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Roles of Sleep in the Learning and Memory of a Motor Skill in Mice

Wan-Kun Gong  Jian Ni  Lu Wang  Zhi-Li Huang  
【摘要】:The question of how sleep contributes to learning and memory is currently a hot topic in the sleep field and neurosciences.The role of sleep in explicit memory has been extensively studied,but whether the implicit memory will benefit from sleep remains unclear and controversial.The dorsal striatum,the primary input nucleus of the basal ganglia,is involved in motor control and motor learning,and is poised to be a hub for neuroplasticity.Our previous works show that the dorsal striatum play an important role in sleep-wake regulation.The striatum may be one of the targets associated with sleep and motor memory,that is,sleep may play a role in motor memory through the striatum.The acquisition and long-term retention of motor skills are essential in our daily lives.However,how sleep contributes to motor skill learning and consolidation is unknown.Firstly,we investigated the role of sleep on motor skill in mice.Mice were trained on the accelerating rotarod task to assess the acquisition,consolidation and retrieval of motor skill.Mice were subjected to 6-h total sleep deprivation(SD) in three stages of motor skill processing through the SD device.Then,we used c-Fos immunohistochemical staining technique in transgenic mice to search for striatal cell types.Finally,we used cell type specific pharmacogenetic manipulation and receptor type specific pharmacological approaches to study the mechanisms of sleep in the motor skill consolidation.With polygraphic recordings,we found that the SD device could significantly decrease both non-rapid movement(non-REM,NREM) and REM sleep during 6-h SD.More than 82% total sleep amount was deprived by SD devices,followed by sleep rebound.Then motor ability in mice was evaluated by open field test,pole test,stepping test and wire suspension.The results showed that SD didn't affect motor ability in mice.In the rotarod task,motor performance significantly improved in mice after 6-h SD immediately starting from training than sleeping control.In contrast,SD before training impaired motor skill consolidation while didn't affect motor skill learning.Subsequent 1-week SD(6 h per day) after training had no influence on motor skill retrieval.Moreover,using c-Fos expression as an indicator for neuronal activation,we found that SD increased the density of c-Fos-expressing neurons in dorsal media striatum more than in dorsal lateral striatum.Pharmacogenetic inhibition of dopamine D1 receptor(R)-MSNs in the dorsal media striatum counteracted effects of SD on motor skill consolidation,but not in thedorsal lateral striatum in D1 R-Cre mice.Using microinjection techniques,we found that intrastriatal injection of SCH23390(D1 R antagonist) after training prevented effects of SD on motor skill consolidation,while intrastriatal injection of raclopride(D2 R antagonist) had no influence.Intrastriatal injection of SKF38393(D1 R agonist) after training promoted motor skill consolidation.In addition,intrastriatal injection of D-AP5(NMDAR antagonist) after training abolished effects of SD on motor skill consolidation,while intrastriatal injection of CNQX(non-NMDAR antagonist) had no effect.These results indicated that 6-h wakefulness after motor skill training consolidates motor skills that strongly depend on D1 R/NMDAR in the dorsal media striatum.

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