Historical Review of the Significance of the Cerebellum and the Role of Purkinje Cells in Motor Learning

Abstract: Classic studies of the cerebellum before the middle of the twentieth century established the structural entity of the cerebellum and characterized its function as enabling animals and humans to carry out smooth and accurate movements, even at a high speed and without visual feedback. In the 1960s, neuronal circuit structures of the cerebellum were analyzed in detail, which promoted computational approaches toward the study of neuronal network principles of the cerebellum. In the 1970s and 1980s, vestibulo‐ocular reflex adaptation, adaptive locomotion, eye blink conditioning, and learning in hand/arm movement were established as effective experimental paradigms for investigating neural mechanisms of cerebellar functions. In the 1980s, long‐term depression (LTD) was discovered and considered as a memory process in the cerebellum; in the 1990s, complex signal transduction processes underlying LTD were revealed. It was also in the 1980s that computational approaches were advanced for modeling control system functions of the cerebellum. Currently, there are two alternative models proposed for VOR adaptation. In this decade, we envisage new developments toward the fusion of knowledge of the cerebellum at molecular and cellular levels and those in systems and computation. Studies of LTD will play a key role in pursuing this direction.

[1]  Masao Ito,et al.  Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells , 1982, The Journal of physiology.

[2]  R. F. Thompson,et al.  Cerebellum: essential involvement in the classically conditioned eyelid response. , 1984, Science.

[3]  J SZENTAGOTHAI,et al.  THE USE OF DEGENERATION METHODS IN THE INVESTIGATION OF SHORT NEURONAL CONNEXIONS. , 1965, Progress in brain research.

[4]  John C. Eccles,et al.  Postsynaptic and Presynaptic Inhibitory Actions in the Spinal Cord , 1963 .

[5]  Masao Ito,et al.  Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex , 1982, Neuroscience Letters.

[6]  Masao Ito Cerebellar learning in the vestibulo–ocular reflex , 1998, Trends in Cognitive Sciences.

[7]  R. Llinás,et al.  Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum , 2004, Experimental Brain Research.

[8]  Frank Rosenblatt,et al.  PRINCIPLES OF NEURODYNAMICS. PERCEPTRONS AND THE THEORY OF BRAIN MECHANISMS , 1963 .

[9]  M. Sakurai Synaptic modification of parallel fibre‐Purkinje cell transmission in in vitro guinea‐pig cerebellar slices. , 1987, The Journal of physiology.

[10]  C. I. de Zeeuw,et al.  A new combination of WGA-HRP anterograde tracing and GABA immunocytochemistry applied to afferents of the cat inferior olive at the ultrastructural level , 1988, Brain Research.

[11]  M. Kawato,et al.  Exploration of Signal Transduction Pathways in Cerebellar Long-Term Depression by Kinetic Simulation , 2001, The Journal of Neuroscience.

[12]  G. Moruzzi,et al.  Cerebellar release phenomena , 1957 .

[13]  M. Ito,et al.  Long-term depression. , 1989, Annual review of neuroscience.

[14]  Professor Dr. John C. Eccles,et al.  The Cerebellum as a Neuronal Machine , 1967, Springer Berlin Heidelberg.

[15]  R. Baker,et al.  Cerebellar role in adaptation of the goldfish vestibuloocular reflex. , 1994, Journal of neurophysiology.

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

[17]  Masao Ito,et al.  The Cerebellar Modification of Rabbit's Horizontal Vestibulo-Ocular Reflex Induced by Sustained Head Rotation Combined with Visual Stimulation , 1974 .

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

[19]  Soichi Nagao,et al.  Location of efferent terminals of the primate flocculus and ventral paraflocculus revealed by anterograde axonal transport methods , 1997, Neuroscience Research.

[20]  M. Ito,et al.  Axon reflex activation of Deiters neurones from the cerebellar cortex through collaterals of the cerebellar afferents , 2004, Experimental Brain Research.

[21]  J. Eccles,et al.  The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum , 1966, The Journal of physiology.

[22]  S. Nagao,et al.  Behavior of floccular Purkinje cells correlated with adaptation of vestibulo-ocular reflex in pigmented rabbits , 2004, Experimental Brain Research.

[23]  D. Linden,et al.  Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. , 1999, Journal of neurophysiology.

[24]  Y. Hirata,et al.  Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. , 2001, Journal of neurophysiology.

[25]  R. L. Nó,et al.  VESTIBULO-OCULAR REFLEX ARC , 1933 .

[26]  Mitsuo Kawato,et al.  Computational study on monkey VOR adaptation and smooth pursuit based on the parallel control-pathway theory. , 2002, Journal of neurophysiology.

[27]  Masao Ito,et al.  Impulse discharge from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation , 1975, Brain Research.

[28]  A. L. Leiner,et al.  Does the cerebellum contribute to mental skills? , 1986, Behavioral neuroscience.

[29]  J. Szentágothai,et al.  Über den Ursprung der Kletterfasern des Kleinhirns , 1959, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[30]  M. Ito Cerebellar control of the vestibulo-ocular reflex--around the flocculus hypothesis. , 1982, Annual review of neuroscience.

[31]  D. Yanagihara,et al.  Nitric oxide plays a key role in adaptive control of locomotion in cat. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  C. Batini,et al.  Cerebellar nuclei and the nucleocortical projections in the rat: Retrograde tracing coupled to GABA and glutamate immunohistochemistry , 1992, The Journal of comparative neurology.

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

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

[35]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[36]  Chris I. De Zeeuw,et al.  Expression of a Protein Kinase C Inhibitor in Purkinje Cells Blocks Cerebellar LTD and Adaptation of the Vestibulo-Ocular Reflex , 1998, Neuron.

[37]  G. Jones,et al.  Extreme vestibulo‐ocular adaptation induced by prolonged optical reversal of vision , 1976, The Journal of physiology.

[38]  M. Kawato,et al.  A hierarchical neural-network model for control and learning of voluntary movement , 2004, Biological Cybernetics.

[39]  C. I. Zeeuw,et al.  Cerebellar LTD facilitates but is not essential for long-term adaptation of the vestibulo-ocular reflex. , 2002 .

[40]  Soichi Nagao,et al.  Contribution of oculomotor signals to the behavior of rabbit floccular Purkinje cells during reflex eye movements , 1991, Neuroscience Research.

[41]  G. Hesslow,et al.  Inhibition of the inferior olive during conditioned responses in the decerebrate ferret , 1996, Experimental Brain Research.

[42]  K. Matsunami,et al.  Synaptic excitation of red nucleus neurones by fibres from interpositus nucleus , 2004, Experimental Brain Research.

[43]  D. Zee,et al.  Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles , 2001, Experimental Brain Research.

[44]  M. Ito,et al.  Cerebellar long-term depression: characterization, signal transduction, and functional roles. , 2001, Physiological reviews.

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

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

[47]  J. Eccles,et al.  The inhibitory interneurones within the cerebellar cortex , 2004, Experimental Brain Research.

[48]  David A. Robinson,et al.  Gain changes of the cat's vestibulo-ocular reflex after flocculus deactivation , 2004, Experimental Brain Research.

[49]  C I De Zeeuw,et al.  Climbing fibre collaterals contact neurons in the cerebellar nuclei that provide a GABAergic feedback to the inferior olive. , 1997, Neuroscience.

[50]  M. Ito,et al.  Cerebellar inhibitory control of the vestibulo-ocular reflex investigated in rabbit IIIrd nucleus , 1972, Experimental Brain Research.

[51]  S G Lisberger,et al.  Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. , 2002, Journal of neurophysiology.

[52]  P. Jastreboff,et al.  A neuronal correlate in rabbit's cerebellum to adaptive modification of the vestibulo-ocular reflex , 1978, Brain Research.

[53]  F. A. Miles,et al.  Plasticity in the vestibulo-ocular reflex: a new hypothesis. , 1981, Annual review of neuroscience.

[54]  F. Crépel,et al.  Cellular mechanisms of cerebellar LTD , 1998, Trends in Neurosciences.

[55]  D. Linden,et al.  An evaluation of the nitric oxide/cGMP/cGMP-dependent protein kinase cascade in the induction of cerebellar long-term depression in culture , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  D. Armstrong,et al.  Complex spikes in Purkinje cells in the lateral vermis (b zone) of the cat cerebellum during locomotion. , 1987, The Journal of physiology.

[57]  D. Linden,et al.  Inositol-1,4,5-trisphosphate receptor-mediated Ca mobilization is not required for cerebellar long-term depression in reduced preparations. , 1998, Journal of neurophysiology.

[58]  O. Oscarsson,et al.  Spatial Distribution of Climbing and Mossy Fibre Inputs into the Cerebellar Cortex , 1976 .

[59]  Y. Miyashita Eye velocity responsiveness and its proprioceptive component in the floccular Purkinje cells of the alert pigmented rabbit , 2004, Experimental Brain Research.

[60]  J. G. Mcelligott,et al.  Effect of cerebellar inactivation by lidocaine microdialysis on the vestibuloocular reflex in goldfish. , 1998, Journal of neurophysiology.

[61]  J. Sanes,et al.  Can molecules explain long-term potentiation? , 1999, Nature Neuroscience.

[62]  E. Watanabe Role of the primate flocculus in adaptation of the vestibulo-ocular reflex , 1985, Neuroscience Research.

[63]  Masao Ito The molecular organization of cerebellar long-term depression , 2002, Nature Reviews Neuroscience.

[64]  D. Robinson Adaptive gain control of vestibuloocular reflex by the cerebellum. , 1976, Journal of neurophysiology.

[65]  M. Uno,et al.  The mode of cerebello-thalamic relay transmission investigated with intracellular recording from cells of the ventrolateral nucleus of cat's thalamus , 2004, Experimental Brain Research.

[66]  R. F. Thompson,et al.  Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. , 1998, Science.

[67]  Masao Ito Movement and thought: identical control mechanisms by the cerebellum , 1993, Trends in Neurosciences.

[68]  R. Dow THE EVOLUTION AND ANATOMY OF THE CEREBELLUM , 1942 .

[69]  Richard Apps,et al.  A Combined Retrograde Tracer and GABA‐immunocytochemical Study of the Projection from Nucleus Interpositus Posterior to the Posterior Lobe c2 Zone of the Cat Cerebellum , 1995, The European journal of neuroscience.

[70]  J. Yamada,et al.  Differences of the primate flocculus and ventral paraflocculus in the mossy and climbing fiber input organization , 1997, The Journal of comparative neurology.

[71]  Tatsuya Kimura,et al.  Cerebellar complex spikes encode both destinations and errors in arm movements , 1998, Nature.

[72]  U. Bhalla,et al.  Emergent properties of networks of biological signaling pathways. , 1999, Science.

[73]  Richard S. Sutton,et al.  Computational Schemes and Neural Network Models for Formation and Control of Multijoint Arm Trajectory , 1995 .

[74]  M. Kano,et al.  Long-term depression of parallel fibre synapses following stimulation of climbing fibres , 1985, Brain Research.

[75]  M. Dickinson,et al.  A long-term depression of AMPA currents in cultured cerebellar purkinje neurons , 1991, Neuron.

[76]  J. Jansen,et al.  Aspects of cerebellar anatomy , 1954 .