences of replay of a familiar experience. These results suggest that internal neuronal dynamics during resting or sleep organize hippocampal cellular assemblies into temporal sequences that contribute to the encoding of a related novel experience occurring in the future.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/c5aa41dd6280576b7f3c5da983ba0c8f13c7c0d5

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Citations in the corpus

Episodic-like memory trace in awake replay of hippocampal place cell activity sequences (2015, background): “The sequential activation of place cell activity associated with SWRs can also represent paths where the animal has never experienced (Dragoi and Tonegawa, 2011; Dragoi and Tonegawa 2013a; 2013b; Ólafsdóttir et al., 2015).”
The restless engram: consolidations never end. (2012, background): “Moreover, Dragoi & Tonegawa (2011) reported that some of the replays in aware-rest states are “preplays,” i.e., sequences that match those subsequently recorded when the rats were running in a new place.”
Navigating cognition: Spatial codes for human thinking (2018, background): “Although it has been suggested that sequential activity might reflect inherent hippocampal dynamics (135, 136), other accounts highlight hippocampal interactions with state-space representations in frontal regions in sequence generation and action selection, as well as the role of striatal regions i”
Human Replay Spontaneously Reorganizes Experience (2019, background): “Abstract Position Representations Play in Sequences Prior to New Object Experience (‘‘Transfer Replay’’) In rodents, prior to experience with a novel environment, hippocampal place cells play out spontaneous trajectories, which later map onto real spatial trajectories when the environment is experie”
The Role of Hippocampal Replay in Memory and Planning (2018, background): “Comparisons of the observed and expected spike sequences can be made using rank-order correlations (for example [50,55,56]) but probability-based methods are more powerful.”
Hippocampal Reactivation of Random Trajectories Resembling Brownian Diffusion. (2019, background): “Competing lines of evidence suggest that sequence firing in replay is generated from either experiencedependent mechanisms or, alternatively, reflects hardwired predetermined assemblies (Dragoi and Tonegawa, 2011; Grosmark and Buzsáki, 2016; Shen and McNaughton, 1996; Silva et al., 2015).”
How Memory Replay in Sleep Boosts Creative Problem-Solving (2018, background): “Fascinatingly, recent work has demonstrated that novel (as yet untraveled) trajectories, which would allow an animal to reach food, are sometimes ‘preplayed’ by the hippocampus, potentially showing the neural basis of problem solving [78,79].”
Permutation Entropy and Its Main Biomedical and Econophysics Applications: A Review (2012, background): “For instance, spontaneous brain activity encompasses a set of dynamically switching states, which are continuously re-edited across the cortex [56], in a non-random way [57,58].”
Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration (2014, background): “…only replay previous events but may instead anticipate (‘‘preplay’’) those that will be triggered by future interactions with the environment, suggesting that spontaneous firing patterns can be recruited to make plans and encode newmemories (Dragoi and Tonegawa, 2011; Pfeiffer and Foster, 2013).”
On the link between conscious function and general intelligence in humans and machines (2022, background): “The term “preplay” has also been used in the literature to refer to the fact that the hippocampus recruits template-like trajectories of hippocampal activity to encode novel experiences Dragoi & Tonegawa (2011).”
About sleep's role in memory. (2013, result): “Interestingly, RA burst activity during sleep in some of these cases appeared to be more similar to that observed during singing after sleep than before sleep, suggesting a kind of “preplay” that occurs during sleep and creates new song features (323).”
Hippocampal place cells construct reward related sequences through unexplored space (2015, methodology): “Recently several studies have described ‘de novo preplay’—preplay of environments that have yet to be experienced (Dragoi and Tonegawa, 2011, 2013, 2013)—which is believed to reflect the activity of preconfigured cell ensembles (McNaughton et al., 1996) that subsequently become bound to sensory…”