Rapid eye movement sleep contributes to the formation of new axonal varicosities in mouse cerebellar parallel fibers after motor training.

Synaptic structural plasticity is essential for the development, learning and memory. It is well established that sleep plays important roles in synaptic plasticity after motor learning. In cerebellar cortex, parallel fibers of granule cells make excitatory synapses to the dendrites of Purkinje cells. However, the synaptic structural dynamics between parallel and Purkinje cells after motor training and the function of sleep in cerebellar synaptic plasticity remain unclear. Here, we used two-photon microscopy to examine presynaptic axonal structural dynamics at parallel fiber-Purkinje cell synapses and investigated the effect of REM sleep in synaptic plasticity of mouse cerebellar cortex following motor training. We found that motor training induces higher formation of new axonal varicosities in cerebellar parallel fibers. Our results also indicate that calcium activities of granule cells significantly increase during REM sleep, and REM sleep deprivation prevents motor training-induced formation of axonal varicosities in parallel fibers, suggesting that higher calcium activity of granule cells was crucial for promoting newly formed axonal varicosities after motor training. Together, these findings reveal the effect of motor training on parallel fiber presynaptic structural modification and the important role of REM sleep in synaptic plasticity in cerebellar cortex.