Abstract
Storing temporal sequences of events (i.e., sequence memory) is fundamental to many cognitive functions. However, it is unknown how the sequence order information is maintained and represented in working memory and its behavioral significance, particularly in human subjects. We recorded electroencephalography (EEG) in combination with a temporal response function (TRF) method to dissociate item-specific neuronal reactivations. We demonstrate that serially remembered items are successively reactivated during memory retention. The sequential replay displays two interesting properties compared to the actual sequence. First, the item-by-item reactivation is compressed within a 200 - 400 ms window, suggesting that external events are associated within a plasticity-relevant window to facilitate memory consolidation. Second, the replay is in a temporally reversed order and is strongly related to the recency effect in behavior. This fast-backward replay, previously revealed in rat hippocampus and demonstrated here in human cortical activities, might constitute a general neural mechanism for sequence memory and learning.
Highlights
Storing and retrieving temporal sequences of events, a capacity shared across species, is crucial to many cognitive functions, including speech recognition, movement planning, and episodic memory (Doyon et al, 2003; Giraud and Poeppel, 2012)
We recorded EEG responses in human participants performing sequence memory tasks and employed a temporal response function (TRF) approach to probe the neuronal response that tracks each item of the temporal sequence during memory retention
Our results consistently demonstrate that individual items are successively reactivated, characterized by a sequence of alpha-band activities
Summary
Storing and retrieving temporal sequences of events (i.e., sequence memory), a capacity shared across species, is crucial to many cognitive functions, including speech recognition, movement planning, and episodic memory (Doyon et al, 2003; Giraud and Poeppel, 2012). Two core components – the content (items) and the ordinal information (temporal order) – of a sequence are vital to be encoded and maintained in working memory. Retention of the sequence order information in memory cannot solely rely on an overall enhancement of neural activity and presumably requires the temporally segregated representations of individual items. Theoretical models postulate that sequence memory is mediated by a theta-gamma coupled neuronal oscillatory mechanism (Jensen and Lisman, 2005; Lisman and Idiart, 1995), such that individual items of the list/sequence, encoded in gamma-band activities, occur at the different phases of a theta-band rhythm.
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