Increased sleep spindles in regions engaged during motor learning predict memory consolidation

Sleep spindles play a critical role in sleep-dependent memory consolidation. Although spindles can occur widely across the cortex, they are often focal. Focal spindles may promote plasticity in distinct circuits to consolidate specific memory types. In this study, we simultaneously acquired EEG and magnetoencephalography (MEG) data from 25 healthy adults (6 female) during daytime naps to investigate whether learning the finger tapping Motor Sequence Task (MST) preferentially increases spindle density (#/min) within cortical regions engaged during task performance and whether these task-related spindle increases predict performance improvement measured after the nap. We employed a novel algorithm to project EEG/MEG signals into source space using anatomical constraints from MRI, and detected spindles in cortical regions. Compared with a Baseline nap, MST training preferentially increased spindle density in regions engaged while learning, which in turn predicted post-nap performance improvement. Learning during training and post-nap improvement were not correlated, suggesting that they reflect discrete processes. They also had different neural correlates. Whereas learning during training correlated with spindle density increases in motor execution regions, post-nap improvement correlated with increases in motor planning regions. We speculate that spindles in motor execution regions represent the memory, while those in planning regions enhance future performance. Our findings demonstrate that spindle expression is influenced by prior learning, and support the theory that spindles in task-related regions promote the neural plasticity necessary for motor memory consolidation. We propose that spindles in task-related regions may be more sensitive biomarkers of learning and sleep-dependent memory consolidation than those occurring elsewhere. Significance Statement Sleep spindles, brain rhythms necessary for consolidating new memories, are deficient in several disorders and are tractable treatment targets. Although spindles can occur widely across the cortex, they are frequently regionally specific. In this study, using EEG and magnetoencephalography (MEG), we found that motor learning preferentially increases spindles in cortical regions engaged during learning and that these regionally specific increases predict performance improvement measured after sleep. Our findings demonstrate that spindle expression is influenced by prior learning, and support the theory that spindles in regions engaged during learning promote the brain plasticity necessary for motor memory consolidation. We propose that spindles in task-related regions may be more sensitive indicators of new learning and sleep-dependent memory consolidation than those occurring elsewhere.