Central regulation of cerebellar climbing fibre input during motor learning

A forelimb-withdrawal classical conditioning paradigm was used in awake cats (n = 4) to investigate changes in transmission in climbing fibre (CF) pathways during motor learning. The conditioned stimulus was an auditory tone, while the unconditioned stimulus was a low-intensity, single or double (0.1 ms) electrical pulse applied to the ipsilateral superficial radial nerve. Microwires chronically implanted into the paravermal cerebellar cortex (lobule V) were used to record the CF field potentials evoked by nerve stimulation, and fields at 22 recording sites (9 C1, 7 C2 and 6 C3 zone sites) were monitored during the complete sequence of at least one training run (i.e. over a period of about 2-3 weeks of conditioning). At 19 sites (86%) conditioning led to a significant reduction in mean size of field. Similar reductions occurred at four sites studied over two successive training runs. At 10 sites (45%) there was a statistically significant increase prior to the reduction. The three sites that failed to exhibit a significant reduction were all located in the C1 zone. Controls showed that the changes in CF transmission were dependent on the animal being conditioned. The mean size of CF field for trials in which a conditioned EMG response was present (in either the cleidobrachialis or biceps muscle) was not significantly different from the mean size for trials in which a conditioned response was absent. Similarly, on a trial-by-trial basis, CF pathway excitability was not correlated with the conditioned EMG activity in the flexor muscles under study. Overall, the results demonstrate that (1) the capacity of spino-olivocerebellar pathways (SOCPs) to forward information to the cerebellar cortex can be altered by recent experience, (2) establishment of a conditioned forelimb flexor reflex to a tone reduces SOCP excitability at most but not all sites within a forelimb-related region of the cerebellar cortex, (3) the extent of reductions differ at different sites and some are preceded by transient increases, and (4) the changes in transmission may not be related to the conditioned movement. The implications of these findings for some key theories of cerebellar cortical function are discussed.