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

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.

Deranged Dimensionality of Vestibular Re-Weighting in Multiple Chemical Sensitivity

“…Furthermore, increased body sways within the middle interval and in classical posturography parameters especially during closed eye condition tend to confirm similar findings in previous studies, and result in a decreased ability to adapt to balance perturbations under complex conditions in certain disorders affected by a lack of vigilance [45][46][47][48][49]. It has previously been noted that the integration of information from the visual, vestibular and somatosensory receptors and motor coordination are processes requiring attention and vigilance [48], especially when information from other sensory systems is not reliable [50].…”

“…Moreover, theoretical models of multisensory combination based on neurophysiological [57], perceptual [58] and behavioural evidence [59] proposed that adaptation to environmental changes would rely on sensory re-weighting to optimize both the relevance of individual sensory inputs and the reliability of estimates [48]. This kind of phenomenon is thought to be determined by maximum likelihood estimation so that the conscious and non-conscious brain processing appears as a near-optimal Bayesian estimator of object properties [56,60].…”

“…It has previously been noted that the integration of information from the visual, vestibular and somatosensory receptors and motor coordination are processes requiring attention and vigilance [48], especially when information from other sensory systems is not reliable [50]. Considering the closeness between MCS and other related idiopathic disorders affected by functional postural impairment and attention and vigilance decrease (i.e., fibromyalgia, chronic fatigue syndrome) [45,51] it could be postulated that such phenomena may lead to slower or inappropriate sensory integration [48].…”

Sequential [18F]FDG µPET whole-brain imaging of central vestibular compensation: a model of deafferentation-induced brain plasticity

“…This process is attributed to neuronal plasticity that takes place mainly in the brainstem and cerebellum (Curthoys and Halmagyi 1995;Dieringer 1995;Vibert et al 1999;Darlington and Smith 2000;Dutia 2010;Peusner et al 2012;Beraneck and Idoux 2012).…”

“…It is thought that the vestibulocerebellum is most likely involved in consolidating vestibular compensation (Darlington and Smith 2000;Beraneck et al 2008). All in all, successful vestibular compensation must be seen as a process involving multiple, synergistic adaptations in neuronal networks in various areas of the brain (Dutia 2010;Beraneck and Idoux 2012).…”