Learning to make predictions in the cerebellum may explain the anticipatory modulation of the vestibulo-ocular reflex (VOR) gain with vergence

Changes in the eye vergence modify the gain of the vestibuloocular reflex (VOR). In a previous dynamical model, this modulation was controlled by the cerebellum using vergence angle information (Coenen & Sejnowski; NIPS 96). However, during a vergence eye movement, the change in the VOR gain anticipates the vergence change (Snyder & King; Vision Res. 323. 92). We demonstrate here how our previous dynamical model and a predictive cerebellar model may be combined to explain these findings. In the predictive model, the cerebellum receives inputs from vergence-disparity cells in the cortex to construct a prediction of vergence angle. By replacing the regular vergence input in our previous dynamical model by the vergence prediction, results similar to the experimental anticipatory gain changes are observed. The inferior olive in the predictive cerebellar model is responsible for computing a prediction error and for selecting the Purkinje cells to be recruited for learning a particular prediction. The learning model is based on the least-mean square (LMS) algorithm to construct predictions from previous context information. This model is a special case of a more general predictive function for the cerebellum that may provide a consistent explanation for the apparently ubiquitous task participation of the cerebellum. We discuss briefly how this more general model may explain some experimental results observed in the cerebellum with positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). In conclusion, a predictive cerebellar model receiving vergence+parity cell inputs learns to predict the time course of vergence eye movement and successfully changes ihe VOR gain in anticipation of vergence changes. 3rd Joint Symposium on Neural Computation Proceedings 203 ,

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

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

[3]  D. Harriman CEREBELLAR CORTEX, CYTOLOGY AND ORGANIZATION , 1974 .

[4]  J. Voogd,et al.  The Human Central Nervous System , 1978, Springer Berlin Heidelberg.

[5]  R. Llinás,et al.  Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage‐dependent ionic conductances. , 1981, The Journal of physiology.

[6]  Richard S. Sutton,et al.  Neuronlike adaptive elements that can solve difficult learning control problems , 1983, IEEE Transactions on Systems, Man, and Cybernetics.

[7]  Peter Kabal,et al.  The Stability of Adaptive Minimum Mean Square Error Equalizers Using Delayed Adjustment , 1983, IEEE Trans. Commun..

[8]  L. Mays Neural control of vergence eye movements: convergence and divergence neurons in midbrain. , 1984, Journal of neurophysiology.

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

[10]  B. C. Motter,et al.  Responses of neurons in visual cortex (V1 and V2) of the alert macaque to dynamic random-dot stereograms , 1985, Vision Research.

[11]  L E Mays,et al.  Neural control of vergence eye movements: neurons encoding vergence velocity. , 1986, Journal of neurophysiology.

[12]  R. Llinás,et al.  Oscillatory properties of guinea‐pig inferior olivary neurones and their pharmacological modulation: an in vitro study. , 1986, The Journal of physiology.

[13]  B G Cumming,et al.  Disparity-induced and blur-induced convergence eye movement and accommodation in the monkey. , 1986, Journal of neurophysiology.

[14]  A. Klopf A neuronal model of classical conditioning , 1988 .

[15]  Michael G. Paulin,et al.  A Kalman filter theory of the cerebellum , 1988 .

[16]  J. Voogd,et al.  Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: Anterograde tracing combined with immunocytochemistry , 1989, The Journal of comparative neurology.

[17]  A. L. Leiner,et al.  Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? , 1989, Behavioral neuroscience.

[18]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[19]  Fuyun Ling,et al.  The LMS algorithm with delayed coefficient adaptation , 1989, IEEE Trans. Acoust. Speech Signal Process..

[20]  S. Lisberger,et al.  Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. , 1990, Journal of neurophysiology.

[21]  J. Keeler A dynamical system view of cerebellar function , 1990 .

[22]  G. Barnes,et al.  The mechanism of prediction in human smooth pursuit eye movements. , 1991, The Journal of physiology.

[23]  S Thorpe,et al.  Modulation of neural stereoscopic processing in primate area V1 by the viewing distance. , 1992, Science.

[24]  Karl J. Friston,et al.  Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  A. M. Smith,et al.  Responses of cerebellar Purkinje cells to slip of a hand-held object. , 1992, Journal of neurophysiology.

[26]  E. Courchesne,et al.  A new role for the cerebellum in cognitive operations. , 1992, Behavioral neuroscience.

[27]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[28]  W. M. King,et al.  Changes in vestibulo-ocular reflex (VOR) anticipate changes in vergence angle in monkey , 1992, Vision Research.

[29]  Fuyun Ling,et al.  Corrections to 'The LMS algorithm with delayed coefficient adaptation' , 1992, IEEE Trans. Signal Process..

[30]  M. Kawato,et al.  The cerebellum and VOR/OKR learning models , 1992, Trends in Neurosciences.

[31]  Terrence J. Sejnowski,et al.  Biologically Plausible Local Learning Rules for the Adaptation of the Vestibulo-Ocular Reflex , 1992, NIPS.

[32]  L. Snyder,et al.  Effect of viewing distance and location of the axis of head rotation on the monkey's vestibuloocular reflex. I. Eye movement responses. , 1992, Journal of neurophysiology.

[33]  Richard S. Sutton,et al.  Adapting Bias by Gradient Descent: An Incremental Version of Delta-Bar-Delta , 1992, AAAI.

[34]  Lawrence K. Cormack,et al.  Disparity tuning in mechanisms of human stereopsis , 1992, Vision Research.

[35]  C. Schor,et al.  A dynamic model of cross-coupling between accommodation and convergence: simulations of step and frequency responses. , 1992, Optometry and vision science : official publication of the American Academy of Optometry.

[36]  J. Bloedel Functional heterogeneity with structural homogeneity: How does the cerebellum operate? , 1992 .

[37]  I. Lampl,et al.  Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. , 1993, Journal of neurophysiology.

[38]  A. L. Leiner,et al.  Cognitive and language functions of the human cerebellum , 1993, Trends in Neurosciences.

[39]  M. Mauk,et al.  Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  C. Darlot The cerebellum as a predictor of neural messages—I. The stable estimator hypothesis , 1993, Neuroscience.

[42]  W. T. Thach,et al.  Preserved Simple and Impaired Compound Movement After Infarction in the Territory of the Superior Cerebellar Artery , 1993, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[43]  R. Llinás,et al.  On the cerebellum and motor learning , 1993, Current Opinion in Neurobiology.

[44]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[45]  S. Hyakin,et al.  Neural Networks: A Comprehensive Foundation , 1994 .

[46]  P. van Donkelaar,et al.  Interactions between the eye and hand motor systems: disruptions due to cerebellar dysfunction. , 1994, Journal of neurophysiology.

[47]  A. Canavan,et al.  Successive roles of the cerebellum and premotor cortices in trajectorial learning. , 1994, Neuroreport.

[48]  B. Schreurs,et al.  A functional anatomical study of associative learning in humans. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Cliff From animals to animats 3 : proceedings of the Third International Conference on Simulation of Adaptive Behavior , 1994 .

[50]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[51]  T. Sejnowski,et al.  A neural model of the cortical representation of egocentric distance. , 1994, Cerebral cortex.

[52]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. , 1994, Journal of neurophysiology.

[53]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

[54]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. , 1994, Journal of neurophysiology.

[55]  P. Strick,et al.  Activation of a cerebellar output nucleus during cognitive processing. , 1994, Science.

[56]  Michael A. Arbib,et al.  Modeling the role of cerebellum in prism adaptation , 1994 .

[57]  M. Mauk,et al.  Extinction of conditioned eyelid responses requires the anterior lobe of cerebellar cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  C. I. Zeeuw,et al.  Postsynaptic Targets of Purkinje Cell Terminals in the Cerebellar and Vestibular Nuclei of the Rat , 1995, The European journal of neuroscience.

[59]  Y Trotter,et al.  Cortical Representation of Visual Three-Dimensional Space , 1995, Perception.

[60]  I. Ohzawa,et al.  Receptive-field dynamics in the central visual pathways , 1995, Trends in Neurosciences.

[61]  Ronald S. Harwerth,et al.  Behavioral studies of local stereopsis and disparity vergence in monkeys , 1995, Vision Research.

[62]  T. Cizadlo,et al.  Short-term and long-term verbal memory: a positron emission tomography study. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[63]  T. Sejnowski,et al.  A Dynamical Model of Context Dependencies for the Vestibulo-Ocular Reflex , 1995, NIPS 1995.

[64]  Paul D. Gamlin,et al.  Single-unit activity in the primate nucleus reticularis tegmenti pontis related to vergence and ocular accommodation. , 1995, Journal of neurophysiology.

[65]  H. Tachibana,et al.  Event-related potentials in patients with cerebellar degeneration: electrophysiological evidence for cognitive impairment. , 1995, Brain research. Cognitive brain research.

[66]  T. Sejnowski,et al.  Learning and memory in the vestibulo-ocular reflex. , 1995, Annual review of neuroscience.

[67]  Richard S. Sutton,et al.  Reinforcement Learning with Replacing Eligibility Traces , 2005, Machine Learning.

[68]  M. Hallett,et al.  Complexity affects regional cerebral blood flow change during sequential finger movements , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.