Abstract
BackgroundIncreasing evidence demonstrates that motor-skill memories improve across a night of sleep, and that non-rapid eye movement (NREM) sleep commonly plays a role in orchestrating these consolidation enhancements. Here we show the benefit of a daytime nap on motor memory consolidation and its relationship not simply with global sleep-stage measures, but unique characteristics of sleep spindles at regionally specific locations; mapping to the corresponding memory representation.Methodology/Principal FindingsTwo groups of subjects trained on a motor-skill task using their left hand – a paradigm known to result in overnight plastic changes in the contralateral, right motor cortex. Both groups trained in the morning and were tested 8 hr later, with one group obtaining a 60–90 minute intervening midday nap, while the other group remained awake. At testing, subjects that did not nap showed no significant performance improvement, yet those that did nap expressed a highly significant consolidation enhancement. Within the nap group, the amount of offline improvement showed a significant correlation with the global measure of stage-2 NREM sleep. However, topographical sleep spindle analysis revealed more precise correlations. Specifically, when spindle activity at the central electrode of the non-learning hemisphere (left) was subtracted from that in the learning hemisphere (right), representing the homeostatic difference following learning, strong positive relationships with offline memory improvement emerged–correlations that were not evident for either hemisphere alone.Conclusions/SignificanceThese results demonstrate that motor memories are dynamically facilitated across daytime naps, enhancements that are uniquely associated with electrophysiological events expressed at local, anatomically discrete locations of the brain.
Highlights
A growing corpus of literature continues to demonstrate that, following learning, additional ‘‘offline’’ memory improvements develop during sleep [1,2]
Considering sleep spindles – a defining electrophysiological signature of non-rapid eye movement (NREM) involving short (,1 ) synchronous burst of activity (12–15 Hz) – may represent candidate triggers of synaptic potentiation leading to neural plasticity [10,11,12], and that spindle activity is highest late in the night [13], this latter correlation was hypothesized to reflected an association between spindle activity and offline memory improvement [4]
While it is known that motor skill memories improve offline across a night sleep, and can correlate with global sleep-stage measures, using a nap paradigm, here we demonstrate that offline motor memory enhancement is proportional not with basic sleep stages, but with locally constrained increases in sleep-spindle activity in central regions of the learning hemisphere, relative to more non-specific activity in the non-learning hemisphere
Summary
A growing corpus of literature continues to demonstrate that, following learning, additional ‘‘offline’’ memory improvements develop during sleep [1,2]. Recent functional imaging data have demonstrated that these overnight motor memory improvements are associated with a systems-level, plastic reorganization within the brain, including a lateralized expansion and increased activation in the right primary motor cortex; contralateral to the hand (left) learning the motor skill memory [14]. Two groups of subjects trained on a motor-skill task using their left hand – a paradigm known to result in overnight plastic changes in the contralateral, right motor cortex Both groups trained in the morning and were tested 8 hr later, with one group obtaining a 60–90 minute intervening midday nap, while the other group remained awake. These results demonstrate that motor memories are dynamically facilitated across daytime naps, enhancements that are uniquely associated with electrophysiological events expressed at local, anatomically discrete locations of the brain
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