The Long-term Structural Plasticity of Cerebellar Parallel Fiber Axons and Its Modulation by Motor Learning

• DOI: 10.1523/jneurosci.3792-12.2013
• Publication Date: 2013-05-08T16:38:10Z
• Authors: Jennifer Carrillo; Shao-Ying Cheng; Kwang Woo Ko; Theresa A. Jones; Hiroshi Nishiyama
• Keywords: 0301 basic medicine; Neuronal Plasticity; Time Factors; Green Fluorescent Proteins; Mice, Transgenic; Axons; Electric Stimulation; Adenoviridae; Mice, Inbred C57BL; Mice; Purkinje Cells; 03 medical and health sciences; Nerve Fibers; Motor Skills; Cerebellum; Synapses; Animals; Learning

Presynaptic axonal varicosities, like postsynaptic spines, are dynamically added and eliminated even in mature neuronal circuitry. To study the role of this axonal structural plasticity in behavioral learning, we performed two-photonin vivoimaging of cerebellar parallel fibers (PFs) in adult mice. PFs make excitatory synapses on Purkinje cells (PCs) in the cerebellar cortex, and long-term potentiation and depression at PF-PC synapses are thought to play crucial roles in cerebellar-dependent learning. Time-lapse vital imaging of PFs revealed that, under a control condition (no behavioral training), ∼10% of PF varicosities appeared and disappeared over a period of 2 weeks without changing the total number of varicosities. The fraction of dynamic PF varicosities significantly diminished during training on an acrobatic motor skill learning task, largely because of reduced addition of new varicosities. Thus, this form of motor learning was associated with greater structural stability of PFs and a slight decrease in the total number of varicosities. Together with prior findings that the number of PF-PC synapses increases during similar training, our results suggest that acrobatic motor skill learning involves a reduction of some PF inputs and a strengthening of others, probably via the conversion of some preexisting PF varicosities into multisynaptic terminals.