Abstract
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.
Highlights
For motor learning, and most notably for sequence learning, it has been shown that while sleep is beneficial for consolidation and retention performance, when performance saturation was reached during prior training (Kvint et al, 2011), behavioral measurements of sequence learning capacity did not differ in the morning compared to the evening (Fischer et al, 2002; Walker et al, 2002; Brawn et al, 2010; Kvint et al, 2011; Sale et al, 2013)
Sleep Group In the sleep group, motor practice did not cause a significant increase of corticomotor excitability in the evening session (prepost × intensity interaction: F(4,36) = 0.45; p = 0.77) while a significant increase was observed during the following morning session (F(4,36) = 2.68; p < 0.05), i.e., after a night of sleep (Figure 3A)
The capacity to undergo synaptic plasticity was probed by measuring changes in corticomotor excitability in response to acquiring a finger sequence tapping task, a learning paradigm that is well-known to induce use-dependent plasticity in M1
Summary
The synaptic homeostasis hypothesis (Tononi and Cirelli, 2003, 2006) assumes that a net increase in synaptic strength occurs when awake due to long-term potentiation (LTP) triggered by learning (Muellbacher et al, 2002; Silva, 2003; Rosenkranz et al, 2007a) or due to synaptic plasticity reflecting statistical regularities of the environment experienced during wakefulness (Cirelli and Tononi, 2000; Tononi and Cirelli, 2001, 2003; Huber et al, 2013). Using a plausible computational model of sleep-dependent renormalization, it has been predicted that the human brain’s ability to form new memories is hereby renormalized in the morning following sleep (Olcese et al, 2010). In accordance with this latter prediction, behavioral studies testing the formation of declarative memories showed that sleep was beneficial for memory consolidation (Born et al, 2006; Gais et al, 2006) and that learning capacity was higher in the morning (i.e., after 12 h including sleep) than in the evening (i.e., after 12 h without sleep; Kvint et al, 2011). For motor learning, and most notably for sequence learning, it has been shown that while sleep is beneficial for consolidation and retention performance, when performance saturation was reached during prior training (Kvint et al, 2011), behavioral measurements of sequence learning capacity did not differ in the morning compared to the evening (Fischer et al, 2002; Walker et al, 2002; Brawn et al, 2010; Kvint et al, 2011; Sale et al, 2013)
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