Intrinsic membrane properties of central vestibular neurons in rodents

Eugène, Daniel; Idoux, Erwin; Beraneck, Mathieu; Moore, Lee E.; Vidal, Pierre‐Paul

doi:10.1007/s00221-011-2569-3

Cited by 23 publications

(18 citation statements)

References 86 publications

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“…These results from in vitro studies (59) and from frogs (60–66) have been shown to apply also in mammalian vestibular system. Type A and B neurons previously found in brainstem slices were identified in the guinea pig whole-brain preparation, and these neurons receive direct inputs from the vestibular nerve.…”

Section: Physiological Datamentioning

confidence: 62%

Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function

et al. 2017

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Otolithic afferents with regular resting discharge respond to gravity or low-frequency linear accelerations, and we term these the static or sustained otolithic system. However, in the otolithic sense organs, there is anatomical differentiation across the maculae and corresponding physiological differentiation. A specialized band of receptors called the striola consists of mainly type I receptors whose hair bundles are weakly tethered to the overlying otolithic membrane. The afferent neurons, which form calyx synapses on type I striolar receptors, have irregular resting discharge and have low thresholds to high frequency (e.g., 500 Hz) bone-conducted vibration and air-conducted sound. High-frequency sound and vibration likely causes fluid displacement which deflects the weakly tethered hair bundles of the very fast type I receptors. Irregular vestibular afferents show phase locking, similar to cochlear afferents, up to stimulus frequencies of kilohertz. We term these irregular afferents the transient system signaling dynamic otolithic stimulation. A 500-Hz vibration preferentially activates the otolith irregular afferents, since regular afferents are not activated at intensities used in clinical testing, whereas irregular afferents have low thresholds. We show how this sustained and transient distinction applies at the vestibular nuclei. The two systems have differential responses to vibration and sound, to ototoxic antibiotics, to galvanic stimulation, and to natural linear acceleration, and such differential sensitivity allows probing of the two systems. A 500-Hz vibration that selectively activates irregular otolithic afferents results in stimulus-locked eye movements in animals and humans. The preparatory myogenic potentials for these eye movements are measured in the new clinical test of otolith function—ocular vestibular-evoked myogenic potentials. We suggest 500-Hz vibration may identify the contribution of the transient system to vestibular controlled responses, such as vestibulo-ocular, vestibulo-spinal, and vestibulo-sympathetic responses. The prospect of particular treatments targeting one or the other of the transient or sustained systems is now being realized in the clinic by the use of intratympanic gentamicin which preferentially attacks type I receptors. We suggest that it is valuable to view vestibular responses by this sustained-transient distinction.

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Section: Physiological Datamentioning

confidence: 62%

Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function

et al. 2017

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“…However, VVM neurons showed a decrease of their spontaneous firing rate in comparison to control neurons (Mann–Whitney test, z = –2.49, p = 0.013) and a slightly more regular spontaneous discharge than control neurons (CV of 0.16 vs. 0.22; Mann–Whitney test, z = 1.97, p = 0.048). MVN neurons were previously shown to be composed of different subpopulations that can be partly segregated using their electrophysiological signature at rest (Straka et al, 2005; Eugène et al, 2011; Beraneck and Idoux, 2012). Hence, we further divided the recorded neurons using the canonical type A and type B classification.…”

Section: Resultsmentioning

confidence: 99%

Long-Lasting Visuo-Vestibular Mismatch in Freely-Behaving Mice Reduces the Vestibulo-Ocular Reflex and Leads to Neural Changes in the Direct Vestibular Pathway

Carcaud

Barros

Idoux

et al. 2017

eNeuro

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Calibration of the vestibulo-ocular reflex (VOR) depends on the presence of visual feedback. However, the cellular mechanisms associated with VOR modifications at the level of the brainstem remain largely unknown. A new protocol was designed to expose freely behaving mice to a visuo-vestibular mismatch during a 2-week period. This protocol induced a 50% reduction of the VOR. In vivo pharmacological experiments demonstrated that the VOR reduction depends on changes located outside the flocculus/paraflocculus complex. The cellular mechanisms associated with the VOR reduction were then studied in vitro on brainstem slices through a combination of vestibular afferent stimulation and patch-clamp recordings of central vestibular neurons. The evoked synaptic activity demonstrated that the efficacy of the synapses between vestibular afferents and central vestibular neurons was decreased. In addition, a long-term depression protocol failed to further decrease the synapse efficacy, suggesting that the VOR reduction might have occurred through depression-like mechanisms. Analysis of the intrinsic membrane properties of central vestibular neurons revealed that the synaptic changes were supplemented by a decrease in the spontaneous discharge and excitability of a subpopulation of neurons. Our results provide evidence that a long-lasting visuo-vestibular mismatch leads to changes in synaptic transmission and intrinsic properties of central vestibular neurons in the direct VOR pathway. Overall, these results open new avenues for future studies on visual and vestibular interactions conducted in vivo and in vitro.

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“…At this age, glutamate receptor-mediated postsynaptic responses within the VN also reach a status that is comparable to that observed at P21, suggesting that effective transmission of head rotational input is achieved within the first postnatal week (cf. Eugène et al 2011). It is noteworthy that appearance of head-turning response (cephalic response) also occurs at P4 in rats (Parrad and Cottereau 1977).…”

Section: Sequential Maturation Of the Vestibulo-olivary Pathwaymentioning

confidence: 98%

Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats

Lai

et al. 2014

Brain Struct Funct

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The recognition of head orientation in the adult involves multi-level integration of inputs within the central vestibular circuitry. How the different inputs are recruited during postnatal development remains unclear. We hypothesize that glutamatergic transmission at the vestibular nucleus contributes to developmental registration of head orientations along the vestibulo-olivary pathway. To investigate the maturation profile by which head rotational signals are registered in the brainstem, we used sinusoidal rotations on the orthogonal planes of the three pairs of semicircular canals. Fos expression was used as readout of neurons responsive to the rotational stimulus. Neurons in the vestibular nucleus and prepositus hypoglossal nucleus responded to all rotations as early as P4 and reached adult numbers by P21. In the reticular formation and inferior olive, neurons also responded to horizontal rotations as early as P4 but to vertical rotations not until P21 and P25, respectively. Neuronal subpopulations that distinguish between rotations activating the orthogonally oriented vertical canals were identifiable in the medial and spinal vestibular nuclei by P14 and in the inferior olivary subnuclei IOβ and IOK by P25. Neonatal perturbation of glutamate transmission in the vestibular nucleus was sufficient to derange formation of this distribution in the inferior olive. This is the first demonstration that developmental refinement of glutamatergic synapses in the central vestibular circuitry is essential for developmental registration of head rotational signals in the brainstem.

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Intrinsic membrane properties of central vestibular neurons in rodents

Cited by 23 publications

References 86 publications

Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function

Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function

Long-Lasting Visuo-Vestibular Mismatch in Freely-Behaving Mice Reduces the Vestibulo-Ocular Reflex and Leads to Neural Changes in the Direct Vestibular Pathway

Maturation of glutamatergic transmission in the vestibulo-olivary pathway impacts on the registration of head rotational signals in the brainstem of rats

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