Summary
Because of the purported critical role of cerebellar lobule HVI in classical conditioning of the nictitating membrane response of the rabbit, we recorded extracellularly from HVI Purkinje cells (PCs) during differential conditioning. Rabbits were trained using tonal conditioned stimuli (CSs) and stimulation of the periocular region as the unconditioned stimulus (US). Many PCs responded to the US, the most frequently observed response being a burst of simple spikes. PCs in HVI showed a variety of responses to CSs that were related to conditioned responses (CRs). The most frequently observed response was an increase in simple spikes correlated with CRs. The activity of many of these cells antedated CRs by 20–200 ms. A smaller proportion of cells exhibited inhibition of simple spike activity that antedated CRs. The existence of PCs that alter their firing before CRs suggests that they may be causally involved in this behavior, and in this respect they reinforce reports that lesions of HVI or its connections disrupt nictitating membrane CRs. Although complex spike activity was not generally related to the US or to CRs, a few PCs responded in relation to CRs with only complex spikes. In demonstrating CR-related activity in cerebellar PCs, this study supports theories of cerebellar learning such as those of Marr and Albus.
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References
Albus JS (1971) A theory of cerebellar function. Math Biosci 10: 25–61
Altman JA, Bechterev NN, Radionova EA, Shmigidina GN, Syka J (1976) Electrical responses of the auditory area of the cerebellar cortex to acoustic stimulation. Exp Brain Res 26: 285–298
Berthier NE, Moore JW (1983) The nictitating membrane response: an electrophysiological study of the abducens nerve and nucleus and the accessory abducens nucleus in the rabbit. Brain Res 253: 201–210
Buchtel HA, Iosif G, Marchesi GF, Provini L, Strata P (1972) Analysis of the activity evoked in the cerebellar cortex by stimulation of the visual pathways. Exp Brain Res 15: 278–288
Freeman JA (1970) Responses of cat cerebellar Purkinje cells to convergent inputs from cerebral cortex and peripheral sensory systems. Brain Res 33: 697–712
Fujita M (1982) Adaptive filter model of the cerebellum. Biol Cybern 45: 195–206
Gilbert PFC (1974) A theory of memory that explains the function and structure of the cerebellum. Brain Res 70: 1–18
Gilbert PFC, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128: 309–328
Highstein S, Coleman PD (1968) Responses of cerebellar vermis to binaural auditory stimulation. Brain Res 10: 470–473
Ikeda M (1979) Projections from the spinal and the principal sensory nuclei of the trigeminal nerve to the cerebellar cortex in the cat, as studied by retrograde transport of horseradish peroxidase. J Comp Neurol 209: 139–175
Ito M (1984) The cerebellum and neural control. Raven Press, New York
Ito M, Kano M (1982) Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett 33: 253–258
Ito M, Sakurai M, Tongroach P (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol (Lond) 324: 113–134
Lemon R (1984) Methods of neuronal recording in conscious animals. Wiley, New York, pp 268–271
Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202: 437–470
McCormick DA, Guyer PE, Thompson RF (1982) Superior cerebellar lesions selectively abolish the ipsilateral classically conditioned nictitating membrane/eyelid response of the rabbit. Brain Res 244: 347–350
McCormick DA, Lavond DG, Clark GA, Kettner RE, Rising CE, Thompson RF (1981) The engram found? Role of the cerebellum in classical conditioning of the nictitating membrane and eyelid response. Bull Psychon Soc, 18: 103–105
McCormick DA, Steinmetz JE, Thompson RF (1985) Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res 359: 120–130
McCormick DA, Thompson RF (1984a) Cerebellum: essential involvement in the classically conditioned eyelid response. Science, 223: 296–299
McCormick DA, Thompson RF (1984b) Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J Neurosci 4: 2811–2822
Miles TS, Wiesendanger M (1975a) Organisation of climbing fibre projections to the cerebellar cortex from trigeminal cutaneous afferents and from SI face area of the cat. J Physiol (Lond) 245: 409–424
Miles TS, Wiesendanger M (1975b) Climbing fibre inputs to cerebellar Purkinje cells from trigeminal cutaneous afferents and from the SI face area of the cerebral cortex in the cat. J Physiol (Lond) 245: 425–445
Moore JW (1972) Stimulus control: Studies of auditory generalization in rabbits. In: Black AH, Prokasy WF (eds) Classical conditioning II. Appleton Century Crofts, New York, pp 206–230
Moore JW, Desmond JE (1982) Latency of the nictitating membrane to periocular stimulation in unanesthetized rabbits. Physiol Behav 28: 1041–1046
Rosenfield ME, Moore JW (1983) Red nucleus lesions disrupt the classically conditioned nictitating membrane response in rabbits. Behav Brain Res 10: 393–398
Rosenfield ME, Moore JW (1985) Red nucleus lesions impair acquisition of the classically conditioned nictitating membrane response but not eye-to-eye savings or UR amplitude. Behav Brain Res 17: 77–81
Shofer RJ, Navhi MJ (1969) Firing patterns induced by sound in single units of the cerebellar cortex. Exp Brain Res 8: 327–345
Thach WT (1967) Somatosensory receptive fields of single units in cat cerebellar cortex. J Neurophysiol 30: 675–696
Woodruff-Pak DS, Lavond DG, Thompson RF (1985) Trace conditioning: abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations. Brain Res 348: 249–260
Yeo CH, Hardiman MJ, Glickstein M (1985a) Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp Brain Res 60: 87–98
Yeo CH, Hardiman MJ, Glickstein M (1985b) Classical conditioning of the nictitating membrane of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60: 99–113
Yeo CH, Hardiman MJ, Glickstein M (1985c) Classical conditioning of the nictitating membrane of the rabbit. III. Connections of cerebellar lobule HVI. Exp Brain Res 60: 114–126
Yeo CH, Hardiman MJ, Glickstein M (1986) Classical conditioning of the nictitating membrane of the rabbit. IV. Lesions of the inferior olive. Exp Brain Res (in press)
Yeo CH, Hardiman MJ, Glickstein M, Steele-Russell I (1982) Lesions of the cerebellar nuclei abolish the classically conditioned nictitating membrane response. Soc Neurosci Abstr 8: 22
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Berthier, N.E., Moore, J.W. Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp Brain Res 63, 341–350 (1986). https://doi.org/10.1007/BF00236851
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DOI: https://doi.org/10.1007/BF00236851