Directional preference of otolith-related neurons in vestibular nucleus

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

Brain Sciences ◽

10.3390/brainsci11080987 ◽

2021 ◽

Vol 11 (8) ◽

pp. 987

Author(s):

Nguyen Nguyen ◽

Kyu-Sung Kim ◽

Gyutae Kim

Keyword(s):

Total Population ◽

Vestibular Nucleus ◽

Head Rotation ◽

Neuronal Responses ◽

Vestibular Neurons ◽

Chemically Induced ◽

Unilateral Labyrinthectomy ◽

Directional Preference ◽

Head Translation ◽

Horizontal Head

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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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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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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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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Effect of Korean Red Ginseng on Early Vestibular Function Restoration after Unilateral Labyrinthectomy

Research in Vestibular Science ◽

10.21790/rvs.2020.19.3.79 ◽

2020 ◽

Vol 19 (3) ◽

pp. 79-88

Author(s):

Jiyeon Lee ◽

Mi Joo Kim ◽

Gyu Cheol Han

Keyword(s):

Vestibular Function ◽

Red Ginseng ◽

Korean Red Ginseng ◽

Unilateral Labyrinthectomy

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GABA receptor efficacy in vestibular nucleus neurones after unilateral labyrinthectomy

The Japanese Journal of Pharmacology ◽

10.1016/s0021-5198(19)48140-7 ◽

2000 ◽

Vol 82 ◽

pp. 169

Author(s):

Toshiaki Yamanaka ◽

Hiroshi Hosoi ◽

Mayank B Dulia ◽

Takashi Matsunaga ◽

Masashi Sasa

Keyword(s):

Gaba Receptor ◽

Vestibular Nucleus ◽

Unilateral Labyrinthectomy

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Sound-evoked vestibular projections to the splenius capitis in humans: comparison with the sternocleidomastoid muscle

Journal of Applied Physiology ◽

10.1152/japplphysiol.00711.2018 ◽

2019 ◽

Vol 126 (6) ◽

pp. 1619-1629 ◽

Cited By ~ 6

Author(s):

Sally M. Rosengren ◽

Konrad P. Weber ◽

Sendhil Govender ◽

Miriam S. Welgampola ◽

Danielle L. Dennis ◽

...

Keyword(s):

Hearing Loss ◽

Motor Unit ◽

Vestibular Function ◽

Head Rotation ◽

Neck Muscle ◽

Vestibular Evoked Myogenic Potential ◽

Vestibular Loss ◽

Single Motor Unit ◽

Single Motor ◽

Splenius Capitis

The short-latency vestibulo-collic reflex in humans is well defined for only the sternocleidomastoid (SCM) neck muscle. However, other neck muscles also receive input from the balance organs and participate in neck stabilization. We therefore investigated the sound-evoked vestibular projection to the splenius capitis (SC) muscles by comparing surface and single motor unit responses in the SC and SCM muscles in 10 normal volunteers. We also recorded surface responses in patients with unilateral vestibular loss but preserved hearing and hearing loss but preserved vestibular function. The single motor unit responses were predominantly inhibitory, and the strongest responses were recorded in the contralateral SC and ipsilateral SCM. In both cases there was a significant decrease or gap in single motor unit activity, in SC at 11.7 ms for 46/66 units and in SCM at 12.7 ms for 51/58 motor units. There were fewer significant responses in the ipsilateral SC and contralateral SCM muscles, and they consisted primarily of weak increases in activity. Surface responses recorded over the contralateral SC were positive-negative during neck rotation, similar to the ipsilateral cervical vestibular evoked myogenic potential in SCM. Responses in SC were present in the patients with hearing loss and absent in the patient with vestibular loss, confirming their vestibular origin. The results describe a pattern of inhibition consistent with the synergistic relationship between these muscles for axial head rotation, with the crossed vestibular projection to the contralateral SC being weaker than the ipsilateral projection to the SCM. NEW & NOTEWORTHY We used acoustic vestibular stimulation to investigate the saccular projections to the splenius capitis (SC) and sternocleidomastoid (SCM) muscles in humans. Single motor unit recordings from within the muscles demonstrated strong inhibitory projections to the contralateral SC and ipsilateral SCM muscles and weak excitatory projections to the opposite muscle pair. This synergistic pattern of activation is consistent with a role for the reflex in axial rotation of the head.

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