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      Reconsidering the Role of Neuronal Intrinsic Properties and Neuromodulation in Vestibular Homeostasis

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          Abstract

          The sensorimotor transformations performed by central vestibular neurons constantly adapt as the animal faces conflicting sensory information or sustains injuries. To ensure the homeostasis of vestibular-related functions, neural changes could in part rely on the regulation of 2° VN intrinsic properties. Here we review evidence that demonstrates modulation and plasticity of central vestibular neurons’ intrinsic properties. We first present the partition of Rodents’ vestibular neurons into distinct subtypes, namely type A and type B. Then, we focus on the respective properties of each type, their putative roles in vestibular functions, fast control by neuromodulators and persistent modifications following a lesion. The intrinsic properties of central vestibular neurons can be swiftly modulated by a wealth of neuromodulators to adapt rapidly to temporary changes of ecophysiological surroundings. To illustrate how intrinsic excitability can be rapidly modified in physiological conditions and therefore be therapeutic targets, we present the modulation of vestibular reflexes in relation to the variations of the neuromodulatory inputs during the sleep/wake cycle. On the other hand, intrinsic properties can also be slowly, yet permanently, modified in response to major perturbations, e.g., after unilateral labyrinthectomy (UL). We revisit the experimental evidence, which demonstrates that drastic alterations of the central vestibular neurons’ intrinsic properties occur following UL, with a slow time course, more on par with the compensation of dynamic deficits than static ones. Data are interpreted in the framework of distributed processes that progress from global, large-scale coping mechanisms (e.g., changes in behavioral strategies) to local, small-scale ones (e.g., changes in intrinsic properties). Within this framework, the compensation of dynamic deficits improves over time as deeper modifications are engraved within the finer parts of the vestibular-related networks. Finally, we offer perspectives and working hypotheses to pave the way for future research aimed at understanding the modulation and plasticity of central vestibular neurons’ intrinsic properties.

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          Most cited references123

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          Vestibular system: the many facets of a multimodal sense.

          Elegant sensory structures in the inner ear have evolved to measure head motion. These vestibular receptors consist of highly conserved semicircular canals and otolith organs. Unlike other senses, vestibular information in the central nervous system becomes immediately multisensory and multimodal. There is no overt, readily recognizable conscious sensation from these organs, yet vestibular signals contribute to a surprising range of brain functions, from the most automatic reflexes to spatial perception and motor coordination. Critical to these diverse, multimodal functions are multiple computationally intriguing levels of processing. For example, the need for multisensory integration necessitates vestibular representations in multiple reference frames. Proprioceptive-vestibular interactions, coupled with corollary discharge of a motor plan, allow the brain to distinguish actively generated from passive head movements. Finally, nonlinear interactions between otolith and canal signals allow the vestibular system to function as an inertial sensor and contribute critically to both navigation and spatial orientation.
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            Cascade models of synaptically stored memories.

            Storing memories of ongoing, everyday experiences requires a high degree of plasticity, but retaining these memories demands protection against changes induced by further activity and experience. Models in which memories are stored through switch-like transitions in synaptic efficacy are good at storing but bad at retaining memories if these transitions are likely, and they are poor at storage but good at retention if they are unlikely. We construct and study a model in which each synapse has a cascade of states with different levels of plasticity, connected by metaplastic transitions. This cascade model combines high levels of memory storage with long retention times and significantly outperforms alternative models. As a result, we suggest that memory storage requires synapses with multiple states exhibiting dynamics over a wide range of timescales, and we suggest experimental tests of this hypothesis.
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              From waking to sleeping: neuronal and chemical substrates.

              Multiple arousal systems maintain waking through the actions of chemical neurotransmitters that are released from broadly distributed nerve terminals when the neurons fire. Among these, noradrenaline-, histamine- and orexin-containing neurons fire during waking with behavioral arousal, decrease firing during slow-wave sleep (SWS) and cease firing during paradoxical sleep (PS), which is also known as rapid-eye-movement sleep. By contrast, acetylcholine (ACh)-containing neurons discharge during waking, decrease firing during SWS and fire at high rates during PS in association with fast cortical activity. Neurons that do not contain ACh, including GABA-containing neurons in the basal forebrain and preoptic area, are active in a reciprocal manner to the neurons of the arousal systems: one group discharges with slow cortical activity during SWS, and another discharges with behavioral quiescence and loss of postural muscle tone during SWS and PS. The reciprocal activities and interactions of these wake-active and sleep-active cell groups determine the alternation between waking and sleeping. Selective enhancement and attenuation of their discharge, transmitter release and postsynaptic actions comprise the substrates for the major stimulant and hypnotic drugs.
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                Author and article information

                Journal
                Front Neurol
                Front Neurol
                Front. Neur.
                Frontiers in Neurology
                Frontiers Research Foundation
                1664-2295
                15 December 2011
                28 February 2012
                2012
                : 3
                : 25
                Affiliations
                [1] 1simpleCentre d’Etude de la SensoriMotricité, CNRS UMR 8194, Université Paris Descartes, Sorbonne Paris Cité Paris, France
                Author notes

                Edited by: Kenna Peusner, George Washington University, USA

                Reviewed by: Maurizio Versino, Pavia University, Italy; Aaron Camp, University of Sydney, Australia

                *Correspondence: Mathieu Beraneck, Centre d’Etude de la SensoriMotricité, CNRS UMR 8194, Université Paris Descartes, Sorbonne Paris Cité, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. e-mail: mathieu.beraneck@ 123456parisdescartes.fr

                This article was submitted to Frontiers in Neurootology, a specialty of Frontiers in Neurology.

                Article
                10.3389/fneur.2012.00025
                3289128
                22403570
                5c4c6258-aad9-44e2-991e-91b63f58e825
                Copyright © 2012 Beraneck and Idoux.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                : 02 December 2011
                : 09 February 2012
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 127, Pages: 13, Words: 1143
                Categories
                Neurology
                Review Article

                Neurology
                vestibular compensation,neuromodulation,postlesional plasticity,intrinsic properties,central vestibular neurons

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