Neural mechanisms for filtering self-generated sensory signals in cerebellum-like circuits

This review focuses on recent progress in understanding mechanisms for filtering self-generated sensory signals in cerebellum-like circuits in fish and mammals. Recent in vitro studies in weakly electric gymnotid fish have explored the interplay among anti-Hebbian plasticity, synaptic dynamics, and feedforward inhibition in canceling self-generated electrosensory inputs. Studies of the mammalian dorsal cochlear nucleus have revealed multimodal integration and anti-Hebbian plasticity, suggesting that this circuit may adaptively filter incoming auditory information. In vivo studies in weakly electric mormryid fish suggest a key role for granule cell coding in sensory filtering. The clear links between synaptic plasticity and systems level sensory filtering in cerebellum-like circuits may provide insights into hypothesized adaptive filtering functions of the cerebellum itself.

[1]  V. Han,et al.  Reversible Associative Depression and Nonassociative Potentiation at a Parallel Fiber Synapse , 2000, Neuron.

[2]  Leonard Maler,et al.  Burst-Induced Anti-Hebbian Depression Acts through Short-Term Synaptic Dynamics to Cancel Redundant Sensory Signals , 2010, The Journal of Neuroscience.

[3]  Timothy J. Ebner,et al.  Cerebellum Predicts the Future Motor State , 2008, The Cerebellum.

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

[5]  M. Sommer,et al.  Corollary discharge across the animal kingdom , 2008, Nature Reviews Neuroscience.

[6]  C. Bell,et al.  The generation and subtraction of sensory expectations within cerebellum-like structures. , 1997, Brain, behavior and evolution.

[7]  E D Young,et al.  Proprioceptive Information from the Pinna Provides Somatosensory Input to Cat Dorsal Cochlear Nucleus , 2001, The Journal of Neuroscience.

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

[9]  K. A. Davis,et al.  Somatosensory context alters auditory responses in the cochlear nucleus. , 2011, Journal of neurophysiology.

[10]  C. Bell An efference copy which is modified by reafferent input. , 1981, Science.

[11]  B. Gramberg-Danielsen [The reafference principle in its significance for ophthalmology]. , 1959, Albrecht von Graefe's Archiv fur Ophthalmologie.

[12]  T. Tzounopoulos,et al.  Distinct functional and anatomical architecture of the endocannabinoid system in the auditory brainstem. , 2009, Journal of neurophysiology.

[13]  N. Sawtell,et al.  Cerebellum-like structures and their implications for cerebellar function. , 2008, Annual review of neuroscience.

[14]  L. Trussell,et al.  Molecular layer inhibitory interneurons provide feedforward and lateral inhibition in the dorsal cochlear nucleus. , 2010, Journal of neurophysiology.

[15]  L. Trussell,et al.  Cell-specific, spike timing–dependent plasticities in the dorsal cochlear nucleus , 2004, Nature Neuroscience.

[16]  L. Trussell,et al.  Coactivation of Pre- and Postsynaptic Signaling Mechanisms Determines Cell-Specific Spike-Timing-Dependent Plasticity , 2007, Neuron.

[17]  Curtis C Bell,et al.  Memory-based expectations in electrosensory systems , 2001, Current Opinion in Neurobiology.

[18]  Patrick D. Roberts,et al.  Computational Consequences of Temporally Asymmetric Learning Rules: II. Sensory Image Cancellation , 2000, Journal of Computational Neuroscience.

[19]  Nathaniel B Sawtell,et al.  Transformations of Electrosensory Encoding Associated with an Adaptive Filter , 2008, The Journal of Neuroscience.

[20]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[21]  P. Manis,et al.  Two distinct types of inhibition mediated by cartwheel cells in the dorsal cochlear nucleus. , 2009, Journal of neurophysiology.

[22]  B. Lindner,et al.  Control of neuronal firing by dynamic parallel fiber feedback: implications for electrosensory reafference suppression , 2007, Journal of Experimental Biology.

[23]  T. Margrie,et al.  Sensory representations in cerebellar granule cells , 2009, Current Opinion in Neurobiology.

[24]  Eric D. Young,et al.  What's a cerebellar circuit doing in the auditory system? , 2004, Trends in Neurosciences.

[25]  L. Trussell,et al.  Fidelity of Complex Spike-Mediated Synaptic Transmission between Inhibitory Interneurons , 2008, The Journal of Neuroscience.

[26]  Patricia S Churchland,et al.  Self‐Representation in Nervous Systems , 2003, Annals of the New York Academy of Sciences.

[27]  Nathaniel B Sawtell,et al.  Multimodal Integration in Granule Cells as a Basis for Associative Plasticity and Sensory Prediction in a Cerebellum-like Circuit , 2010, Neuron.

[28]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[29]  D. Bodznick,et al.  The importance of N-methyl-d-aspartate (NMDA) receptors in subtraction of electrosensory reafference in the dorsal nucleus of skates , 2010, Journal of Experimental Biology.

[30]  T. Tzounopoulos,et al.  Physiological Activation of Cholinergic Inputs Controls Associative Synaptic Plasticity via Modulation of Endocannabinoid Signaling , 2011, The Journal of Neuroscience.

[31]  Jianxun Zhou,et al.  Somatosensory influence on the cochlear nucleus and beyond , 2006, Hearing Research.

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

[33]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[34]  Leonard Maler,et al.  Dynamics of electrosensory feedback: short-term plasticity and inhibition in a parallel fiber pathway. , 2002, Journal of neurophysiology.

[35]  D. Bodznick,et al.  Adaptive mechanisms in the elasmobranch hindbrain , 1999, The Journal of experimental biology.

[36]  J Bastian,et al.  Plasticity in an electrosensory system. I. General features of a dynamic sensory filter. , 1996, Journal of neurophysiology.

[37]  Henrik Jörntell,et al.  Synaptic Memories Upside Down: Bidirectional Plasticity at Cerebellar Parallel Fiber-Purkinje Cell Synapses , 2006, Neuron.

[38]  M. Fujita,et al.  Adaptive filter model of the cerebellum , 1982, Biological Cybernetics.

[39]  Donata Oertel,et al.  Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  James V. Stone,et al.  Decorrelation control by the cerebellum achieves oculomotor plant compensation in simulated vestibulo-ocular reflex , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  Martti Juhola,et al.  Simulation of aphasic naming errors in finnish language with neural networks , 1995, Neural Networks.

[42]  K. Grant,et al.  Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[43]  A. Bastian Learning to predict the future: the cerebellum adapts feedforward movement control , 2006, Current Opinion in Neurobiology.

[44]  Curtis C. Bell,et al.  Evolution of Cerebellum-Like Structures , 2002, Brain, Behavior and Evolution.