Learning from the past: A reverberation of past errors in the cerebellar climbing fiber signal

The cerebellum allows us to rapidly adjust motor behavior to the needs of the situation. It is commonly assumed that cerebellum-based motor learning is guided by the difference between the desired and the actual behavior, i.e., by error information. Not only immediate but also future behavior will benefit from an error because it induces lasting changes of parallel fiber synapses on Purkinje cells (PCs), whose output mediates the behavioral adjustments. Olivary climbing fibers, likewise connecting with PCs, are thought to transport information on instant errors needed for the synaptic modification yet not to contribute to error memory. Here, we report work on monkeys tested in a saccadic learning paradigm that challenges this concept. We demonstrate not only a clear complex spikes (CS) signature of the error at the time of its occurrence but also a reverberation of this signature much later, before a new manifestation of the behavior, suitable to improve it.

[1]  Clayton E Curtis,et al.  Obligatory adaptation of saccade gains. , 2008, Journal of neurophysiology.

[2]  Reza Shadmehr,et al.  Quantifying Generalization from Trial-by-Trial Behavior of Adaptive Systems that Learn with Basis Functions: Theory and Experiments in Human Motor Control , 2003, The Journal of Neuroscience.

[3]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[4]  M. Ito,et al.  Neural design of the cerebellar motor control system. , 1972, Brain research.

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

[6]  C. I. Zeeuw,et al.  Motor Learning and the Cerebellum , 2015 .

[7]  Stephen G Lisberger,et al.  Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning , 2013, eLife.

[8]  Yoshiko Kojima,et al.  Encoding of action by the Purkinje cells of the cerebellum , 2015, Nature.

[9]  Liam Paninski,et al.  Estimating entropy on m bins given fewer than m samples , 2004, IEEE Transactions on Information Theory.

[10]  Yasushi Kishimoto,et al.  Junctophilin‐mediated channel crosstalk essential for cerebellar synaptic plasticity , 2007, The EMBO journal.

[11]  T. Otis,et al.  Effects of Climbing Fiber Driven Inhibition on Purkinje Neuron Spiking , 2012, The Journal of Neuroscience.

[12]  Peter Thier,et al.  Cerebellum-dependent motor learning: lessons from adaptation of eye movements in primates. , 2014, Progress in brain research.

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

[14]  Peter Thier,et al.  Specific vermal complex spike responses build up during the course of smooth-pursuit adaptation, paralleling the decrease of performance error , 2010, Experimental Brain Research.

[15]  Timothy J. Ebner,et al.  The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning , 2015, The Cerebellum.

[16]  Yoshiko Kojima,et al.  Complex spike activity in the oculomotor vermis of the cerebellum: a vectorial error signal for saccade motor learning? , 2008, Journal of neurophysiology.

[17]  R. Shadmehr,et al.  Cerebellar Contributions to Adaptive Control of Saccades in Humans , 2009, The Journal of Neuroscience.

[18]  Peter Thier,et al.  The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning , 2011, The European journal of neuroscience.

[19]  Timothy J Ebner,et al.  What Do Complex Spikes Signal about Limb Movements? , 2002, Annals of the New York Academy of Sciences.

[20]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[21]  Peter Földiák,et al.  Bayesian bin distribution inference and mutual information , 2005, IEEE Transactions on Information Theory.

[22]  S. C. Mclaughlin Parametric adjustment in saccadic eye movements , 1967 .

[23]  Reza Shadmehr,et al.  Encoding of error and learning to correct that error by the Purkinje cells of the cerebellum , 2018, Nature Neuroscience.

[24]  Michael R. Ibbotson,et al.  Visual Perception: Saccadic Omission — Suppression or Temporal Masking? , 2009, Current Biology.

[25]  Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. , 2008, Nature neuroscience.

[26]  Yan Yang,et al.  Duration of complex-spikes grades Purkinje cell plasticity and cerebellar motor learning , 2014, Nature.

[27]  Peer Wulff,et al.  Evolving Models of Pavlovian Conditioning: Cerebellar Cortical Dynamics in Awake Behaving Mice , 2015, Cell reports.

[28]  Robijanto Soetedjo,et al.  Complex Spike Activity of Purkinje Cells in the Oculomotor Vermis during Behavioral Adaptation of Monkey Saccades , 2006, The Journal of Neuroscience.

[29]  Dominik Endres,et al.  Bayesian and information-theoretic tools for neuroscience , 2006 .

[30]  C. D. De Zeeuw,et al.  Motor Learning and the Cerebellum. , 2015, Cold Spring Harbor perspectives in biology.

[31]  Mario Negrello,et al.  Duration of Purkinje cell complex spikes increases with their firing frequency , 2015, Front. Cell. Neurosci..

[32]  Peter Thier,et al.  Cerebellar Complex Spike Firing Is Suitable to Induce as Well as to Stabilize Motor Learning , 2005, Current Biology.

[33]  Mitsuo Kawato,et al.  The Roles of the Olivocerebellar Pathway in Motor Learning and Motor Control. A Consensus Paper , 2017, The Cerebellum.

[34]  Peter Thier,et al.  Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response , 2008, Proceedings of the National Academy of Sciences.

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

[36]  Stefano Panzeri,et al.  Analytical estimates of limited sampling biases in different information measures. , 1996, Network.

[37]  P. Thier,et al.  Saccadic Dysmetria and Adaptation after Lesions of the Cerebellar Cortex , 1999, The Journal of Neuroscience.

[38]  Javier F. Medina,et al.  Beyond “all-or-nothing” climbing fibers: graded representation of teaching signals in Purkinje cells , 2013, Front. Neural Circuits.

[39]  Peter W Dicke,et al.  Characteristics of Responses of Golgi Cells and Mossy Fibers to Eye Saccades and Saccadic Adaptation Recorded from the Posterior Vermis of the Cerebellum , 2009, The Journal of Neuroscience.

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

[41]  M. Cynader,et al.  Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. , 1974, Journal of neurophysiology.

[42]  William Bialek,et al.  Entropy and information in neural spike trains: progress on the sampling problem. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[44]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.