Directional preference of otolith-related neurons in vestibular nucleus

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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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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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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Quantitative assessment of self-treated canalith repositioning procedures using inertial measurement unit sensors

Journal of Vestibular Research ◽

10.3233/ves-190747 ◽

2021 ◽

pp. 1-9

Author(s):

Chiheon Kwon ◽

Yunseo Ku ◽

Shinhye Seo ◽

Eunsook Jang ◽

Hyoun-Joong Kong ◽

...

Keyword(s):

Evaluation Criteria ◽

Head Rotation ◽

Large Error ◽

Head Movements ◽

The Self ◽

Measurement Unit ◽

Success Rates ◽

Home Based ◽

Epley Maneuver ◽

Head Rotations

BACKGROUND: Low success and high recurrence of benign paroxysmal positional vertigo (BPPV) after home-based self-treated Epley and Barbeque (BBQ) roll maneuvers is an important issue. OBJECTIVE: To quantify the cause of low success rate of self-treated Epley and BBQ roll maneuvers and provide a clinically acceptable criterion to guide self-treatment head rotations. METHODS: Twenty-five participants without active BPPV wore a custom head-mount rotation monitoring device for objective measurements. Self-treatment and specialist-assisted maneuvers were compared for head rotation accuracy. Absolute differences between the head rotation evaluation criteria (American Academy of Otolaryngology guidelines) and measured rotation angles were considered as errors. Self-treatment and specialist-treated errors in maneuvers were compared. Between-trial variations and age effects were evaluated. RESULTS: A significantly large error and between-trial variation occurred in step 4 of the self-treated Epley maneuver, with a considerable error in the second trial. The cumulative error of all steps of self-treated BBQ roll maneuver was significantly large. Age effect occurred only in the self-treated BBQ roll maneuver. Errors in specialist-treated maneuvers ranged from 10 to 20 degrees. CONCLUSIONS: Real-time feedback of head movements during simultaneous head-body rotations could increase success rates of self-treatments. Specialist-treated maneuvers can be used as permissible rotation margin criteria.

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“Torso Rotation”' experiments. 4: the role of vision and the cervico-ocular reflex in compensation for a deficient VOR

Journal of Vestibular Research ◽

10.3233/ves-1999-9203 ◽

1999 ◽

Vol 9 (2) ◽

pp. 89-101

Author(s):

L.J.G. Bouyer ◽

D.G.D. Watt

Keyword(s):

Motion Sickness ◽

Vestibular Function ◽

Repeated Exposure ◽

Head Movements ◽

Upper Body ◽

Calibration Data ◽

En Bloc ◽

Mean Velocity ◽

Gaze Stability ◽

Velocity Gain

Acute, reversible changes in human vestibular function can be produced by exposure to “Torso Rotation” (TR), a method involving the overuse of certain types of simple, self-generated movements. A single session results in multiple, short-lasting aftereffects, including perceptual illusions, VOR gain reduction,gaze and postural instability, and motion sickness. With repeated exposure, motion sickness susceptibility disappears and gaze stability improves. VOR gain continues to be reduced, however. Therefore, another gaze stabilizing system must come into play. Are visual and/or neck inputs involved in this functional compensation? Six subjects participated in this 7-day experiment. Eye and head movements were measured during 2 tests: 1) voluntary “head only” shaking between 0.3 and 3.0 Hz (lights off) and 2) voluntary “head and torso” shaking, moving the upper body en bloc (neck immobilized). Measurements were obtained before and repeatedly after TR. Velocity gain (eye velocity/head velocity) was determined for each of these tests. Each day, mean velocity gain during “head only” shaking in the dark (averaged over 1.0 to 2.0 Hz) dropped significantly after TR ( P < 0.01), with no long-term improvement ( P > 0.9). Similar results, although more noisy, were obtained for “head and torso” shaking. As a control, EOG calibration data confirmed that gaze stability in the light did improve over the 7 days of testing. This experiment demonstrates that the reduction in gaze instability following repeated exposure to TR results from an increased use of vision. It excludes the VOR, the COR, and predictive mechanisms (including efference copy) as contributors. In addition, in the 20 minutes following TR completion, gaze stability recovered less than during previous VOR testing in the dark. These results are compatible with the motion that exposure to TR leads to a change in sensorimotor strategy involving a de-emphasis of vestibular inputs.

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Horizontal Vestibuloocular Reflex Evoked by High-Acceleration Rotations in the Squirrel Monkey. II. Responses After Canal Plugging

Journal of Neurophysiology ◽

10.1152/jn.1999.82.3.1271 ◽

1999 ◽

Vol 82 (3) ◽

pp. 1271-1285 ◽

Cited By ~ 57

Author(s):

David M. Lasker ◽

Douglas D. Backous ◽

Anna Lysakowski ◽

Griffin L. Davis ◽

Lloyd B. Minor

Keyword(s):

High Frequency ◽

Peak Velocity ◽

Vestibular Function ◽

Semicircular Canals ◽

Vestibuloocular Reflex ◽

Half Cycle ◽

High Acceleration ◽

Linear And Nonlinear ◽

Residual Response ◽

Sinusoidal Rotations

The horizontal angular vestibuloocular reflex (VOR) evoked by high-frequency, high-acceleration rotations was studied in four squirrel monkeys after unilateral plugging of the three semicircular canals. During the period (1–4 days) that animals were kept in darkness after plugging, the gain during steps of acceleration (3,000°/s2, peak velocity = 150°/s) was 0.61 ± 0.14 (mean ± SD) for contralesional rotations and 0.33 ± 0.03 for ipsilesional rotations. Within 18–24 h after animals were returned to light, the VOR gain for contralesional rotations increased to 0.88 ± 0.05, whereas there was only a slight increase in the gain for ipsilesional rotations to 0.37 ± 0.07. A symmetrical increase in the gain measured at the plateau of head velocity was noted after animals were returned to light. The latency of the VOR was 8.2 ± 0.4 ms for ipsilesional and 7.1 ± 0.3 ms for contralesional rotations. The VOR evoked by sinusoidal rotations of 0.5–15 Hz, ±20°/s had no significant half-cycle asymmetries. The recovery of gain for these responses after plugging was greater at lower than at higher frequencies. Responses to rotations at higher velocities for frequencies ≥4 Hz showed an increase in contralesional half-cycle gain, whereas ipsilesional half-cycle gain was unchanged. A residual response that appeared to be canal and not otolith mediated was noted after plugging of all six semicircular canals. This response increased with frequency to reach a gain of 0.23 ± 0.03 at 15 Hz, resembling that predicted based on a reduction of the dominant time constant of the canal to 32 ms after plugging. A model incorporating linear and nonlinear pathways was used to simulate the data. The coefficients of this model were determined from data in animals with intact vestibular function. Selective increases in the gain for the linear and nonlinear pathways predicted the changes in recovery observed after canal plugging. An increase in gain of the linear pathway accounted for the recovery in VOR gain for both responses at the velocity plateau of the steps of acceleration and for the sinusoidal rotations at lower peak velocities. The increase in gain for contralesional responses to steps of acceleration and sinusoidal rotations at higher frequencies and velocities was due to an increase in the gain of the nonlinear pathway. This pathway was driven into inhibitory cutoff at low velocities and therefore made no contribution for rotations toward the ipsilesional side.

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Interstitial Nucleus of Cajal Encodes Three-Dimensional Head Orientations in Fick-Like Coordinates

Journal of Neurophysiology ◽

10.1152/jn.00379.2006 ◽

2007 ◽

Vol 97 (1) ◽

pp. 604-617 ◽

Cited By ~ 22

Author(s):

Eliana M. Klier ◽

Hongying Wang ◽

J. Douglas Crawford

Keyword(s):

Coordinate System ◽

Degrees Of Freedom ◽

Three Dimensional ◽

Semicircular Canals ◽

Head Rotation ◽

Head Orientation ◽

Interstitial Nucleus Of Cajal ◽

The Gaze ◽

Behavioral Constraints ◽

The Right

Two central, related questions in motor control are 1) how the brain represents movement directions of various effectors like the eyes and head and 2) how it constrains their redundant degrees of freedom. The interstitial nucleus of Cajal (INC) integrates velocity commands from the gaze control system into position signals for three-dimensional eye and head posture. It has been shown that the right INC encodes clockwise (CW)-up and CW-down eye and head components, whereas the left INC encodes counterclockwise (CCW)-up and CCW-down components, similar to the sensitivity directions of the vertical semicircular canals. For the eyes, these canal-like coordinates align with Listing’s plane (a behavioral strategy limiting torsion about the gaze axis). By analogy, we predicted that the INC also encodes head orientation in canal-like coordinates, but instead, aligned with the coordinate axes for the Fick strategy (which constrains head torsion). Unilateral stimulation (50 μA, 300 Hz, 200 ms) evoked CW head rotations from the right INC and CCW rotations from the left INC, with variable vertical components. The observed axes of head rotation were consistent with a canal-like coordinate system. Moreover, as predicted, these axes remained fixed in the head, rotating with initial head orientation like the horizontal and torsional axes of a Fick coordinate system. This suggests that the head is ordinarily constrained to zero torsion in Fick coordinates by equally activating CW/CCW populations of neurons in the right/left INC. These data support a simple mechanism for controlling head orientation through the alignment of brain stem neural coordinates with natural behavioral constraints.

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Responses to Moving Visual Stimuli in Pretectal Neurons of the Small-Spotted Dogfish (Scyliorhinus canicula)

Journal of Neurophysiology ◽

10.1152/jn.00926.2007 ◽

2008 ◽

Vol 99 (1) ◽

pp. 200-207 ◽

Cited By ~ 16

Author(s):

Olivia Andrea Masseck ◽

Klaus-Peter Hoffmann

Keyword(s):

Visual Information ◽

Visual Stimulation ◽

Semicircular Canals ◽

Neuronal Responses ◽

Vertical Movements ◽

Scyliorhinus Canicula ◽

Random Dot Patterns ◽

Pretectal Area ◽

Corpus Geniculatum Laterale ◽

Sensitive Direction

Single-unit recordings were performed from a retinorecipient pretectal area (corpus geniculatum laterale) in Scyliorhinus canicula. The function and homology of this nucleus has not been clarified so far. During visual stimulation with a random dot pattern, 45 (35%) neurons were found to be direction selective, 10 (8%) were axis selective (best neuronal responses to rotations in both directions around one particular stimulus axis), and 75 (58%) were movement sensitive. Direction-selective responses were found to the following stimulus directions (in retinal coordinates): temporonasal and nasotemporal horizontal movements, up- and downward vertical movements, and oblique movements. All directions of motion were represented equally by our sample of pretectal neurons. Additionally we tested the responses of 58 of the 130 neurons to random dot patterns rotating around the semicircular canal or body axes to investigate whether direction-selective visual information is mapped into vestibular coordinates in pretectal neurons of this chondrichthyan species. Again all rotational directions were represented equally, which argues against a direct transformation from a retinal to a vestibular reference frame. If a complete transformation had occurred, responses to rotational axes corresponding to the axes of the semicircular canals should have been overrepresented. In conclusion, the recorded direction-selective neurons in the Cgl are plausible detectors for retinal slip created by body rotations in all directions.

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A case series shows independent vestibular labyrinthine function after major surgical trauma to the human cochlea

Communications Medicine ◽

10.1038/s43856-021-00036-w ◽

2021 ◽

Vol 1 (1) ◽

Author(s):

Stefan K. Plontke ◽

Torsten Rahne ◽

Ian S. Curthoys ◽

Bo Håkansson ◽

Laura Fröhlich

Keyword(s):

Case Series ◽

Vestibular Function ◽

Semicircular Canals ◽

Vestibular Evoked Myogenic Potentials ◽

Head Impulse Test ◽

Surgical Trauma ◽

Cochlear Function ◽

Receptor System ◽

Tertiary Referral Center ◽

Significant Difference

Abstract Background The receptors for hearing and balance are housed together in the labyrinth of the inner ear and share the same fluids. Surgical damage to either receptor system was widely believed to cause certain permanent loss of the receptor function of the other. That principle, however, has been called into question because there have been anecdotal reports in individual patients of at least partial preservation of cochlear function after major surgical damage to the vestibular division and vice versa. Methods We performed specific objective vestibular function tests before and after surgical trauma (partial or subtotal cochlear removal) for treatment of intracochlear tumors in 27 consecutive patients in a tertiary referral center. Vestibular function was assessed by calorics (low-frequency response of the lateral semicircular canal), vestibulo-ocular reflex by video head impulse test (vHIT) of the three semicircular canals, cervical and ocular vestibular evoked myogenic potentials (cVEMP, saccule and oVEMP, utricle). Preoperative and postoperative distributions were compared with paired t-tests. Results Here we show that there was no significant difference between pre- and post-operative measures for all tests of the five vestibular organs, and that after major surgical cochlear trauma, the vestibular receptors continue to function independently. Conclusions These surprising observations have important implications for our understanding of the function and the surgery of the peripheral auditory and vestibular system in general and open up new possibilities for the development, construction and evaluation of neural interfaces for electrical or optical stimulation of the peripheral auditory and vestibular nervous system.

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Convergence of linear acceleration and yaw rotation signals on non-eye movement neurons in the vestibular nucleus of macaques

Journal of Neurophysiology ◽

10.1152/jn.00382.2017 ◽

2018 ◽

Vol 119 (1) ◽

pp. 73-83 ◽

Cited By ~ 4

Author(s):

Shawn D. Newlands ◽

Ben Abbatematteo ◽

Min Wei ◽

Laurel H. Carney ◽

Hongge Luan

Keyword(s):

Eye Movement ◽

Multisensory Integration ◽

Vestibular Nucleus ◽

Semicircular Canals ◽

Linear Acceleration ◽

Vestibular Nuclei ◽

Otolith Organs ◽

Angular Rotation ◽

Sensory Signals ◽

Nonlinear Integration

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.

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