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Journal of Neuroscience, Vol 13, 1708-1718, Copyright © 1993 by Society for Neuroscience
Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses
SP Perrett, BP Ruiz and MD Mauk
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston 77225.
Among the many issues surrounding the involvement of the cerebellum in
motor learning, the relative roles of the cerebellar cortex and cerebellar
nuclei in Pavlovian conditioning have been particularly difficult to
assess. While previous studies have investigated the effects of cerebellar
cortex lesions on the acquisition and retention of conditioned movements,
we have examined the effects of these lesions on the timing of Pavlovian
eyelid responses. The rationale for this approach arises from previous
studies indicating that this timing is a component of Pavlovian eyelid
responses that is learned and that involves temporal discrimination. To
permit within-animal comparisons, rabbits were trained to produce
differently timed responses to high- and low-frequency auditory conditioned
stimuli (CSs). Before the lesion the conditioned responses to both CSs were
appropriately timed--each peaked near the time at which the unconditioned
stimulus was presented for that CS. However, after the lesion both CSs
could elicit similarly timed conditioned responses that peaked
inappropriately at very short latencies. The changes in responses timing
were sensitive to the size of the lesion, particularly its rostral-caudal
extent. Similar results were obtained in animals trained with one CS,
indicating that the disruption of response timing is not related to
impaired auditory discrimination. Because response timing is learned and
therefore requires synaptic plasticity, these data suggest that there are
at least two sites of plasticity involved in the motor expression of
Pavlovian eyelid responses. Plasticity at one site is necessary for the
learned timing of conditioned responses, while plasticity at another site
is revealed by the inappropriately timed responses observed following
removal of the cerebellar cortex. This lesion-induced dissociation of the
expression of motor responses and their learned timing supports a synthesis
of competing views by suggesting that motor learning involves both the
cerebellar cortex and cerebellar nuclei. We hypothesize that motor learning
involves a decrease in strength of the granule cell-Purkinje cell synapses
(e.g., Ito and Kano, 1982) in the cerebellar cortex and an increase in
strength of the mossy fiber- cerebellar nuclei synapses (e.g., Racine et
al., 1986). Finally, these data suggest that the cerebellar cortex may
mediate the temporal discriminations that are necessary for the learned
timing of conditioned responses.
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