Deep sleep maintains learning efficiency of the human brain

It is hypothesized that deep sleep is essential for restoring the brain's capacity to learn efficiently, especially in regions heavily activated during the day. However, causal evidence in humans has been lacking due to the inability to sleep deprive one target area while keeping the natural sleep pattern intact. Here we introduce a novel approach to focally perturb deep sleep in motor cortex, and investigate the consequences on behavioural and neurophysiological markers of neuroplasticity arising from dedicated motor practice. We show that the capacity to undergo neuroplastic changes is reduced by wakefulness but restored during unperturbed sleep. This restorative process is markedly attenuated when slow waves are selectively perturbed in motor cortex, demonstrating that deep sleep is a requirement for maintaining sustainable learning efficiency

A Day Awake Attenuates Motor Learning-Induced Increases in Corticomotor Excitability

The "synaptic homeostasis hypothesis" proposes that the brain's capacity to exhibit synaptic plasticity is reduced during the day but restores when sleeping. While this prediction has been confirmed for declarative memories, it is currently unknown whether it is also the case for motor memories. We quantified practice-induced changes in corticomotor excitability in response to repetitive motor sequence training as an indirect marker of synaptic plasticity in the primary motor cortex (M1). Subjects either practiced a motor sequence in the morning and a new motor sequence in the evening, i.e., after a 12 h period of wakefulness (wake group); or they practiced a sequence in the evening and a new sequence in the morning, i.e., after a 12 h period including sleep (sleep group). In both wake and sleep groups motor training improved movement performance irrespective of the time of day. Learning a new sequence in the morning triggered a clear increase in corticomotor excitability suggesting that motor training triggered synaptic adaptation in the M1 that was absent when a new sequence was learned in the evening. Thus, the magnitude of the practice-induced increase in corticomotor excitability was significantly influenced by time of day while the magnitude of motor performance improvements were not. These results suggest that the motor cortex's potential to efficiently adapt to the environment by quickly adjusting synaptic strength in an activity-dependent manner is higher in the morning than in the evening

A Day Awake Attenuates Motor Learning-Induced Increases in Corticomotor Excitability

The “synaptic homeostasis hypothesis” proposes that the brain’s capacity to exhibit synaptic plasticity is reduced during the day but restores when sleeping. While this prediction has been confirmed for declarative memories, it is currently unknown whether it is also the case for motor memories. We quantified practice-induced changes in corticomotor excitability in response to repetitive motor sequence training as an indirect marker of synaptic plasticity in the primary motor cortex (M1). Subjects either practiced a motor sequence in the morning and a new motor sequence in the evening, i.e., after a 12 h period of wakefulness (wake group); or they practiced a sequence in the evening and a new sequence in the morning, i.e., after a 12 h period including sleep (sleep group). In both wake and sleep groups motor training improved movement performance irrespective of the time of day. Learning a new sequence in the morning triggered a clear increase in corticomotor excitability suggesting that motor training triggered synaptic adaptation in the M1 that was absent when a new sequence was learned in the evening. Thus, the magnitude of the practice-induced increase in corticomotor excitability was significantly influenced by time of day while the magnitude of motor performance improvements were not. These results suggest that the motor cortex’s potential to efficiently adapt to the environment by quickly adjusting synaptic strength in an activity-dependent manner is higher in the morning than in the evening

Deep sleep maintains learning efficiency of the human brain

It is hypothesized that deep sleep is essential for restoring the brain's capacity to learn efficiently, especially in regions heavily activated during the day. However, causal evidence in humans has been lacking due to the inability to sleep deprive one target area while keeping the natural sleep pattern intact. Here we introduce a novel approach to focally perturb deep sleep in motor cortex, and investigate the consequences on behavioural and neurophysiological markers of neuroplasticity arising from dedicated motor practice. We show that the capacity to undergo neuroplastic changes is reduced by wakefulness but restored during unperturbed sleep. This restorative process is markedly attenuated when slow waves are selectively perturbed in motor cortex, demonstrating that deep sleep is a requirement for maintaining sustainable learning efficiency

Reconsolidation of motor memories is a time-dependent process

Reconsolidation is observed when a consolidated stable memory is recalled, which renders it transiently labile and requires re-stabilization. Motor memory reconsolidation has previously been demonstrated using a three-day design: on day 1 the memory is encoded, on day 2 it is reactivated and experimentally manipulated, and on day 3 memory strength is tested. The aim of the current study is to determine specific boundary conditions in order to consistently degrade motor memory through reconsolidation paradigms. We investigated a sequence tapping task (n = 48) with the typical three-day design and confirmed that reactivating the motor sequence briefly (10 times tapping the learned motor sequence) destabilizes the memory trace and makes it susceptible to behavioral interference. By systematically varying the time delay between memory reactivation and interference while keeping all other aspect constant we found that a short delay (i.e., 20 s) significantly decreased performance on day 3, whereas performance was maintained or small (but not significant) improvements were observed for longer delays (i.e., 60 s). We also tested a statistical model that assumed a linear effect of the different time delays (0 s, 20 s, 40 s, 60 s) on the performance changes from day 2 to day 3. This linear model revealed a significant effect consistent with the interpretation that increasing time delays caused a gradual change from performance degradation to performance conservation across groups. These findings indicate that re-stabilizing motor sequence memories during reconsolidation does not solely rely on additional motor practice but occurs with the passage of time. This study provides further support for the hypothesis that reconsolidation is a time-dependent process with a transition phase from destabilization to re-stabilization

Correction: Author Correction: Deep sleep maintains learning efficiency of the human brain

This corrects the article DOI: 10.1038/ncomms15405