Sleep restores the potential to undergo learning-induced increases of corticomotor excitability: new evidence in line with the synaptic downscaling hypothesis

“Synaptic downscaling” is hypothesized to be an important process during sleep such that previously potentiated synapses are reset. This is necessary for the acquisition of new memories during subsequent wakefulness. Even though synaptic downscaling is an appealing concept, there is little experimental evidence available in humans. Here we measured training-induced changes in corticomotor excitability as a marker for a person’s capacity to undergo neuroplastic changes. In accordance with synaptic downscaling, we hypothesized that the neuroplastic potential would be reduced in the evening, but would be restored again after one night of sleep. Subjects (n=19) were assigned to one of two groups: the WAKE-group acquired a 5-element sequence at 8am and a different sequence at 8pm after a day awake, while the SLEEP-group first learned a sequence at 8pm and a second at 8am after a night of sleep. Neuroplasticity was quantified by measuring Input-Output (I/O) curves with transcranial magnetic stimulation (TMS) before and after the learning task. In the WAKE-group, repeated measures ANOVA revealed a significantly larger increase from pre- to post-learning in the morning than evening. Moreover, pre-learning excitability was higher in the evening than morning (p<.05). In the SLEEP-group, the opposite pattern of neuroplasticity was observed (p<.05) such that changes from pre- to post-learning were smaller in the evening than morning when tested after a sufficient amount of sleep. Behaviorally both groups improved significantly during training with no differences between groups or between learning sessions. In conclusion, our neural data are in line with the synaptic downscaling hypothesis and provide new evidence on the interaction between sleep and neuroplasticity. However, these neural effects were subtle and were not reflected in behavioral estimates of motor memory formation.status: publishe