Sleep Promotes Branch-Specific Spine Formation and Long-Term Memory Storage After Motor Learning

Sleep is essential for learning and memory consolidation, but the underlying processes remain elusive. There are conflicting views as to whether non-REM sleep contributes to memory consolidation by either promoting or down-regulating synaptic plasticity (19–22, 29). By directly imaging postsynaptic dendritic spines over time in the mouse cortex, our results indicate that sleep after learning promotes new spine formation on different sets of apical tuft branches of individual layer V pyramidal neurons. Furthermore, this sleep-dependent, branch-specific spine formation facilitates new spine survival when animals learn different tasks. These findings suggest that sleep promotes learning-induced synapse formation to aid long-term memory storage.

Different motor learning tasks cause spine formation on different sets of dendritic branches. Furthermore, additional training without sleep could promote branch-specific formation (Fig. 2D). Thus, it appears that which set of dendritic branches forms new spines is determined by specific features (input or activity patterns) of a learning task, rather than by sleep. Our data suggest that reactivation of task-specific neurons during NREM sleep is involved in forming new synapses after learning, although definitive proof that reactivation causes synaptic formation would require simultaneous imaging of both reactivation and synapses in the same neurons over time. Neuronal reactivation during sleep may promote branch-specific spine formation in a manner similar to awake learning experiences (Fig. 2D), and its effectiveness in promoting spine formation may vary at different times of the day (fig. S8). Sleep reactivation could also allow the expression of specific genes critical for the growth of new synaptic connections (32, 33). Future studies are needed to address these questions in order to better understand how sleep contributes to memory storage in the brain.