Unilateral Labyrinthectomy Modifies the Membrane Properties of Contralesional Vestibular Neurons

2004 ◽  
Vol 92 (3) ◽  
pp. 1668-1684 ◽  
Author(s):  
Mathieu Beraneck ◽  
Erwin Idoux ◽  
Atsuhiko Uno ◽  
Pierre-Paul Vidal ◽  
Lee E. Moore ◽  
...  

Vestibular compensation after a unilateral labyrinthectomy leads to nearly complete disappearance of the static symptoms triggered by the lesion. However, the dynamic vestibular reflexes associated with head movements remain impaired. Because the contralesional labyrinth plays a prominent role in the generation of these dynamic responses, intracellular recordings of contralesional medial vestibular nucleus neurons (MVNn) were done after 1 mo of compensation. Their firing properties and cell type were characterized at rest, and their response dynamics investigated using step, ramp, and sinusoidal current stimulations. The sensitivity of the contralesional MVNn firing rates to applied current was increased, which, along with increased phase leads, suggests that significant changes in active conductances occurred. We found an increased proportion of the phasic type B neurons relative to the tonic type A neurons in the contralesional MVN. In addition, the remaining contralesional type A MVNn response dynamics tended to approach those of type B MVNn. Thus the contralesional MVNn in general showed more phasic response dynamics than those of control MVNn. Altogether, the firing properties of MVNn are differentially modified on the ipsilesional and contralesional sides of the brain stem 1 mo after unilateral labyrinthectomy. Ipsilesional MVNn acquire more “type A–like” tonic membrane properties, which would contribute to the stabilization of the spontaneous activity that recovers in the deafferented neurons during vestibular compensation. The bilateral increase in the sensitivity of MVNn and the acquisition of more “B-like” phasic membrane properties by contralesional MVNn should promote the restoration of the vestibular reflexes generated by the remaining, contralesional labyrinth.

2003 ◽  
Vol 90 (1) ◽  
pp. 184-203 ◽  
Author(s):  
Mathieu Beraneck ◽  
Mohammed Hachemaoui ◽  
Erwin Idoux ◽  
Laurence Ris ◽  
Atsuhiko Uno ◽  
...  

Unilateral labyrinthectomy results in oculomotor and postural disturbances that regress in a few days during vestibular compensation. The long-term (after 1 mo) consequences of unilateral labyrinthectomy were investigated by characterizing the static and dynamic membrane properties of the ipsilesional vestibular neurons recorded intracellularly in guinea pig brain stem slices. We compared the responses of type A and type B medial vestibular nucleus neurons identified in vitro to current steps and ramps and to sinusoidal currents of various frequencies. All ipsilesional vestibular neurons were depolarized by 6–10 mV at rest compared with the cells recorded from control slices. Both their average membrane potential and firing threshold were more depolarized, which suggests that changes in active conductances compensated for the loss of excitatory afferents. The afterhyperpolarization and discharge regularity of type B but not type A neurons were increased. All ipsilesional vestibular cells became more sensitive to current injections over a large range of frequencies (0.2–30 Hz), but this increase in sensitivity was greater for type B than for type A neurons. This was associated with an increase of the peak frequency of linear response restricted to type B neurons, from 4–6 to 12–14 Hz. Altogether, we show that long-term vestibular compensation involves major changes in the membrane properties of vestibular neurons on the deafferented side. Many of the static and dynamic membrane properties of type B neurons became more similar to those of type A neurons than in control slices, leading to an increase in the overall homogeneity of medial vestibular nucleus neurons.


2003 ◽  
Vol 90 (3) ◽  
pp. 1689-1703 ◽  
Author(s):  
Atsuhiko Uno ◽  
Erwin Idoux ◽  
Mathieu Beraneck ◽  
Pierre-Paul Vidal ◽  
Lee E. Moore ◽  
...  

In vitro intracellular recordings of central vestibular neurons have been restricted so far to the medial vestibular nucleus (MVN). We performed intracellular recordings of large Deiters' neurons in the lateral vestibular nucleus (LVN) to determine their static and dynamic membrane properties, and compare them with those of type A and type B neurons identified in the MVN. Unlike MVN neurons (MVNn), the giant-size LVN neurons (LVNn) form a homogeneous population of cells characterized by sharp spikes, a low-amplitude, biphasic after-hyperpolarization like type B MVNn, but also an A-like rectification like type A MVNn. In accordance with their lower membrane resistance, the sensitivity of LVNn to current injection was lower than that of MVNn over a large range of frequencies. The main difference between LVNn and MVNn was that the Bode plots showing the sensitivity of LVNn as a function of stimulation frequency were flatter than those of MVNn, and displayed a weaker resonance. Furthermore, most LVNn did not show a gradual decrease of their firing rate modulation in the frequency range where it was observed in MVNn. LVNn synchronized their firing with the depolarizing phase of high-frequency sinusoidal current injections. In vivo studies have shown that the MVN would be mainly involved in gaze control, whereas the giant LVNn that project to the spinal cord are involved in the control of posture. We suggest that the difference in the membrane properties of LVNn and MVNn may reflect their specific physiological roles.


2020 ◽  
Author(s):  
Ingrid Nogueira ◽  
Jessica Winne ◽  
Thiago Z. Lima ◽  
Thawann Malfatti ◽  
Richardson N. Leao ◽  
...  

ABSTRACTLoud noise-exposure generates tinnitus in both humans and animals. Macroscopic studies show that noise exposure affects the auditory cortex; however, cellular mechanisms of tinnitus generation are unclear. Here we compare membrane properties of layer 5 (L5) pyramidal cells (PCs) of the primary auditory cortex (A1) from control and noise-exposed mice. PCs were previously classified in type A or type B based on connectivity and firing properties. Our analysis based on a logistic regression model predicted that afterhyperpolatization and afterdepolarization following the injection of inward and outward current are enough to predict cell type and these features are preserved after noise trauma. One week after a noise-exposure (4-18kHz, 90dB, 1.5 hr, followed by 1.5hr silence) no passive membrane properties of type A or B PCs were altered but principal component analysis showed greater separation between control/noise-exposure recordings for type A neurons. When comparing individual firing properties, noise exposure differentially affected type A and B PC firing frequency in response to depolarizing current steps. Specifically, type A PCs decreased both initial and steady state firing frequency and type B PCs significantly increased steady state firing frequency following noise exposure. These results show that loud noise can cause distinct effects on type A and B L5 auditory cortex PCs one week following noise exposure. As the type A PC electrophysiological profile is correlated to corticofugal L5 neurons, and type B PCs correlate to contralateral projecting PCs these alterations could partially explain the reorganization of the auditory cortex observed in tinnitus patients.


2006 ◽  
Vol 95 (5) ◽  
pp. 3012-3023 ◽  
Author(s):  
Chris Sekirnjak ◽  
Sascha du Lac

Neurons in the medial vestibular nucleus (MVN) vary in their projection patterns, responses to head movement, and intrinsic firing properties. To establish whether neurons that participate in the vestibulo-ocular reflex (VOR) have distinct intrinsic physiological properties, oculomotor nucleus (OMN)–projecting neurons were identified in mouse brainstem slices by fluorescent retrograde labeling from the oculomotor complex and targeted for patch-clamp recordings. Such neurons were located in the magnocellular portion of the MVN contralateral to tracer injection, were mostly multipolar, and had soma diameters of around 20 μm. They fired spontaneous action potentials at rates higher than those of other MVN neurons and their spikes were of unusually short duration. OMN-projecting neurons responded to 1-s intracellular current injection with exceptionally high firing rates of >500 spikes/s. Their current–firing relationship was highly linear, with weak firing response adaptation during steady depolarization and little postinhibitory rebound firing after membrane hyperpolarization. Their firing responses were approximately in phase with sinusoidal current injection. The response dynamics of OMN-projecting neurons could be simulated with a simple integrate-and-fire model modified with the addition of small adaptation and rebound conductances. These findings indicate that the membrane properties of OMN-projecting neurons allow them to respond to head movements reliably and with high sensitivity but without substantially altering input dynamics.


1987 ◽  
Vol 57 (6) ◽  
pp. 1716-1729 ◽  
Author(s):  
Y. S. Chan ◽  
J. Kasper ◽  
V. J. Wilson

With the use of floating electrodes we recorded from the C2 dorsal root ganglion of decerebrate cats during sinusoidal and trapezoidal head rotation. Fifty-one spontaneously firing afferents were identified as muscle spindle endings. Some were identified by their excitatory response to injection of succinylcholine, others by the similarity of their behavior to that of endings excited by the drug. Because afferent input to the ganglion was restricted by sectioning most nerve trunks, most spindle endings were presumably located in ventral and ventrolateral perivertebral muscles. The firing of each spindle afferent was modulated most effectively by tilting the head in a specific direction; this direction was termed its response vector. Responses to sine waves and trapezoids were then studied with stimuli oriented as closely as possible to the vertical plane of this vector. Most spindle afferents could be classified in one of two categories. Those with high gain, pronounced nonlinearity, and high dynamic index were called type A. Those classified as type B had low gain, a fairly linear response, and low dynamic index. In response to small (0.5 degrees) stimuli, type A endings had phase leads of approximately 40 degrees at frequencies of sinusoidal stimulation of 0.02-0.1 Hz, increasing to approximately 80 degrees at 4 Hz; with larger (2.5 degrees) stimuli, phase was advanced by an additional 10-20 degrees at all frequencies. Phase of type B responses was less advanced than that of type A responses. Gain slopes of the two types of endings were similar. Bode plots of spindle afferents strongly resembled those of upper cervical neurons whose activity is modulated by head rotation. Each spindle afferent had a response vector whose direction remained stable with time, different frequencies of stimulation, and different stimulus amplitudes. The distribution of response vectors covered approximately 270 degrees, with a gap near nose down pitch. Changing initial head position usually had little effect on the direction of an afferent's response vector or on response dynamics. However, stimulation far from the best plane could transform a type A into a type B response. This raises the possibility that type B receptors could be type A receptors best stimulated by yaw and with only low sensitivity to stimulation in vertical planes. Type A receptors have all the properties of spindle primaries. The identification of type B receptors remains uncertain, because they may include secondary afferents as well as primaries stimulated far from their best three-dimensional vector.(ABSTRACT TRUNCATED AT 400 WORDS)


2021 ◽  
Vol 11 (3) ◽  
pp. 360
Author(s):  
Junya Fukuda ◽  
Kazunori Matsuda ◽  
Go Sato ◽  
Tadashi Kitahara ◽  
Momoyo Matsuoka ◽  
...  

Background: Vestibular compensation (VC) after unilateral labyrinthectomy (UL) consists of the initial and late processes. These processes can be evaluated based on the decline in the frequency of spontaneous nystagmus (SN) and the number of MK801-induced Fos-positive neurons in the contralateral medial vestibular nucleus (contra-MVe) in rats. Histamine H3 receptors (H3R) are reported to be involved in the development of VC. Objective: We examined the effects of betahistine, an H3R antagonist, on the initial and late processes of VC in UL rats. Methods: Betahistine dihydrochloride was continuously administered to the UL rats at doses of 100 and 200 mg/kg/day using an osmotic minipump. MK801 (1.0 mg/kg) was intraperitoneally administered on days 7, 10, 12, and 14 after UL, while Fos-positive neurons were immunohistochemically stained in the contra-MVe. Results: The SN disappeared after 42 h, and continuous infusion of betahistine did not change the decline in the frequency of SN. The number of MK801-induced Fos-positive neurons in contra-MVe significantly decreased on days 7, 10, and 12 after UL in a dose-dependent manner in the betahistine-treated rats, more so than in the saline-treated rats. Conclusion: These findings suggest that betahistine facilitated the late, but not the initial, process of VC in UL rats.


1998 ◽  
Vol 119 (1) ◽  
pp. 34-42 ◽  
Author(s):  
Pierre-Paul Vidal ◽  
Catherine De Waele ◽  
Nicolas Vibert ◽  
Michel Mühlethaler

Vestibular compensation for the static and dynamic disorders induced by unilateral labyrinthectomy is a good model of plasticity in the central nervous system. After the lesion, the static deficits generally disappear in a few days, whereas recuperation of the dynamic, vestibular-related synergies is much slower and merely partial. The goal of this article is to reexamine some aspects of vestibular compensation in light of several recent findings. In the first part, we show that in vertebrates the organization of the neural networks underlying vestibular reflexes is deeply linked with the skeletal geometry of the animals. Accordingly, we propose that the neuronal mechanisms underlying vestibular compensation might be plane specific. We then deal with several issues related to the exact timing of vestibular compensation in various species. In the second part, we give several examples showing that vestibular compensation can now be studied at the molecular and cellular levels. For instance, we summarize some of our recent data, which indicate that glial cells could be strongly involved in the compensation process. (Otolaryngol Head Neck Surg 1998;119:34–42.)


2006 ◽  
Vol 95 (5) ◽  
pp. 3208-3218 ◽  
Author(s):  
Aaron J. Camp ◽  
Robert J. Callister ◽  
Alan M. Brichta

Fast inhibitory synaptic transmission in the medial vestibular nucleus (MVN) is mediated by GABAA receptors (GABAARs) and glycine receptors (GlyRs). To assess their relative contribution to inhibition in the MVN, we recorded miniature inhibitory postsynaptic currents (mIPSCs) in physiologically characterized type A and type B MVN neurons. Transverse brain stem slices were prepared from mice (3–8 wk old), and whole cell patch-clamp recordings were obtained from visualized MVN neurons (CsCl internal; Vm = –70 mV; 23°C). In 81 MVN neurons, 69% received exclusively GABAAergic inputs, 6% exclusively glycinergic inputs, and 25% received both types of mIPSCs. The mean amplitude of GABAAR-mediated mIPSCs was smaller than those mediated by GlyRs (22.6 ± 1.8 vs. 35.3 ± 5.3 pA). The rise time and decay time constants of GABAAR- versus GlyR-mediated mIPSCs were slower (1.3 ± 0.1 vs. 0.9 ± 0.1 ms and 10.5 ± 0.3 vs. 4.7 ± 0.3 ms, respectively). Comparison of type A ( n = 20) and type B ( n = 32) neurons showed that type A neurons received almost exclusively GABAAergic inhibitory inputs, whereas type B neurons received GABAAergic inputs, glycinergic inputs, or both. Intracellular labeling in a subset of MVN neurons showed that morphology was not related to a MVN neuron's inhibitory profile ( n = 15), or whether it was classified as type A or B ( n = 29). Together, these findings indicate that both GABA and glycine contribute to inhibitory synaptic processing in MVN neurons, although GABA dominates and there is a difference in the distribution of GABAA and Gly receptors between type A and type B MVN neurons.


2007 ◽  
Vol 98 (4) ◽  
pp. 1883-1897 ◽  
Author(s):  
Matthijs A. A. van der Meer ◽  
James J. Knierim ◽  
D. Yoganarasimha ◽  
Emma R. Wood ◽  
Mark C. W. van Rossum

The rodent head-direction (HD) system, which codes for the animal's head direction in the horizontal plane, is thought to be critically involved in spatial navigation. Electrophysiological recording studies have shown that HD cells can anticipate the animal's HD by up to 75–80 ms. The origin of this anticipation is poorly understood. In this modeling study, we provide a novel explanation for HD anticipation that relies on the firing properties of neurons afferent to the HD system. By incorporating spike rate adaptation and postinhibitory rebound as observed in medial vestibular nucleus neurons, our model produces realistic anticipation on a large corpus of rat movement data. In addition, HD anticipation varies between recording sessions of the same cell, between active and passive movement, and between different studies. Such differences do not appear to be correlated with behavioral variables and cannot be accounted for using earlier models. In the present model, anticipation depends on the power spectrum of the head movements. By direct comparison with recording data, we show that the model explains 60–80% of the observed anticipation variability. We conclude that HD afferent dynamics and the statistics of rat head movements are important in generating HD anticipation. This result contributes to understanding the functional circuitry of the HD system and has methodological implications for studies of HD anticipation.


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