The cerebellum is necessary for rabbit classical eyeblink conditioning with a non-somatosensory (photic) unconditioned stimulus

The present research investigated the acquisition of classically conditioned eyeblinks in rabbits using a light flash unconditioned stimulus (US), as well as the contribution of deep cerebellar nuclei to such an association. Two independent groups of animals experienced three phases of training: (1) pre-lesion delay conditioning using either a light- (Group 1) or an air puff-US (Group 2), (2) post-lesion testing of response performance, and (3) post-lesion acquisition to the opposite US. During the initial acquisition (720 trials), the groups did not differ with regard to their rate of learning or their overall level of responding. To assess the contribution of the cerebellum to the maintenance of responding, the interpositus nucleus was electrolytically lesioned and animals were given 8 days of additional training. Both groups exhibited a profound reduction in conditioned responding (CR) and showed no signs of recovery over the remainder of this phase (480 trials). Animals were then shifted to the opposite US (same eye) and given 12 days of training to assess the effect of interpositus lesions on the acquisition of CRs to a novel US. No learning was observed during this phase, regardless of whether animals experienced the light- or air puff-US. These results demonstrate: (1) the ability of a non-somatosensory stimulus to serve as a US during classical eyeblink conditioning; and (2) a common reliance on deep cerebellar nuclei for both somatosensory- and non-somatosensory-based reflexive motor learning. The findings are discussed in reference to the processing of conditioning stimuli within the brainstem-cerebellar circuitry that underlies eyeblink conditioning.

[1]  Richard F. Thompson,et al.  Effects of lidocaine injection in the interpositus nucleus and red nucleus on conditioned behavioral and neuronal responses , 1990, Brain Research.

[2]  R. F. Thompson,et al.  Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[3]  J. Delgado-García,et al.  Kinematic analyses of classically-conditioned eyelid movements in the cat suggest a brain stem site for motor learning , 1994, Neuroscience Letters.

[4]  R. Clark,et al.  Reacquisition of eyeblink classical conditioning following large cerebellar cortical lesions in dutch belted rabbits , 1994, Behavioural Brain Research.

[5]  T. Akaike,et al.  Electrophysiological analysis of the tecto-olivocerebellar (lobule VII) projection in the rat , 1985, Brain Research.

[6]  UCS PROPERTIES IN CLASSICAL CONDITIONING OF THE ALBINO RABBIT'S NICTITATING MEMBRANE RESPONSE. , 1965, Journal of experimental psychology.

[7]  N. Barmack,et al.  Multiple-unit activity evoked in dorsal cap of inferior olive of the rabbit by visual stimulation. , 1980, Journal of neurophysiology.

[8]  B J Anderson,et al.  Cerebellar and Brainstem Circuits Involved in Classical Eyeblink Conditioning , 1994, Reviews in the neurosciences.

[9]  J. Freeman Responses of cat cerebellar Purkinje cells to convergent inputs from cerebral cortex and peripheral sensory systems. , 1970, Journal of neurophysiology.

[10]  Masao Ito The Cerebellum And Neural Control , 1984 .

[11]  James A. Mortimer,et al.  Cerebellar responses to teleceptive stimuli in alert monkeys , 1975, Brain Research.

[12]  T. Akaike Spatial distribution of evoked potentials in the inferior olivary nucleus by stimulation of the visual afferents in the rat , 1986, Brain Research.

[13]  R. H. Steinberg,et al.  Oscillatory activity in the optic tract of cat and light adaptation. , 1966, Journal of neurophysiology.

[14]  Bernard G. Schreurs,et al.  US-US conditioning of the rabbit’s nictitating membrane response: Emergence of a conditioned response without alpha conditioning , 1990, Psychobiology.

[15]  A. Gruart,et al.  Discharge of identified deep cerebellar nuclei neurons related to eye blinks in the alert cat , 1994, Neuroscience.

[16]  M. C. Smith,et al.  CS-US interval and US intensity in classical conditioning of the rabbit's nictitating membrane response. , 1968, Journal of comparative and physiological psychology.

[17]  Joseph E. Steinmetz,et al.  A general-purpose computer system for behavioral conditioning and neural recording experiments , 1998 .

[18]  J. Simpson,et al.  Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. , 1973, Journal of neurophysiology.

[19]  J. Simpson,et al.  Climbing fiber activation of Purkinje cells in the flocculus by impulses transferred through the visual pathway. , 1972, Brain research.

[20]  R. F. Thompson,et al.  Classical conditioning in rabbits using pontine nucleus stimulation as a conditioned stimulus and inferior olive stimulation as an unconditioned stimulus , 1989, Synapse.