Neural Interruption by Unilateral Labyrinthectomy Biases the Directional Preference of Otolith-Related Vestibular Neurons

Background: The directional preference of otolith-related vestibular neurons elucidates the neuroanatomical link of labyrinths, but few direct experimental data have been provided. Methods: The directional preference of otolith-related vestibular neurons was measured in the vestibular nucleus using chemically induced unilateral labyrinthectomy (UL). For the model evaluation, static and dynamic behavioral tests as well as a histological test were performed. Extracellular neural activity was recorded for the neuronal responses to the horizontal head rotation and the linear head translation. Results: Seventy-seven neuronal activities were recorded, and the total population was divided into three groups: left UL (20), sham (35), and right UL (22). Based on directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance in the number of those sub-groups (contra-, 15/35, 43%; ipsi-, 20/35, 57%) in the sham (p = 0.155). However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL (p = 6.056 × 10−5), while left UL caused more contra-preferred neurons (13/20, 65%) (p = 0.058). In particular, the convergent neurons mainly led this biased difference (ipsi-, 100% after right UL and contra-, 89% after left UL) (p < 0.002). Conclusions: The directional preference of the neurons depended on the side of the lesion, and its dominance was mainly led by the convergent neurons.

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Directional preference of otolith-related neurons in vestibular nucleus

10.21203/rs.3.rs-16440/v1 ◽

2020 ◽

Author(s):

Nguyen Nguyen ◽

Kyu-Sung Kim ◽

Gyutae Kim

Keyword(s):

Vestibular Nucleus ◽

Vestibular Function ◽

Head Rotation ◽

Neuronal Responses ◽

Chemically Induced ◽

Neural Information ◽

Commissural Pathway ◽

Unilateral Labyrinthectomy ◽

Directional Preference ◽

Mechanical Movement

Abstract Background: Due to the paired structure of two labyrinths at both sides of ear, their communication is conducted through the interconnected commissural pathway. The close interconnection produces the neural responding property in vestibular nucleus, and the mechanical movement of the hair cells mainly specifies the property. However, the mechanism to initiate the responding property was evident based on the structure, but few direct experimental data were provided to understand the responding property based on the structure.Experimental Approach: The directional preference was investigated, which was one of critical neural responding property to illustrate the functional structure. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to emphasize the preference. For the model evaluation, static and dynamic behavioral tests were applied, and the results demonstrated a practical model construction. Following the evaluation, an extracellular neural activity was conducted for the neuronal responses to the horizontal head rotation and the linear head movement.Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance between those sub-groups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in sham model. However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL while left UL caused more contra-preferred neurons (13/20, 65%). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL).Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation.

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Directional preference of otolith-related neurons in vestibular nucleus

10.21203/rs.3.rs-16440/v3 ◽

2020 ◽

Author(s):

Nguyen Nguyen ◽

Kyu-Sung Kim ◽

Gyutae Kim

Keyword(s):

Vestibular Nucleus ◽

Vestibular Function ◽

Semicircular Canals ◽

Head Rotation ◽

Head Movements ◽

Neuronal Responses ◽

Neural Communication ◽

Neural Information ◽

Commissural Pathway ◽

Directional Preference

Abstract Background: Due to the paired structure of two labyrinths, their neural communication is conducted through the interconnected commissural pathway. Using the tight link, the neural responding characteristics are formed in vestibular nucleus, and these responses are initially generated by the mechanical movement of the hair cells in the semicircular canals and otoliths. Although the mechanism to describe the neuronal responses to the head movements was evident, few direct experimental data were provided, especially the directional preference of otolith-related neurons as one of critical responses to elucidate the function of the neurons in vestibular nucleus (VN). Experimental Approach: The directional preference of otolith-related neurons was investigated in VN. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to identify the origin of the directional preference. For the model evaluation, static and dynamic behavioral tests were performed. Following the evaluation, an extracellular neural activity was recorded for the neuronal responses to the horizontal head rotation and the linear head translation. Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance in the number of those sub-groups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in the sham (p=0.155). However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL (p=6.056×10-5) while left UL caused more contra-preferred neurons (13/20, 65%) (p=0.058). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL) (p<0.002). Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation.

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Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig

Journal of Neurophysiology ◽

10.1152/jn.1995.74.5.2087 ◽

1995 ◽

Vol 74 (5) ◽

pp. 2087-2099 ◽

Cited By ~ 115

Author(s):

L. Ris ◽

C. de Waele ◽

M. Serafin ◽

P. P. Vidal ◽

E. Godaux

Keyword(s):

Guinea Pig ◽

Vestibular Nucleus ◽

Head Rotation ◽

Second Order ◽

Vestibular Nerve ◽

Control Group ◽

Head Velocity ◽

Vestibular Neurons ◽

Unilateral Labyrinthectomy ◽

Control State

1. Neuronal activity was investigated in the left superior vestibular nucleus (SVN), lateral vestibular nucleus (LVN), and rostral part of the medial vestibular nucleus (MVN) in the alert guinea pig after a unilateral (left) labyrinthectomy was performed. Vestibular neurons were recorded either immediately (just-postoperative group, n = 6) or 1 wk after labyrinthectomy (1-wk-postoperative group, n = 6) and compared with the activity recorded in intact animals (control group, n = 6). 2. Animals were prepared for extracellular recording of single-unit activity and for eye movement recording (scleral search coil technique). To enable stimulation of the left vestibular nerve, bipolar silver ball electrodes were chronically implanted either in contact with the bony labyrinth in the control group or close to the stump of the vestibular nerve after labyrinthectomy. Complete labyrinthectomy was performed under halothane anesthesia. 3. The criterion used to select vestibular neurons for analysis was their recruitment by an electric shock on the vestibular nerve. Of the 589 recorded neurons, 424, defined as second-order vestibular neurons, were recruited at monosynaptic latencies (0.85-1.15 ms) and 165 were recruited at polysynaptic latencies. One hundred three second-order vestibular neurons were recorded in the control group, 173 in the just-postoperative group, and 148 in the 1-wk-postoperative group. 4. The activity of the electrically recruited neurons was recorded during sinusoidal horizontal head rotation in the dark (0.3 Hz, 40 degrees/s peak velocity). The behavior of the neurons was analyzed by plotting their firing rate against head velocity. The Y-intercept of the regression line was used to express spontaneous firing rate (resting discharge), and its slope was used to express the sensitivity of the neuron-to-head velocity. 5. In the absence of statistically significant difference between the characteristics of the neuronal discharge of the second-order vestibular neurons recorded in the SVN, LVN, and rostral MVN, the data were pooled. The Resting discharge of these cells amounted to 41.0 +/- 24.7 (SD) spikes/s in the control state, fell to 7.2 +/- 13.9 spikes/s just after labyrinthectomy, and completely returned to normal values 1 wk after surgery (42.5 +/- 21.6 spikes/s). Among the monosynaptically recruited neurons, the percentage of silent units was 0% in the control group, 69% in the just-postoperative group, and 0% in the 1-wk-postoperative group. 6. By contrast, the sensitivity to head velocity of the second-order vestibular neurons, which was 0.69 +/- 0.48 (SD) spikes.s-1/deg.s-1 in the control state and which fell to 0.03 +/- 0.11 spikes.s-1/deg.s-1 just after labyrinthectomy, remained low 1 wk after injury (0.21 +/- 0.26 spikes.s-1/deg.s-1). Moreover, the slight recovery of sensitivity to head rotation was due only to units behaving as type II neurons. 7. The mean resting discharge of the polysynaptically recruited neurons (pooled from the 3 explored nuclei) was 31.6 +/- 19.3 spikes/s in the control group. It decreased to 11.6 +/- 12.1 spikes/s in the just-postoperative group and recovered to 39.8 +/- 20.2 spikes/s in the 1-wk-postoperative group. No neuron was silent at rest either in the control group or in the 1-wk-postoperative group. Just after labyrinthectomy, 35% of the neurons had a null resting activity. The mean sensitivity to head velocity of these neurons was 0.55 +/- 0.42 spikes.s-1/deg.s-1 in the control group. It decreased to 0.05 +/- 0.12 spikes.s-1/deg.s-1 in the just-postoperative group and recovered to 0.22 +/- 0.17 spikes.s-1/deg.s-1 in the 1-wk-postoperative group. 8. We conclude that, at least in the guinea pig, the restoration of the spontaneous activity of the deafferented neurons is complete 1 wk after a unilateral labyrinthectomy and thus probably plays an important role in vestibular compensation...

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Directional preference of otolith-related neurons in vestibular nucleus

10.21203/rs.3.rs-16440/v2 ◽

2020 ◽

Author(s):

Nguyen Nguyen ◽

Kyu-Sung Kim ◽

Gyutae Kim

Keyword(s):

Vestibular Nucleus ◽

Vestibular Function ◽

Semicircular Canals ◽

Head Rotation ◽

Head Movements ◽

Neuronal Responses ◽

Neural Communication ◽

Neural Information ◽

Commissural Pathway ◽

Directional Preference

Abstract Background: Due to the paired structure of two labyrinths, their neural communication is conducted through the interconnected commissural pathway. Using the tight link, the neural responding characteristics are formed in vestibular nucleus, and these responses are initially generated by the mechanical movement of the hair cells in the semicircular canals and otoliths. Although the mechanism to describe the neuronal responses to the head movements was evident, few direct experimental data were provided, especially the directional preference of otolith-related neurons as one of critical responses to elucidate the function of the neurons in vestibular nucleus (VN).Experimental Approach: The directional preference of otolith-related neurons was investigated in VN. Also, a chemically induced unilateral labyrinthectomy (UL) was performed to identify the origin of the directional preference. For the model evaluation, static and dynamic behavioral tests were performed. Following the evaluation, an extracellular neural activity was recorded for the neuronal responses to the horizontal head rotation and the linear head translation.Results: Seventy seven neuronal activities were recorded from thirty SD rats (270-450 g, male), and total population was divided into three groups; left UL (20), sham (35), right UL (22). Based on the directional preference, two sub-groups were again classified as contra- and ipsi-preferred neurons. There was no significance in the number of those sub-groups (contra-: 15/35, 43%; ipsi-: 20/35, 57%) in the sham (p=0.155). However, more ipsi-preferred neurons (19/22, 86%) were observed after right UL (p=6.056×10-5) while left UL caused more contra-preferred neurons (13/20, 65%) (p=0.058). In particular, the convergent neurons mainly led this biased difference in the population (ipsi-: 100% after right UL & contra-: 89% after left UL) (p<0.002).Conclusion: The directional preference was evenly maintained under a normal vestibular function, and its unilateral loss biased the directional preference of the neurons, depending on the side of lesion. Moreover, the dominance of the directional preference was mainly led by the convergent neurons which had the neural information related with head rotation and linear translation.

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Long-Term Plasticity of Ipsilesional Medial Vestibular Nucleus Neurons After Unilateral Labyrinthectomy

Journal of Neurophysiology ◽

10.1152/jn.01140.2002 ◽

2003 ◽

Vol 90 (1) ◽

pp. 184-203 ◽

Cited By ~ 73

Author(s):

Mathieu Beraneck ◽

Mohammed Hachemaoui ◽

Erwin Idoux ◽

Laurence Ris ◽

Atsuhiko Uno ◽

...

Keyword(s):

Vestibular Nucleus ◽

Type A ◽

Vestibular Compensation ◽

Membrane Properties ◽

Medial Vestibular Nucleus ◽

Type B ◽

Dynamic Membrane ◽

Vestibular Neurons ◽

Unilateral Labyrinthectomy

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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Responses of central vestibular neurons to sinusoidal yaw rotation in compensated macaques after unilateral labyrinthectomy

Journal of Neurophysiology ◽

10.1152/jn.00365.2013 ◽

2013 ◽

Vol 110 (8) ◽

pp. 1822-1836 ◽

Cited By ~ 9

Author(s):

Shawn D. Newlands ◽

Min Wei

Keyword(s):

Vestibular Nucleus ◽

Vestibular Function ◽

Neuronal Firing ◽

Type I ◽

Vestibular Neurons ◽

Dynamic Function ◽

Individual Type ◽

Vestibular Commissures ◽

Unilateral Labyrinthectomy ◽

Contralateral Rotation

After vestibular labyrinth injury, behavioral measures of vestibular function partially recover through the process of vestibular compensation. The present study was performed to improve our understanding of the physiology of macaque vestibular nucleus neurons in the compensated state (>6 wk) after unilateral labyrinthectomy (UL). The responses of neurons to sinusoidal yaw rotation at a series of frequencies (0.1–2.0 Hz) and peak velocities (7.5–210°/s) were examined to determine how the behavior of these cells differed from those in animals with intact labyrinths. The sensitivity of neurons responding to ipsilateral rotation (type I) did not differ between the intact and injured sides after UL, although this sensitivity was lower bilaterally after lesion than before lesion. The sensitivity of neurons that increase firing with contralateral rotation (type II) was higher ipsilateral to the UL than before lesion or in the nucleus contralateral to the UL. UL did not increase asymmetry in the responses of individual type I or II neurons to ipsilateral vs. contralateral rotation, nor does it change the power law relationship between neuronal firing and level of stimulation. Increased sensitivities of contralesional type I neurons to the remaining vestibular nerve input and increased efficacy of inhibitory vestibular commissures projecting to the ipsilesional vestibular nucleus appear to be responsible for recovery of dynamic function of central vestibular neurons in compensated animals. The portion of type I neurons on the ipsilesional side is reduced in compensated animals, which likely accounts for the asymmetries in vestibular reflexes and perception that characterize vestibular function after UL.

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Recent advances in head impulse test findings in central vestibular disorders

Neurology ◽

10.1212/wnl.0000000000005206 ◽

2018 ◽

Vol 90 (13) ◽

pp. 602-612 ◽

Cited By ~ 26

Author(s):

Jeong-Yoon Choi ◽

Hyo-Jung Kim ◽

Ji-Soo Kim

Keyword(s):

Vestibular Nucleus ◽

Head Rotation ◽

Medial Longitudinal Fasciculus ◽

Head Impulse Test ◽

Vestibular Disorders ◽

Head Impulse ◽

Acute Vestibular Syndrome ◽

Corrective Saccades ◽

Cerebellar Lesions ◽

Horizontal Head

The head impulse test (HIT) is used to evaluate the vestibulo-ocular reflex (VOR) during a high-velocity head rotation. Corrective catch-up saccades that occur during or after the HITs usually indicate peripheral vestibular hypofunction, whereas in acute vestibular syndrome, normal clinical (bedside) HITs should prompt a search for a central lesion. However, recent quantitative studies that evaluated HITs using magnetic search coils or video-based techniques have demonstrated that specific patterns of HIT abnormalities are associated with central vestibular disorders. While normal clinical HITs are typical of central lesions, discrepancies have been observed between clinical and quantitative HITs. The horizontal head impulse VOR gains can be significantly reduced unilaterally or bilaterally (positive HITs) in lesions involving the vestibular nucleus, nucleus prepositus hypoglossi, or flocculus. In diffuse cerebellar lesions, the VOR gain during horizontal head impulses may increase (hyperactive) with corrective saccades directed the opposite way. The presence of cross-coupled vertical corrective saccades during horizontal HITs is also suggestive of diffuse cerebellar lesions. Lesions involving the vestibular nucleus, medial longitudinal fasciculus, and cerebellum may show decreased or increased gains of the VOR during vertical HITs. Defining the differences in patterns observed during abnormal HITs may help practitioners localize the responsible lesions in both central and peripheral vestibulopathy.

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Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats

Frontiers in Neuroscience ◽

10.3389/fnins.2021.741571 ◽

2021 ◽

Vol 15 ◽

Author(s):

Tianwen Chen ◽

Jun Huang ◽

Yue Yu ◽

Xuehui Tang ◽

Chunming Zhang ◽

...

Keyword(s):

Eye Movements ◽

Vestibular Nucleus ◽

Head Rotation ◽

Vestibular Evoked Myogenic Potentials ◽

Type I ◽

Evoked Responses ◽

Vestibular Neurons ◽

Ocular Reflex ◽

Discharge Rates ◽

Vestibulo Ocular Reflex

Vestibular evoked myogenic potentials (VEMP) have been used to assess otolith function in clinics worldwide. However, there are accumulating evidence suggesting that the clinically used sound stimuli activate not only the otolith afferents, but also the canal afferents, indicating canal contributions to the VEMPs. To better understand the neural mechanisms underlying the VEMPs and develop discriminative VEMP protocols, we further examined sound-evoked responses of the vestibular nucleus neurons and the abducens neurons, which have the interneurons and motoneurons of the vestibulo-ocular reflex (VOR) pathways. Air-conducted clicks (50–80 dB SL re ABR threshold, 0.1 ms duration) or tone bursts (60–80 dB SL, 125–4,000 Hz, 8 ms plateau, 1 ms rise/fall) were delivered to the ears of Sprague-Dawley or Long-Evans rats. Among 425 vestibular nucleus neurons recorded in anesthetized rats and 18 abducens neurons recorded in awake rats, sound activated 35.9% of the vestibular neurons that increased discharge rates for ipsilateral head rotation (Type I neuron), 15.7% of the vestibular neurons that increased discharge rates for contralateral head rotation (Type II neuron), 57.2% of the vestibular neurons that did not change discharge rates during head rotation (non-canal neuron), and 38.9% of the abducens neurons. Sound sensitive vestibular nucleus neurons and abducens neurons exhibited characteristic tuning curves that reflected convergence of canal and otolith inputs in the VOR pathways. Tone bursts also evoked well-defined eye movements that increased with tone intensity and duration and exhibited peak frequency of ∼1,500 Hz. For the left eye, tone bursts evoked upward/rightward eye movements for ipsilateral stimulation, and downward/leftward eye movements for contralateral stimulation. These results demonstrate that sound stimulation results in activation of the canal and otolith VOR pathways that can be measured by eye tracking devices to develop discriminative tests of vestibular function in animal models and in humans.

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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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