Stimulation or lesion of the medial vestibular nucleus increases the number of choline acetyltransferase-positive efferent vestibular neurons in the brainstem

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.

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Spatial Properties of Central Vestibular Neurons of Monkeys After Bilateral Lateral Canal Nerve Section

Journal of Neurophysiology ◽

10.1152/jn.01102.2004 ◽

2005 ◽

Vol 94 (6) ◽

pp. 3860-3871 ◽

Cited By ~ 9

Author(s):

Sergei B. Yakushin ◽

Theodore Raphan ◽

Jean A. Büttner-Ennever ◽

Jun-Ichi Suzuki ◽

Bernard Cohen

Keyword(s):

Vestibular Nucleus ◽

Vertical Axis ◽

Medial Vestibular Nucleus ◽

Head Orientation ◽

Nerve Section ◽

Vestibular Neurons ◽

Lateral Canal ◽

Spatial Properties ◽

Central Neurons ◽

Central Compensation

Thirty-seven neurons were recorded in the superior vestibular nucleus (SVN) of two cynomolgus monkeys 1–2 yr after bilateral lateral canal nerve section to test whether the central neurons had spatially adapted for the loss of lateral canal input. The absence of lateral canal function was verified with eye movement recordings. The relation of unit activity to the vertical canals was determined by oscillating the animals about a horizontal axis with the head in various orientations relative to the axis of rotation. Animals were also oscillated about a vertical axis while upright or tilted in pitch. In the second test, the vertical canals are maximally activated when the animals are tilted back about −50° from the spatial upright and the lateral canals when the animals are tilted forward about 30°. We reasoned that if central compensation occurred, the head orientation at which the response of the vertical canal-related neurons was maximal should be shifted toward the plane of the lateral canals. No lateral canal-related units were found after nerve section, and vertical canal-related units were found only in SVN not in the rostral medial vestibular nucleus. SVN canal-related units were maximally activated when the head was tilted back at −47 ± 17 and −50 ± 12° (means ± SD) in the two animals, close to the predicted orientation of the vertical canals. This indicated that spatial adaptation of vertical canal-related vestibular neurons had not occurred. There were substantial neck and/or otolith-related inputs activating the vertical canal-related neurons in the nerve-sectioned animals, which could have contributed to oculomotor compensation after nerve section.

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Vestibular neurons with direct projections to the solitary nucleus in the rat

Journal of Neurophysiology ◽

10.1152/jn.00082.2019 ◽

2019 ◽

Vol 122 (2) ◽

pp. 512-524 ◽

Cited By ~ 6

Author(s):

Amelia H. Gagliuso ◽

Emily K. Chapman ◽

Giorgio P. Martinelli ◽

Gay R. Holstein

Keyword(s):

Blood Pressure ◽

Heart Rate ◽

Vestibular Nucleus ◽

Vasovagal Syncope ◽

Vestibular Nuclei ◽

Medial Vestibular Nucleus ◽

Postural Orthostatic Tachycardia Syndrome ◽

Vestibular Neurons ◽

Direct Demonstration ◽

Vestibular Nuclear Neurons

Anterograde and retrograde tract tracing were combined with neurotransmitter and modulator immunolabeling to identify the chemical anatomy of vestibular nuclear neurons with direct projections to the solitary nucleus in rats. Direct, sparsely branched but highly varicose axonal projections from neurons in the caudal vestibular nuclei to the solitary nucleus were observed. The vestibular neurons giving rise to these projections were predominantly located in ipsilateral medial vestibular nucleus. The cell bodies were intensely glutamate immunofluorescent, and their axonal processes contained vesicular glutamate transporter 2, supporting the interpretation that the cells utilize glutamate for neurotransmission. The glutamate-immunofluorescent, retrogradely filled vestibular cells also contained the neuromodulator imidazoleacetic acid ribotide, which is an endogenous CNS ligand that participates in blood pressure regulation. The vestibulo-solitary neurons were encapsulated by axo-somatic GABAergic terminals, suggesting that they are under tight inhibitory control. The results establish a chemoanatomical basis for transient vestibular activation of the output pathways from the caudal and intermediate regions of the solitary nucleus. In this way, changes in static head position and movement of the head in space may directly influence heart rate, blood pressure, respiration, as well as gastrointestinal motility. This would provide one anatomical explanation for the synchronous heart rate and blood pressure responses observed after peripheral vestibular activation, as well as disorders ranging from neurogenic orthostatic hypotension, postural orthostatic tachycardia syndrome, and vasovagal syncope to the nausea and vomiting associated with motion sickness. NEW & NOTEWORTHY Vestibular neurons with direct projections to the solitary nucleus utilize glutamate for neurotransmission, modulated by imidazoleacetic acid ribotide. This is the first direct demonstration of the chemical neuroanatomy of the vestibulo-solitary pathway.

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Direct projections from vestibular nuclei to facial nucleus in cats

Journal of Neurophysiology ◽

10.1152/jn.1983.50.6.1265 ◽

1983 ◽

Vol 50 (6) ◽

pp. 1265-1280 ◽

Cited By ~ 26

Author(s):

M. D. Shaw ◽

R. Baker

Keyword(s):

Nerve Stimulation ◽

Vestibular Nucleus ◽

Medial Vestibular Nucleus ◽

Facial Nucleus ◽

Antidromic Activation ◽

Postsynaptic Potentials ◽

Vestibular Neurons ◽

Time To Peak ◽

Trigeminal Nerve Stimulation ◽

Facial Motoneurons

Postsynaptic potentials were recorded from motoneurons in the facial nucleus in response to stimulation of the vestibular and trigeminal nerves. The motoneurons were identified by antidromic activation from their peripheral axons. Disynaptic excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) and mixed EPSP/IPSPs were recorded in response to vestibular nerve stimulation, ranging in latency from 0.9 to 2.1 ms, with most at 1.5 ms. Activity in secondary vestibular axons recorded within the facial nucleus occurred at a latency of 0.7-1.1 ms. The amplitudes of the vestibular postsynaptic potentials were small, generally less than a millivolt, but double shocks produced marked summation. The average time to peak of ipsilateral vestibular EPSPs, 1.1 ms, was faster than that of either ipsilateral IPSPs, 1.6 ms, or contralateral EPSPs, 1.4 ms. The double-spiked vestibular activity was detectable in double-peaked PSPs. Disynaptic EPSPs, ranging in latency from 2.0 to 3.0 ms, were recorded in response to trigeminal nerve stimulation. The average time to peak was 1.3 ms. The multiple-spiked activity of the trigeminal neurons was detectable in multipeaked EPSPs. Inhibitory ipsilateral effects (Vi IPSPs) were recorded twice as often as excitatory ipsilateral effects (Vi EPSPs), being found in 29% versus 15% of the motoneurons. Contralateral effects were found in 13% of the motoneurons studied, and almost all were excitatory. Analysis of synaptic potential shapes suggested that the excitatory and inhibitory vestibular synapses probably contact distal dendrites preferentially, with the excitatory connections being somewhat closer to the soma. The trigeminal inputs probably contact the facial motoneurons more extensively near the soma. Horseradish peroxidase was injected into the facial nucleus, and retrograde uptake by vestibular neurons was studied. The majority of filled vestibular neurons was ipsilateral to the injection site, especially in the medial vestibular nucleus, ventral y group, and supravestibular nucleus. On the contralateral side, filled vestibular cells were found almost exclusively in the medial nucleus. Filled cells were also noted in the trigeminal nucleus, predominantly ipsilaterally at all rostrocaudal levels. We have demonstrated monosynaptic projections to facial motoneurons from both vestibular and trigeminal nuclei. The trigeminal input is likely to be involved in facial reflexes, especially blinking and grimacing. The afferent vestibular population overlaps that going to the oculomotor and cervical motoneurons; these projections may be collaterals of single vestibular neurons.4+.

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Ultrastructural features of non-commissural GABAergic neurons in the medial vestibular nucleus of the monkey

Neuroscience ◽

10.1016/s0306-4522(99)00140-2 ◽

1999 ◽

Vol 93 (1) ◽

pp. 183-193 ◽

Cited By ~ 18

Author(s):

G.R. Holstein ◽

G.P. Martinelli ◽

B. Cohen

Keyword(s):

Vestibular Nucleus ◽

Gabaergic Neurons ◽

Medial Vestibular Nucleus

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Excitation and inhibition of rat medial vestibular nucleus neurones by 5-hydroxytryptamine

Experimental Brain Research ◽

10.1007/bf00228397 ◽

1993 ◽

Vol 93 (2) ◽

Cited By ~ 30

Author(s):

A.R. Johnston ◽

Bridin Murnion ◽

D.S. McQueen ◽

M.B. Dutia

Keyword(s):

Vestibular Nucleus ◽

Medial Vestibular Nucleus

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Plasticity of γ-aminobutyrate receptors in the medial vestibular nucleus of rat after inferior cerebellar peduncle transection

Journal of Vestibular Research ◽

10.3233/ves-2002-12101 ◽

2002 ◽

Vol 12 (1) ◽

pp. 1-14

Author(s):

Yizhe Sun ◽

Donald A. Godfrey ◽

Allan M. Rubin

Keyword(s):

Vestibular Nucleus ◽

Brain Slices ◽

Medial Vestibular Nucleus ◽

Grouped Data ◽

Spontaneous Firing ◽

Gaba A ◽

Endogenous Gaba ◽

Single Unit Recordings ◽

Cerebellar Peduncle ◽

Inferior Cerebellar Peduncle

Extracellular single unit recordings were made from regularly discharging medial vestibular nucleus neurons in brain slices from control rats and from rats surviving 7 days after bilateral transection of the inferior cerebellar peduncle. Decreases in firing rate during perfusion with the Îş-aminobutyric acid (GABA) agonists, muscimol (GABA A ) and baclofen (GABA B ), were greater in lesioned rats than in control rats. For the grouped data, the half-maximally-effective concentrations of muscimol and baclofen were 3.2 µM, as compared with 19.6 µM for control, and 0.8 µM, as compared with 2.7 µM for control, respectively. The antagonists bicuculline (GABA A ) and 2-OH-saclofen (GABA B ) only minimally affected the spontaneous firing rates of neurons in lesioned rats, significantly less than in control rats. The data suggest that the decreases of endogenous GABA levels in the medial vestibular nucleus after inferior cerebellar peduncle transection are accompanied by up-regulation of GABA A and, to a lesser extent, GABA B receptors.

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Unilateral labyrinthectomy induced changes on GDNF receptor complex proteins in the rat medial vestibular nuclei

Journal of Vestibular Research ◽

10.3233/ves-2006-164-502 ◽

2007 ◽

Vol 16 (4-5) ◽

pp. 171-177

Author(s):

Adrian Lozada ◽

Kaj Karlstedt ◽

Pertti Panula ◽

Antti A. Aarnisalo

Keyword(s):

Mrna Expression ◽

Vestibular Nucleus ◽

Medial Vestibular Nucleus ◽

Receptor Complex ◽

Trophic Effect ◽

Expression Levels ◽

Protein Levels ◽

Unilateral Labyrinthectomy ◽

Ganglion Neurons ◽

Mrna Expression Levels

In the auditory periphery, GDNF has been shown to have a trophic effect to spiral ganglion neurons, both during development and in adult animals. We have studied the effect of unilateral labyrinthectomy (UL) on protein levels and expression of GDNF multicomponent receptor complex: the ret tyrosine kinase and coreceptor GFRα-1 in the medial vestibular nucleus of the adult rat. GFRα-1 protein levels display an increasing trend in ipsilateral medial vestibular nucleus culminating at 48 h post UL. On the other hand, GFRα-1 mRNA expression levels in ipsi- and contralateral medial vestibular nucleus show a steadily decreasing trend that is significant at 1 week post-lesion. Protein levels for c-Ret isoforms also show an initial bilateral decreasing trend that ceases at 48 h in ipsilateral medial vestibular nucleus but persists on the contralateral side. c-Ret mRNA expression levels show a significant decrease at 4 h post UL followed by another significant decrease 1 week post UL. Our data would suggest that neurotrophins belonging to the GDNF family are involved in this model of post-lesional CNS plasticity.

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Measurement of 5-hydroxytryptamine release in the rat medial vestibular nucleus using in vivo microdialysis

Neuroscience Letters ◽

10.1016/s0304-3940(02)00152-0 ◽

2002 ◽

Vol 323 (3) ◽

pp. 234-238 ◽

Cited By ~ 5

Author(s):

Shino Inoue ◽

Taizo Kita ◽

Toshiaki Yamanaka ◽

Yohichi Ogawa ◽

Toshikatsu Nakashima ◽

...

Keyword(s):

Vestibular Nucleus ◽

In Vivo Microdialysis ◽

Medial Vestibular Nucleus

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Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques

Journal of Neurophysiology ◽

10.1152/jn.1992.68.1.319 ◽

1992 ◽

Vol 68 (1) ◽

pp. 319-332 ◽

Cited By ~ 211

Author(s):

J. L. McFarland ◽

A. F. Fuchs

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Smooth Pursuit ◽

Vestibular Nucleus ◽

Medial Vestibular Nucleus ◽

Eye Position ◽

Head Velocity ◽

Firing Rates ◽

Prepositus Hypoglossi ◽

Eye Velocity

1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the “marginal zone”). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral “on” directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

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