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      Speed of time-compressed forward replay flexibly changes in human episodic memory

      , , ,
      Nature Human Behaviour
      Springer Nature

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          Abstract

          Remembering information from continuous past episodes is a complex task1. On the one hand, we must be able to recall events in a highly accurate way, often including exact timings. On the other hand, we can ignore irrelevant details and skip to events of interest. Here, we track continuous episodes consisting of different subevents as they are recalled from memory. In behavioural and magnetoencephalography data, we show that memory replay is temporally compressed and proceeds in a forward direction. Neural replay is characterized by the reinstatement of temporal patterns from encoding2,3. These fragments of activity reappear on a compressed timescale. Herein, the replay of subevents takes longer than the transition from one subevent to another. This identifies episodic memory replay as a dynamic process in which participants replay fragments of fine-grained temporal patterns and are able to skip flexibly across subevents.

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          Most cited references30

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          The phase of ongoing EEG oscillations predicts visual perception.

          Oscillations are ubiquitous in electrical recordings of brain activity. While the amplitude of ongoing oscillatory activity is known to correlate with various aspects of perception, the influence of oscillatory phase on perception remains unknown. In particular, since phase varies on a much faster timescale than the more sluggish amplitude fluctuations, phase effects could reveal the fine-grained neural mechanisms underlying perception. We presented brief flashes of light at the individual luminance threshold while EEG was recorded. Although the stimulus on each trial was identical, subjects detected approximately half of the flashes (hits) and entirely missed the other half (misses). Phase distributions across trials were compared between hits and misses. We found that shortly before stimulus onset, each of the two distributions exhibited significant phase concentration, but at different phase angles. This effect was strongest in the theta and alpha frequency bands. In this time-frequency range, oscillatory phase accounted for at least 16% of variability in detection performance and allowed the prediction of performance on the single-trial level. This finding indicates that the visual detection threshold fluctuates over time along with the phase of ongoing EEG activity. The results support the notion that ongoing oscillations shape our perception, possibly by providing a temporal reference frame for neural codes that rely on precise spike timing.
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            Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval.

            The hippocampus is required for the encoding, consolidation and retrieval of event memories. Although the neural mechanisms that underlie these processes are only partially understood, a series of recent papers point to awake memory replay as a potential contributor to both consolidation and retrieval. Replay is the sequential reactivation of hippocampal place cells that represent previously experienced behavioral trajectories and occurs frequently in the awake state, particularly during periods of relative immobility. Awake replay may reflect trajectories through either the current environment or previously visited environments that are spatially remote. The repetition of learned sequences on a compressed time scale is well suited to promote memory consolidation in distributed circuits beyond the hippocampus, suggesting that consolidation occurs in both the awake and sleeping animal. Moreover, sensory information can influence the content of awake replay, suggesting a role for awake replay in memory retrieval.
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              Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point.

              Neural ensembles were recorded from the CA3 region of rats running on T-based decision tasks. Examination of neural representations of space at fast time scales revealed a transient but repeatable phenomenon as rats made a decision: the location reconstructed from the neural ensemble swept forward, first down one path and then the other. Estimated representations were coherent and preferentially swept ahead of the animal rather than behind the animal, implying it represented future possibilities rather than recently traveled paths. Similar phenomena occurred at other important decisions (such as in recovery from an error). Local field potentials from these sites contained pronounced theta and gamma frequencies, but no sharp wave frequencies. Forward-shifted spatial representations were influenced by task demands and experience. These data suggest that the hippocampus does not represent space as a passive computation, but rather that hippocampal spatial processing is an active process likely regulated by cognitive mechanisms.
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                Author and article information

                Journal
                Nature Human Behaviour
                Nat Hum Behav
                Springer Nature
                2397-3374
                December 17 2018
                Article
                10.1038/s41562-018-0491-4
                30944439
                e9fe0b51-9f30-4e50-b78d-9c0cadb6535a
                © 2018

                http://www.springer.com/tdm

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