Adaptive coupling of inferior olive neurons in cerebellar learning

In the cerebellar learning hypothesis, inferior olive neurons are presumed to transmit high fidelity error signals, despite their low firing rates. The idea of chaotic resonance has been proposed to realize efficient error transmission by desynchronized spiking activities induced by moderate electrical coupling between inferior olive neurons. A recent study suggests that the coupling strength between inferior olive neurons can be adaptive and may decrease during the learning process. We show that such a decrease in coupling strength can be beneficial for motor learning, since efficient coupling strength depends upon the magnitude of the error signals. We introduce a scheme of adaptive coupling that enhances the learning of a neural controller for fast arm movements. Our numerical study supports the view that the controlling strategy of the coupling strength provides an additional degree of freedom to optimize the actual learning in the cerebellum.

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

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

[3]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[4]  Kazuyuki Aihara,et al.  Duality of Rate Coding and Temporal Coding in Multilayered Feedforward Networks , 2003, Neural Computation.

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

[6]  M. Garwicz,et al.  Gating of cutaneous input to cerebellar climbing fibres during a reaching task in the cat , 1997, The Journal of physiology.

[7]  J. Teramae,et al.  Robustness of the noise-induced phase synchronization in a general class of limit cycle oscillators. , 2004, Physical review letters.

[8]  M. Arbib,et al.  Role of the cerebellum in reaching movements in humans. II. A neural model of the intermediate cerebellum , 1998, The European journal of neuroscience.

[9]  Kazuyuki Aihara,et al.  Quantitative Modeling of Spatio-Temporal Dynamics of inferior Olive Neurons with a Simple Conductance-Based Model , 2010, Int. J. Bifurc. Chaos.

[10]  Kazuyuki Aihara,et al.  The role of chaotic resonance in cerebellar learning , 2010, Neural Networks.

[11]  M Lidierth,et al.  Gating in the spino‐olivocerebellar pathways to the c1 zone of the cerebellar cortex during locomotion in the cat. , 1990, The Journal of physiology.

[12]  Kazuyuki Aihara,et al.  Solution to the inverse problem of estimating gap-junctional and inhibitory conductance in inferior olive neurons from spike trains by network model simulation , 2013, Neural Networks.

[13]  D. Signorini,et al.  Neural networks , 1995, The Lancet.

[14]  Germund Hesslow Inhibition of inferior olivary transmission by mesencephalic stimulation in the cat , 1986, Neuroscience Letters.

[15]  W. Regehr,et al.  Inhibitory Regulation of Electrically Coupled Neurons in the Inferior Olive Is Mediated by Asynchronous Release of GABA , 2009, Neuron.

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

[17]  R. Llinás,et al.  Electrotonic coupling between neurons in cat inferior olive. , 1974, Journal of neurophysiology.

[18]  C. I. Zeeuw,et al.  Anti-Malaria Drug Mefloquine Induces Motor Learning Deficits in Humans , 2010, Front. Neurosci..

[19]  K. Doya,et al.  Electrophysiological properties of inferior olive neurons: A compartmental model. , 1999, Journal of neurophysiology.

[20]  James S. Albus,et al.  I A New Approach to Manipulator Control: The I Cerebellar Model Articulation Controller , 1975 .

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

[22]  Ichiro Tsuda,et al.  Itinerant Dynamics of Class I* Neurons Coupled by Gap Junctions , 2003, Summer School on Neural Networks.

[23]  K. J. Quinn,et al.  The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation , 1993, Experimental Brain Research.

[24]  G Bard Ermentrout,et al.  Dynamics of limit-cycle oscillators subject to general noise. , 2009, Physical review letters.

[25]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.

[26]  M. Kawato,et al.  Reproduction of complex spike firing patterns with modulated effective coupling conductance in inferior olive neurons , 2010, Neuroscience Research.

[27]  R. Llinás,et al.  Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro. , 1981, The Journal of physiology.

[28]  I. Shimada,et al.  A Numerical Approach to Ergodic Problem of Dissipative Dynamical Systems , 1979 .

[29]  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.

[30]  R. Llinás,et al.  GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. , 1996, Journal of neurophysiology.

[31]  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.

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

[33]  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.

[34]  Mitsuo Kawato,et al.  Cerebellar supervised learning revisited: biophysical modeling and degrees-of-freedom control , 2011, Current Opinion in Neurobiology.

[35]  Kazuyuki Aihara,et al.  Bridging rate coding and temporal spike coding by effect of noise. , 2002, Physical review letters.

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

[37]  E. J. Lang,et al.  Local Changes in the Excitability of the Cerebellar Cortex Produce Spatially Restricted Changes in Complex Spike Synchrony , 2009, The Journal of Neuroscience.

[38]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.

[39]  Mitsuo Kawato,et al.  A computational model of four regions of the cerebellum based on feedback-error learning , 2004, Biological Cybernetics.

[40]  L. Christensen,et al.  University of Birmingham Disruption of state estimation in the human lateral cerebellum , 2007 .

[41]  Idan Segev,et al.  Low-amplitude oscillations in the inferior olive: a model based on electrical coupling of neurons with heterogeneous channel densities. , 1997, Journal of neurophysiology.

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

[43]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Nicolas Schweighofer,et al.  A model of activity-dependent formation of cerebellar microzones , 1998, Biological Cybernetics.

[45]  Richard Apps,et al.  Cerebellar cortical organization: a one-map hypothesis , 2009, Nature Reviews Neuroscience.

[46]  J. Simpson,et al.  Microcircuitry and function of the inferior olive , 1998, Trends in Neurosciences.

[47]  Erik De Schutter,et al.  The mysterious microcircuitry of the cerebellar nuclei , 2011, The Journal of physiology.

[48]  J. Houk,et al.  Movement-related inputs to intermediate cerebellum of the monkey. , 1993, Journal of neurophysiology.

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

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

[51]  J. Houk,et al.  Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. , 1985, Journal of neurophysiology.

[52]  K. Doya,et al.  Unsupervised learning of granule cell sparse codes enhances cerebellar adaptive control , 2001, Neuroscience.

[53]  M. Garwicz,et al.  Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat , 2004, Experimental Brain Research.

[54]  J. Deuchars,et al.  Role of Olivary Electrical Coupling in Cerebellar Motor Learning , 2008, Neuron.

[55]  K. Doya,et al.  Chaos may enhance information transmission in the inferior olive. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Germund Hesslow,et al.  Cerebellar control of the inferior olive , 2008, The Cerebellum.

[57]  Role of the Y-group of the vestibular nuclei and flocculus of the cerebellum in motor learning of the vertical vestibulo-ocular reflex. , 1997, Progress in brain research.

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

[59]  J. Yorke,et al.  Chaotic behavior of multidimensional difference equations , 1979 .

[60]  R. Llinás,et al.  Experimentally determined chaotic phase synchronization in a neuronal system. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Alfréd Rényi,et al.  Probability Theory , 1970 .

[62]  M. Kawato,et al.  Virtual trajectory and stiffness ellipse during multijoint arm movement predicted by neural inverse models , 2005, Biological Cybernetics.

[63]  S. Highstein,et al.  Chapter 22 Role of the Y-Group of the vestibular nuclei and flocculus of the cerebellum in motor learning of the vertical vestibulo-ocular reflex , 1997 .

[64]  M. Ito A new physiological concept on cerebellum. , 1990, Revue neurologique.

[65]  James S. Albus,et al.  New Approach to Manipulator Control: The Cerebellar Model Articulation Controller (CMAC)1 , 1975 .

[66]  E. Mugnaini,et al.  Origins of GABAergic Inputs to the Inferior Olive , 1989 .

[67]  S. Lisberger,et al.  The Cerebellum: A Neuronal Learning Machine? , 1996, Science.

[68]  R. Llinás,et al.  Morphological Correlates of Bilateral Synchrony in the Rat Cerebellar Cortex , 1996, The Journal of Neuroscience.

[69]  Ichiro Tsuda,et al.  Chaotic itinerancy as a mechanism of irregular changes between synchronization and desynchronization in a neural network. , 2004, Journal of integrative neuroscience.

[70]  O. Rössler CONTINUOUS CHAOS—FOUR PROTOTYPE EQUATIONS , 1979 .

[71]  E. D’Angelo,et al.  Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fiber-granule cell transmission in rat cerebellum. , 1999, Journal of neurophysiology.

[72]  M Ito,et al.  Neurophysiological aspects of the cerebellar motor control system. , 1970, International journal of neurology.

[73]  M. Kawato,et al.  Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum , 1993, Nature.

[74]  Robert Baker,et al.  Chapter 21 Characterization of Purkinje cells in the goldfish cerebellum during eye movement and adaptive modification of the vestibulo-ocular reflex , 1997 .

[75]  Richard F. Thompson,et al.  The Nature of Reinforcement in Cerebellar Learning , 1998, Neurobiology of Learning and Memory.