Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation

By Dhakshin Ramanathan, T. Gulati, Karunesh Ganguly. 2015

168 citations recorded by the source corpus.

Despite many prior studies demonstrating offline behavioral gains in motor skills after sleep, the underlying neural mechanisms remain poorly understood. To investigate the neurophysiological basis for offline gains, we performed single-unit recordings in motor cortex as rats learned a skilled upper-limb task. We found that sleep improved movement speed with preservation of accuracy. These offline improvements were linked to both replay of task-related ensembles during non-rapid eye movement (NREM) sleep and temporal shifts that more tightly bound motor cortical ensembles to movements; such offline gains and temporal shifts were not evident with sleep restriction. Interestingly, replay was linked to the coincidence of slow-wave events and bursts of spindle activity. Neurons that experienced the most consistent replay also underwent the most significant temporal shift and binding to the motor task. Significantly, replay and the associated performance gains after sleep only occurred when animals first learned the skill; continued practice during later stages of learning (i.e., after motor kinematics had stabilized) did not show evidence of replay. Our results highlight how replay of synchronous neural activity during sleep mediates large-scale neural plasticity and stabilizes kinematics during early motor learning.

Subfields: Cognitive Neuroscience, Experimental and Cognitive Psychology

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Citations in the corpus

Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “Spiking activity from motor cortex during NREM sleep has firing patterns that are similar to those of recent learning (Ramanathan, Gulati, & Ganguly, 2015; Gulati, Guo, Ramanathan, Bodepudi, & Ganguly, 2017; Gulati, Ramanathan, Wong, & Ganguly, 2014).”
Sleep prevents catastrophic forgetting in spiking neural networks by forming a joint synaptic weight representation (2022, background): “It has been suggested that Rapid Eye Movement (REM) sleep supports the consolidation of non-declarative or procedural memories, while non-REM sleep supports the consolidation of declarative memories [16,21–23].”
Neural ensemble reactivation in rapid eye movement and slow-wave sleep coordinate with muscle activity to promote rapid motor skill learning (2020, background): “However, they are consistent with a similar study in which they did not report sequential replay following reach training [20].”
Can sleep protect memories from catastrophic forgetting? (2019, unknown): “In a recent animal study (Ramanathan et al., 2015) consolidation of the procedural (skilled upper-limb) memory depended on the bursts of spindle activity and the waves of slow oscillation during NREM sleep.”
Cellular and Systems Consolidation of Declarative Memory (2017, background): “…al. 2004), VTA (Gomperts et al. 2015), olfactory/prefrontal/visual/motor cortex (Barnes and Wilson 2014; Ji and Wilson 2007; Peyrache et al. 2009; Ramanathan et al. 2015; Yang et al. 2014) and disrupting sharp-wave-ripples and thus replay during sleep leads to a deficit in hippocampal led…”