Consolidation of human skill linked to waking hippocampo-neocortical replay

Summary

The introduction of rest intervals interspersed with practice strengthens wakeful consolidation of skill. The mechanisms by which the brain binds discrete action representations into consolidated, highly temporally resolved skill sequences during waking rest are not known. To address this question, we recorded magnetoencephalography (MEG) during acquisition and rapid consolidation of a sequential motor skill. We report the presence of prominent, fast waking neural replay during the same rest periods in which rapid consolidation occurs. The observed replay is temporally compressed by approximately 20-fold relative to the acquired skill, is selective for the trained sequence, and predicts the magnitude of skill consolidation. Replay representations extend beyond the hippocampus and entorhinal cortex to the contralateral sensorimotor cortex. These results document the presence of robust hippocampo-neocortical replay supporting rapid wakeful consolidation of skill.

 

Introduction

The idiom “practice makes perfect” emphasizes intense practice's importance in skill acquisition. However, waking rest intervals interleaved with practice blocks (distributed practice) are crucial for skill memory consolidation, superior to continuous practice blocks (massed practice). Much of skill learning occurs offline during rest rather than actual practice. Micro-offline gains during waking rest indicate rapid skill memory consolidation, developing over shorter timescales than previously thought and significantly greater in magnitude than overnight consolidation requiring sleep. The brain binds sequences of discrete action representations into consolidated, temporally precise skills during waking rest, potentially through neural replay, a process of temporally compressed reactivation of neural activity patterns representing behavioral sequences during rest.

 

Results

Skill was evaluated using a keypress sequence task, with 36 practice periods interleaved with rest. Fast waking replay of skill sequences was detected during rest, temporally compressed by approximately 20-fold. Replay rates were highest during inter-practice rest, selective for the trained sequence, and correlated with rapid skill consolidation. Replay representations involved a mediotemporal-sensorimotor network.

 

Discussion

Waking replay in hippocampal and sensorimotor regions during rest periods supports memory consolidation. The replay is temporally compressed, increases rapidly after practice onset, is selective for trained sequences, and predicts skill consolidation. Waking replay reinforces hippocampus and neocortical associations learned during prior practice, relevant for improving subsequent performance and wakeful consolidation of skill. Limitations include potential mislabeling artifacts in classifier-based analysis.

 

Methods

Detailed methods include resource availability, experimental models, behavior tasks, MRI and MEG data acquisition, training and evaluation of keypress decoders, sequence replay detection, replay rate calculation, and replay network characterization.

 

KEY TERMINOLOGY

Wakeful Consolidation: The process of stabilizing and integrating a newly learned skill or information during periods of wakefulness.

Neural Replay: The reactivation of neural activity patterns representing a behavioral sequence during rest.

Magnetoencephalography (MEG): A neuroimaging technique for mapping brain activity by recording magnetic fields produced by electrical currents occurring naturally in the brain.

Hippocampo-neocortical Replay: Repetition of neural activity patterns involving both the hippocampus and the neocortex.

Temporal Compression: The phenomenon where replayed sequences are accelerated compared to their original performance duration.

Micro-offline Gains: Small, rapid improvements in skill performance occurring during short rest intervals between practice sessions.

Distributed Practice: Practice sessions interspersed with rest periods.

Massed Practice: Continuous practice sessions without rest intervals.

Skill Memory Consolidation: The process by which newly acquired skills are stabilized and stored in long-term memory.

Principal Component Analysis (PCA): A statistical procedure that transforms data into a set of orthogonal components, capturing the most variance in the data.

Link to Original Paper

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