Learning-Dependent Synaptic Modifications in the Cerebellar Cortex of the Adult Rat Persist for at Least Four Weeks

Several experiments have demonstrated increased synapse number within the cerebellar cortex in association with motor skill learning but not with motor activity alone. The persistence of these synaptic changes in the absence of continued training was examined in the present experiment. Adult female rats were randomly allocated to either an acrobatic condition (AC) or a motor activity condition (MC). The AC animals were trained to traverse a complex series of obstacles, and each AC animal was pair-matched with an MC animal that traversed an obstacle-free runway. These animals were further assigned to one of three training conditions. Animals in the EARLY condition were trained for 10 consecutive days before being killed, animals in the DELAY condition received the same 10 d of training followed by a 28 d period without training, and animals in the CONTINUOUS condition were trained for the entire 38 d. Unbiased stereological techniques were used to obtain estimates of the number of synapses per Purkinje cell within the cerebellar paramedian lobule. Results showed the AC animals to have significantly more synapses per Purkinje cell than the MC animals in all three training conditions. There were no differences in the number of synapses per Purkinje cell among the EARLY, DELAY, and CONTINUOUS conditions. These data demonstrate that both the motor skills and the increases in synapse number presumed to support them persist in the absence of continued training.

[1]  W. Greenough,et al.  Persistence of visual cortex dendritic alterations induced by postweaning exposure to a "superenriched" environment in rats. , 1986, Behavioral neuroscience.

[2]  P. Bhide,et al.  The effects of a lengthy period of environmental diversity on well‐fed and previously undernourished rats. II. Synapse‐to‐neuron ratios , 1984, The Journal of comparative neurology.

[3]  W. Greenough,et al.  Reach training selectively alters dendritic branching in subpopulations of layer II–III pyramids in rat motor-somatosensory forelimb cortex , 1989, Neuropsychologia.

[4]  D. Forgays,et al.  Crucial periods for free-environmental experience in the rat. , 1962, Journal of Comparative and Physiological Psychology.

[5]  B. Cragg,et al.  Estimation of the number of synapses in a volume of nervous tissue from counts in thin sections by electron microscopy , 1974, Journal of neurocytology.

[6]  C. Davies,et al.  Effects of differential environments on the cerebral anatomy of rats as a function of previous and subsequent housing conditions , 1984, Experimental Neurology.

[7]  E. Kandel,et al.  Structural changes accompanying memory storage. , 1993, Annual review of physiology.

[8]  C. H. Bailey,et al.  Time course of structural changes at identified sensory neuron synapses during long-term sensitization in Aplysia , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  David A. McCormick,et al.  Ipsilateral cerebellar lesions prevent learning of the classically conditioned nictitating membrane/eyelid response , 1982, Brain Research.

[10]  J. Larson,et al.  Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. , 1985, Behavioral and neural biology.

[11]  J. Kleim,et al.  Synaptogenesis and FOS Expression in the Motor Cortex of the Adult Rat after Motor Skill Learning , 1996, The Journal of Neuroscience.

[12]  T. Ebner,et al.  Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. , 1992, Journal of neurophysiology.

[13]  W. Greenough,et al.  Motor-Skill Learning: Changes in Synaptic Organization of the Rat Cerebellar Cortex , 1996, Neurobiology of Learning and Memory.

[14]  C. H. Bailey,et al.  The anatomy of a memory: convergence of results across a diversity of tests , 1988, Trends in Neurosciences.

[15]  D. Lavond,et al.  Lesions of the cerebellar interpositus nucleus abolish both nictitating membrane and eyelid EMG conditioned responses , 1990, Brain Research.

[16]  W. Greenough,et al.  Exercise and the Brain: Angiogenesis in the Adult Rat Cerebellum after Vigorous Physical Activity and Motor Skill Learning , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[17]  M. Diamond,et al.  The effects of an enriched environment on the histology of the rat cerebral cortex , 1964, The Journal of comparative neurology.

[18]  W. Greenough,et al.  Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries , 1987, Brain Research.

[19]  D. C. Sterio The unbiased estimation of number and sizes of arbitrary particles using the disector , 1984, Journal of microscopy.

[20]  C. H. Bailey,et al.  Morphological basis of long-term habituation and sensitization in Aplysia. , 1983, Science.

[21]  J. Yu,et al.  Brain Mechanisms Underlying Motor Skill Learning in the Rat , 1990, American journal of physical medicine & rehabilitation.

[22]  D. Forgays,et al.  The nature of the effect of free-environmental experience in the rat. , 1952, Journal of comparative and physiological psychology.

[23]  W. Greenough,et al.  Lateralized effects of monocular training on dendritic branching in adult split-brain rats , 1982, Brain Research.

[24]  E. Bennett,et al.  Effects of environmental complexity and training on brain chemistry and anatomy: a replication and extension. , 1962, Journal of comparative and physiological psychology.

[25]  W. Greenough,et al.  Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[26]  W. Greenough,et al.  Glial hypertrophy is associated with synaptogenesis following motor‐skill learning, but not with angiogenesis following exercise , 1994, Glia.

[27]  H J Gundersen,et al.  Total number of neurons and glial cells in human brain nuclei estimated by the disector and the fractionator , 1988, Journal of microscopy.

[28]  W. Greenough,et al.  Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron , 1985, Brain Research.

[29]  F. Volkmar,et al.  Rearing Complexity Affects Branching of Dendrites in the Visual Cortex of the Rat , 1972, Science.

[30]  W. T. Thach,et al.  Purkinje cell activity during motor learning , 1977, Brain Research.

[31]  F. Volkmar,et al.  Maze training effects on dendritic branching in occipital cortex of adult rats. , 1979, Behavioral and neural biology.

[32]  M R Rosenzweig,et al.  Effects of differential experience on dendritic spine counts in rat cerebral cortex. , 1973, Journal of comparative and physiological psychology.

[33]  T. Vilis,et al.  A Cerebellar-dependent Efference Copy Mechanism for Generating Appropriate Muscle Responses to Limb Perturbations , 1984 .