Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Sleep promotes formation of Dendritic Spines


Science 6 June 2014:  Vol. 344  no. 6188  pp. 1173-1178

Sleep promotes branch-specific formation of dendritic spines after learning

Guang Yang,

Skirball Institute, Department of Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA.

Department of Anesthesiology, New York University School of Medicine, New York, NY 10016, USA.

Drug Discovery Center, Key Laboratory of Chemical Genomics, Peking University Shenzhen Graduate School, Shenzhen, 518055, China.


How sleep helps learning and memory remains unknown. We report in mouse motor cortex that sleep after motor learning promotes the formation of postsynaptic dendritic spines on a subset of branches of individual layer V pyramidal neurons.   New spines are formed on different sets of dendritic branches in response to different learning tasks and are protected from being eliminated when multiple tasks are learned.   Neurons activated during learning of a motor task are reactivated during subsequent non–rapid eye movement sleep, and disrupting this neuronal reactivation prevents branch-specific spine formation. These findings indicate that sleep has a key role in promoting learning-dependent synapse formation and maintenance on selected dendritic branches, which contribute to memory storage.

Sleep has an important role in learning and memory consolidation. During sleep, neurons involved in wakeful experiences are reactivated in multiple brain regions, and neuronal networks exhibit various patterns of rhythmic activity. Given the crucial function of neuronal activity in synaptic plasticity, sleep likely modulates synaptic connections that are important for long-term memory formation. Nevertheless, the role of sleep in experience-dependent changes of synaptic connections remains controversial. Overall synaptic strength and numerous synaptic proteins are up-regulated during wakefulness and down-regulated during slow-wave sleep. A net loss of synapses is found during sleep in the developing mouse cortex and in the invertebrate nervous system. These observations support the hypothesis that sleep is important for the downscaling of synaptic connectivity that has been potentiated during wakefulness. However, ocular dominance plasticity and cortical-evoked local field potential increase rather than decrease after a slow-wave sleep episode. The expression of several proteins required for synaptic plasticity increases during the early hours of sleep. Furthermore, the number of synapses increases during early development when animals sleep the most. Together, these studies support the opposing view that sleep promotes, rather than down-regulates, synaptic plasticity related to learning and memory.

We examined how sleep affects the remodeling of postsynaptic dendritic spines induced by motor learning in the mouse primary motor cortex. Rotarod motor learning increases dendritic spine formation on apical tuft dendrites of layer V pyramidal neurons in the motor cortex within 2 days. To investigate whether sleep is involved in this process, we first determined the time course of spine remodeling in mice that were trained to run forward on an accelerated rotating rod. Yellow fluorescent protein (YFP)–labeled dendrites in the hind limb region of the motor cortex were imaged in awake head-restrained mice before and in the hours after training with transcranial two-photon microscopy. The formation rate of new spines in trained mice was significantly higher within 6 hours after training and continued to increase within the first day when compared to that in untrained controls (P < 0.05). In contrast, rotarod training had no significant effect on the elimination rate of existing spines within 6 to 48 hours.

Sleep is widely believed to be important for 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. 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. 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, and its effectiveness in promoting spine formation may vary at different times of the day. Sleep reactivation could also allow the expression of specific genes critical for the growth of new synaptic connections. Future studies are needed to address these questions in order to better understand how sleep contributes to memory storage in the brain.

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