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Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning.

ABSTRACT: Brain-machine interfaces can allow neural control over assistive devices. They also provide an important platform for studying neural plasticity. Recent studies have suggested that optimal engagement of learning is essential for robust neuroprosthetic control. However, little is known about the neural processes that may consolidate a neuroprosthetic skill. On the basis of the growing body of evidence linking slow-wave activity (SWA) during sleep to consolidation, we examined whether there is 'offline' processing after neuroprosthetic learning. Using a rodent model, we found that, after successful learning, task-related units specifically experienced increased locking and coherency to SWA during sleep. Moreover, spike-spike coherence among these units was substantially enhanced. These changes were not present with poor skill acquisition or after control awake periods, demonstrating the specificity of our observations to learning. Notably, the time spent in SWA predicted the performance gains. Thus, SWA appears to be involved in offline processing after neuroprosthetic learning.

SUBMITTER: Gulati T

PROVIDER: S-EPMC5568667 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning.

Gulati Tanuj T Ramanathan Dhakshin S DS Wong Chelsea C CC Ganguly Karunesh K

Nature neuroscience 20140706 8

Brain-machine interfaces can allow neural control over assistive devices. They also provide an important platform for studying neural plasticity. Recent studies have suggested that optimal engagement of learning is essential for robust neuroprosthetic control. However, little is known about the neural processes that may consolidate a neuroprosthetic skill. On the basis of the growing body of evidence linking slow-wave activity (SWA) during sleep to consolidation, we examined whether there is 'of ...[more]

PMID: 24997761

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Project description:BackgroundThere is evidence that slow wave sleep (SWS) promotes the consolidation of memories that are subserved by mediotemporal- and hippocampo-cortical neural networks. In contrast to implicit memories, explicit memories are accompanied by conscious (attentive and controlled) processing. Awareness at pre-sleep encoding has been recognized as critical for the off-line memory consolidation. The present study elucidated the role of task-dependent cortical activation guided by attentional control at pre-sleep encoding for the consolidation of hippocampus-dependent memories during sleep.MethodologyA task with a hidden regularity was used (Number Reduction Task, NRT), in which the responses that can be implicitly predicted by the hidden regularity activate hippocampo-cortical networks more strongly than responses that cannot be predicted. Task performance was evaluated before and after early-night sleep, rich in SWS, and late-night sleep, rich in rapid eye movement (REM) sleep. In implicit conditions, slow cortical potentials (SPs) were analyzed to reflect the amount of controlled processing and the localization of activated neural task representations.Principal findingsDuring implicit learning before sleep, the amount of controlled processing did not differ between unpredictable and predictable responses, nor between early- and late-night sleep groups. A topographic re-distribution of SPs indicating a spatial reorganization occurred only after early, not after late sleep, and only for predictable responses. These SP changes correlated with the amount of SWS and were covert because off-line RT decrease did not differentiate response types or sleep groups.ConclusionsIt is concluded that SWS promotes the neural reorganization of task representations that rely on the hippocampal system despite absence of conscious access to these representations.SignificanceOriginal neurophysiologic evidence is provided for the role of SWS in the consolidation of memories encoded with hippocampo-cortical interaction before sleep. It is demonstrated that this SWS-mediated mechanism does not depend critically on explicitness at learning nor on the amount of controlled executive processing during pre-sleep encoding.

Dataset Information

Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning.

Publications

Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning.

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