Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits

SummaryThe activity of neurons in the interposed and dentate nuclei of the cerebellum was investigated during differential classical conditioning of the rabbit eye blink/ nictitating membrane response. Forty-seven percent of the 165 cells in the study responded to the orbital stimulation used as the unconditioned stimulus (US). The latency distribution of US-elicited responses was bimodal with peaks at 7 and 19 ms. Twenty-one percent of the cells responded with short latencies to the tones used as conditioned stimuli (CSs). These cells typically responded to both the reinforced and nonreinforced CSs. Forty-one percent of the cells responded on conditioned response (CR) trials but not on trials without CRs. The average lead of the neural response to the CR was 71.4 ms. Cells that responded on CR trials were more likely to respond to the CSs, or to the CSs and the US, than cells that did not respond on CR trials. For about half of the cells that responded on CR trials the latency of response followed trial-by-trial variations of CR latency. For the remainder, the response was time-locked to CS-onset. Cells whose responses paralleled the CR may be involved in the initiation or modulation of the CR, while those whose responses were time-locked to the CS may be involved in sensory processing underlying the initiation of the movement. The pathways that may underlie the US- and CS-elicited responses are also discussed.

[1]  I. Darian‐Smith,et al.  A single‐neurone investigation of somatotopic organization within the cat's trigeminal brain‐stem nuclei , 1963, The Journal of physiology.

[2]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

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

[4]  S. Gilman Corticonuclear and Corticovestibular Projections of the Cerebellum. , 1970 .

[5]  J. Albus A Theory of Cerebellar Function , 1971 .

[6]  L. Aitkin,et al.  Responses of single units in cerebellar vermis of the cat to monaural and binaural stimuli. , 1975, Journal of neurophysiology.

[7]  S. T. Kitai,et al.  Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. I. Climbing fiber system , 1977, Brain Research.

[8]  G. Bishop,et al.  Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. II. Mossy fiber system , 1977, Brain Research.

[9]  L. Aitkin,et al.  Acoustic input to the lateral pontine nuclei , 1978, Hearing Research.

[10]  M. Ikeda 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 , 1979, Neuroscience Letters.

[11]  H. C. Richardson,et al.  Mossy and climbing fibre mediated responses evoked in the cerebellar cortex of the cat by trigeminal afferent stimulation. , 1979, The Journal of physiology.

[12]  F. A. Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. , 1980, Journal of neurophysiology.

[13]  D Marr,et al.  Theory of edge detection , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[14]  F. A. Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. IV. Electrophysiological observations in flocculus of adapted monkeys. , 1980, Journal of neurophysiology.

[15]  N. Tsukahara,et al.  Classical conditioning mediated by the red nucleus in the cat. , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  H. C. Richardson,et al.  Patterns of activity evoked in cerebellar interpositus nuclear neurones by natural somatosensory stimuli in awake cats , 1981, The Journal of physiology.

[17]  J. M. Gibson,et al.  Trigeminocerebellar mossy fiber branching to granule cell layer patches in the rat cerebellum , 1981, Brain Research.

[18]  David G. Lavond,et al.  Concomitant classical conditioning of the rabbit nictitating membrane and eyelid responses: Correlations and implications , 1982, Physiology & Behavior.

[19]  M. D. Egger,et al.  Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vagal nuclei , 1982, Brain Research.

[20]  G. A. Clark,et al.  Initial localization of the memory trace for a basic form of learning. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Rosa H. Huang,et al.  Projections from the cochlear nucleus to the cerebellum , 1982, Brain Research.

[22]  David A. McCormick,et al.  Superior cerebellar peduncle lesions selectively abolish the ipsilateral classically conditioned nictitating membrane/eyelid response of the rabbit , 1982, Brain Research.

[23]  J. W. Moore,et al.  Red nucleus lesions disrupt the classically conditioned nictitating membrane response in rabbits , 1983, Behavioural Brain Research.

[24]  Y. Lamarre,et al.  Fast ballistic arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. I. Activity of precentral cortical neurons. , 1983, Journal of neurophysiology.

[25]  J. Courville,et al.  Projections from the reticular formation of the medulla, the spinal trigeminal and lateral reticular nuclei to the inferior olive , 1983, Neuroscience.

[26]  Wally Welker,et al.  Fractured cutaneous projections to the granule cell layer of the posterior cerebellar hemisphere of the domestic cat , 1984, The Journal of comparative neurology.

[27]  D. Armstrong,et al.  Discharges of nucleus interpositus neurones during locomotion in the cat. , 1984, The Journal of physiology.

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

[29]  J. Fraissard,et al.  NMR study of 129Xe adsorbed on L, Z and ZSM zeolites , 1984 .

[30]  R. F. Thompson,et al.  Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  P. Strata Inferior Olive: Functional Aspects , 1984 .

[32]  L. Kruger,et al.  Projections of the rat trigeminal sensory nuclear complex demonstrated by multiple fluorescent dye retrograde transport , 1985, Brain Research.

[33]  T. Miles,et al.  Climbing fiber lesions disrupt conditioning of the nictitating membrane response in the rabbit , 1986, Brain Research.

[34]  Y. Lamarre,et al.  Activity of dentate neurons during arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. , 1986, Journal of neurophysiology.

[35]  D. Commenges,et al.  The formulae-relating slopes, correlation coefficients and variance ratios used to determine stimulus- or movement-related neuronal activity , 1986, Brain Research.

[36]  E. Dietrichs,et al.  The cerebellar nucleo-olivary and olivocerebellar nuclear projections in the cat as studied with anterograde and retrograde transport in the same animal after implantation of crystalline WGA-HRP. III. The interposed nuclei , 1986, Brain Research.

[37]  R. Burkard,et al.  Frequency sensitivities of auditory neurons in the cerebellum of the cat , 1986, Brain Research.

[38]  D. Tracey,et al.  Somatosensory nuclei in the brainstem of the rat: Independent projections to the thalamus and cerebellum , 1987, The Journal of comparative neurology.

[39]  J. W. Moore,et al.  Purkinje Cell Activity and the Conditioned Nictitating Membrane Response , 1987 .

[40]  J. Billard,et al.  The red nucleus activity in rats deprived of the inferior olivary complex , 1988, Behavioural Brain Research.

[41]  S G Lisberger,et al.  The neural basis for learning of simple motor skills. , 1988, Science.

[42]  J. Voogd,et al.  Anterograde tracing of the rat olivocerebellar system with phaseolus vulgaris leucoagglutinin (PHA‐L). Demonstration of climbing fiber collateral innervation of the cerebellar nuclei , 1989, The Journal of comparative neurology.

[43]  G. Lynch,et al.  The neurobiology of learning and memory , 1989, Cognition.

[44]  JOHN W. Moore,et al.  Single-unit activity in red nucleus during the classically conditioned rabbit nictitating membrane response , 1991, Neuroscience Research.

[45]  E. Dietrichs,et al.  The cerebellar nucleo-olivary and olivo-cerebellar nuclear projections in the cat as studied with anterograde and retrograde transport in the same animal after implantation of crystalline WGA-HRP , 1985, Anatomy and Embryology.

[46]  C. Evinger,et al.  A model system for motor learning: adaptive gain control of the blink reflex , 2004, Experimental Brain Research.

[47]  J. W. Moore,et al.  Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response , 2004, Experimental Brain Research.

[48]  E. Dietrichs,et al.  Cerebellar nuclear afferents — where do they originate? , 1987, Anatomy and Embryology.

[49]  R. F. Thompson,et al.  Reacquisition of classical conditioning after removal of cerebellar cortex , 2004, Experimental Brain Research.

[50]  M. Glickstein,et al.  Classical conditioning of the nictitating membrane response of the rabbit , 2004, Experimental Brain Research.

[51]  F. Walberg The trigemino-olivary projection in the cat as studied with retrograde transport of horseradish peroxidase , 2004, Experimental Brain Research.

[52]  M. Glickstein,et al.  Classical conditioning of the nictitating membrane response of the rabbit , 2004, Experimental Brain Research.