Name: using unidirectional rotations to improve vestibular system asymmetry in patients with vestibular dysfunction
Uploaded: 2019-08-30T15:00:00
Description: Watch this Scientific Journal Video about Using Unidirectional Rotations to Improve Vestibular System Asymmetry in Patients with Vestibular Dysfunction at JoVE.com

N. R. was supported by a research fund from Shahid Beheshti University of Medical Sciences and Health Services. S. G. S. was supported by NIDCD R03 DC015091 grant.

The data presented here and previously published3 were obtained by studies carried out in accordance with the recommendations of the Ethics Committee of Shahid Beheshti University of Medical Sciences, Tehran, Iran and a protocol that was approved by the Institutional Review Board of the University.
1. Participant screening and preparation
<ol>
	<li>Recruit participants who have had a history of balance problems for more than one year. 
	NOTE: Vestibular compensat...

<ol>
	<li>Agrawal, Y., Ward, B. K., Minor, L. B. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Vestibular+dysfunction:+prevalence,+impact+and+need+for+targeted+treatment.">Vestibular dysfunction: prevalence, impact and need for targeted treatment.</a> Journal of Vestibular Research. 23 (3), 113-117 (2013).</li><li>Huterer, M., Cullen, K. E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Vestibuloocular+reflex+dynamics+during+high-frequency+and+high-acceleration+rotations+of+the+head+on+body+in+rhesus+monkey.">Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey.</a> Journal of Neurophysiology. 88 (1), 13-28 (2002).</li><li>Sadeghi, N. G., Sabetazad, B., Rassaian, N., Sadeghi, S. G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Rebalancing+the+Vestibular+System+by+Unidirectional+Rotations+in+Patients+With+Chronic+Vestibular+Dysfunction.">Rebalancing the Vestibular System by Unidirectional Rotations in Patients With Chronic Vestibular Dysfunction.</a> Frontiers in Neurology. 9, 1196 (2018).</li><li>Beraneck, M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Long-term+plasticity+of+ipsilesional+medial+vestibular+nucleus+neurons+after+unilateral+labyrinthectomy.">Long-term plasticity of ipsilesional medial vestibular nucleus neurons after unilateral labyrinthectomy.</a> Journal of Neurophysiology. 90 (1), 184-203 (2003).</li><li>Beraneck, M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Unilateral+labyrinthectomy+modifies+the+membrane+properties+of+contralesional+vestibular+neurons.">Unilateral labyrinthectomy modifies the membrane properties of contralesional vestibular neurons.</a> Journal of Neurophysiology. 92 (3), 1668-1684 (2004).</li><li>Sadeghi, S. G., Minor, L. B., Cullen, K. E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Neural+correlates+of+motor+learning+in+the+vestibulo-ocular+reflex:+dynamic+regulation+of+multimodal+integration+in+the+macaque+vestibular+system.">Neural correlates of motor learning in the vestibulo-ocular reflex: dynamic regulation of multimodal integration in the macaque vestibular system.</a> Journal of Neuroscience. 30 (30), 10158-10168 (2010).</li><li>Sadeghi, S. G., Minor, L. B., Cullen, K. 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E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Response+of+vestibular-nerve+afferents+to+active+and+passive+rotations+under+normal+conditions+and+after+unilateral+labyrinthectomy.">Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy.</a> Journal of Neurophysiology. 97 (2), 1503-1514 (2007).</li><li>Sadeghi, S. G., Minor, L. B., Cullen, K. E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Dynamics+of+the+horizontal+vestibuloocular+reflex+after+unilateral+labyrinthectomy:+response+to+high+frequency,+high+acceleration,+and+high+velocity+rotations.">Dynamics of the horizontal vestibuloocular reflex after unilateral labyrinthectomy: response to high frequency, high acceleration, and high velocity rotations.</a> Experimental Brain Research. 175 (3), 471-484 (2006).</li><li>Halmagyi, G. M., Black, R. A., Thurtell, M. J., Curthoys, I. 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C., Lasker, D. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Unidirectional+rotations+produce+asymmetric+changes+in+horizontal+VOR+gain+before+and+after+unilateral+labyrinthectomy+in+macaques.">Unidirectional rotations produce asymmetric changes in horizontal VOR gain before and after unilateral labyrinthectomy in macaques.</a> Experimental Brain Research. 210 (3-4), 651-660 (2011).</li><li>Whitney, S. L., Rossi, M. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Efficacy+of+vestibular+rehabilitation.">Efficacy of vestibular rehabilitation.</a> Otolaryngology Clinics of North America. 33 (3), 659-672 (2000).</li><li>Telian, S. A., Shepard, N. 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An abridged version of a Cochrane Review.</a> European Journal of Physical Rehabilitation Medicine. 52 (4), 541-556 (2016).</li><li>Denham, T., Wolf, A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Vestibular+rehabilitation.">Vestibular rehabilitation.</a> Rehabilitation Management. 10 (3), 93-94 (1997).</li><li>Cooksey, F. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Rehabilitation+in+Vestibular+Injuries.">Rehabilitation in Vestibular Injuries.</a> Proceedings of the Royal Society of Medicine. 39 (5), 273-278 (1946).</li><li>Enticott, J. C., Vitkovic, J. 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M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=.">.</a> Disorders of the vestibular system. , (1996).</li><li>Furman, J. M., Cass, S. P., Furman, J. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=.">.</a> Vestibular disorders: a case-study approach. , (2003).</li><li>Brey, R. H., McPherson, J. H., Lynch, R. M., Jacobson, G. P., Shepard, N. T. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=.">.</a> Balance Function Assessment and Management. , 253-280 (2008).</li><li>Funabiki, K., Naito, Y. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Validity+and+limitation+of+detection+of+peripheral+vestibular+imbalance+from+analysis+of+manually+rotated+vestibulo-ocular+reflex+recorded+in+the+routine+vestibular+clinic.">Validity and limitation of detection of peripheral vestibular imbalance from analysis of manually rotated vestibulo-ocular reflex recorded in the routine vestibular clinic.</a> Acta Otolaryngology. 122 (1), 31-36 (2002).</li><li>Zalewski, C. K. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=.">.</a> Rotational Vestibular Assessment. , (2018).</li><li>Furman, J. M., Cass, S. P., Baloh, R. W., Halmagyi, G. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Ch.+17.">Ch. 17.</a> Disorders of the vestibular system. , 191-210 (1996).</li><li>Desmond, A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=.">.</a> Vestibular function: evaluation and treatment. , (2004).</li><li>Shepard, N. T., Goulson, A. M., McPherson, J. H., Jacobson, G. P., Shepard, N. T. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Ch.+15.">Ch. 15.</a> Balance function assessment and management. , 365-390 (2016).</li><li>Clement, G., Flandrin, J. M., Courjon, J. H. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Comparison+between+habituation+of+the+cat+vestibulo-ocular+reflex+by+velocity+steps+and+sinusoidal+vestibular+stimulation+in+the+dark.">Comparison between habituation of the cat vestibulo-ocular reflex by velocity steps and sinusoidal vestibular stimulation in the dark.</a> Experimental Brain Research. 142 (2), 259-267 (2002).</li><li>Clement, G., Tilikete, C., Courjon, J. 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The rehabilitation method presented here consists of repeated unidirectional rotations in the dark toward the less responsive (LR) side in patients with vestibular imbalance and VOR asymmetry. Most rehabilitation techniques enhance multisensory integration in order to improve balance16,17,18,19,20. The method presented here targets the vestibular pathway, and ...

Vestibular dysfunction is a common disorder with a prevalence of ~35% in adults above 40 years old1. Most vestibular disorders result in an asymmetry between input from both sides, resulting in an illusion of rotation called vertigo. In the absence of normal vestibular function, even simple daily activities can be challenging. Vestibular dysfunction is often quantified by the vestibulo-ocular reflex (VOR). During natural activities, such as walking or running, the VOR moves the eyes in the opposite direction&#160;and with the same velocity as head movement. This reflex has a short latency of ~5 ms, and it is mediated in the horizontal plane through a simple, three-neuron arc2. The information travels from vestibular receptors to the vestibular nuclei, then to the abducens motor neurons. These eye movements result in stabilization of horizontal gaze during daily activities. The symmetry of the VOR in response to clockwise and counterclockwise rotations is an important test of vestibular function.
Unilateral vestibular dysfunction produces central compensatory changes and centrally driven peripheral changes to overcome defective asymmetric VOR and resulting vestibular imbalance. Even after permanent vestibular lesions, such as a unilateral vestibular neurectomy, the vertigo and accompanying symptoms improve over a short period (days to weeks) of time. Due to this ability, the vestibular system has been a model for studying adaptation and compensation in neural pathways. It has been previously shown3 that changes in central vestibular pathways can be implemented by a unidirectional rotation based on a hypothesis proposed by one of the authors (N.R.) about 20 years ago. Other studies have also shown compensatory changes in different parts of the sensory pathway, including the vestibular nuclei (VN)4,5,6,7,8, commissural pathways between the VN on both sides9, cerebellar inputs10, and the vestibular periphery11. These compensatory changes result in a new balance in the activity of VN neurons on both sides.
Despite the impressive ability of the vestibular system to compensate for asymmetric inputs from the two ears, research has shown that responses to fast movements are never fully compensated12,13. It is now known that natural vestibular compensation does not use the full capacity of the system, and the compensated VOR response can be improved in animals that have participated in visual-vestibular training14,15. It has long been known that vestibular rehabilitation exercises improve the compensation in patients with chronic imbalance problems by enhancing the (non-vestibular) multisensory nature of balance control16,17,18,19,20,21. The goal of these vestibular rehabilitation exercises is to use physiological or behavioral approaches to improve symptoms as well as a patient&#39;s quality of life and independence22,23.
Described herein is a rehabilitation method that uses unidirectional rotations toward the &#34;weaker&#34; side (Figure 1A). The basic idea for this method comes from Hebbian plasticity, in which neural connections become stronger when they are stimulated. This method specifically modifies vestibular inputs rather than enhancing multisensory integration, which is the basis for other vestibular rehabilitation exercises. Previous research has shown that unidirectional rotations decreases VOR asymmetry in 1-2 sessions in patients with unilateral vestibular dysfunction3. This effect was mainly due to an increase in the activity of the side with a lower response (LR), as well as a slight decrease in the activity of the side with a higher response (HR). This change is most likely mediated by modifications in the central pathways (e.g., strengthening of afferent pathways, such as VN connections or changes in commissural inputs). In effect, this technique may be used as a supervised method for vestibular rehabilitation in those with longstanding vestibular asymmetry.

<table border="1" fo:keep-together.within-page="1" fo:keep-with-next.within-page="always">
	<tbody>
		<tr>
			<td>VEST operating and analysis software</td>
			<td>NeuroKinetics</td>
			<td></td>
			<td></td>
		</tr>
		<tr>
			<td>Electronystagmograph</td>
			<td>Nicolet</td>
			<td>Spirit Model 1992</td>
			<td>Equipment used for collecting the data presented in the Results section</td>
		</tr>
		<tr>
			<td>I-Portal NOTC (Neurotologic Test Center)</td>
			<td>NeuroKinetics</td>
			<td></td>
			<td>Equipment shown for current studies and shown in the movie</td>
		</tr>
	</tbody>
</table>

using unidirectional rotations to improve vestibular system asymmetry in patients with vestibular dysfunction

The vestibular system provides information about head movement and mediates reflexes that contribute to balance control and gaze stabilization during daily activities. Vestibular sensors are located in the inner ear on both sides of the head and project to the vestibular nuclei in the brainstem. Vestibular dysfunction is often due to an asymmetry between input from the two sides. This results in asymmetrical neural inputs from the two ears, which can produce an illusion of rotation, manifested as vertigo. The vestibular system has an impressive capacity for compensation, which serves to rebalance how asymmetrical information from the sensory end organs on both sides is processed at the central level. To promote compensation, various rehabilitation programs are used in the clinic; however, they primarily use exercises that improve multisensory integration. Recently, visual-vestibular training has also been used to improve the vestibulo-ocular reflex (VOR) in animals with compensated unilateral lesions. Here, a new method is introduced for rebalancing the vestibular activity on both sides in human subjects. This method consists of five unidirectional rotations in the dark (peak velocity of 320&#176;/s) toward the weaker side. The efficacy of this method was shown in a sequential, double-blinded clinical trial in 16 patients with VOR asymmetry (measured by the directional preponderance in response to sinusoidal rotations). In most cases, VOR asymmetry decreased after a single session, reached normal values within the first two sessions in one week, and the effects lasted up to 6 weeks. The rebalancing effect is due to both an increase in VOR response from the weaker side and a decrease in response from the stronger side. The findings suggest that unidirectional rotation can be used as a supervised rehabilitation method to reduce VOR asymmetry in patients with longstanding vestibular dysfunction.

Short-term effects of the unidirectional rotation were evaluated by measuring the VOR with a 0.2 Hz (40&#176;/s) sinusoidal rotation test at 70 min after rehabilitation3. Figure 2 shows the peak eye velocities during the VOR responses to rotations in the two directions (Figure 2A) and the change in the DP (Figure 2B). Following unidirectional rotation, the response to rotation...

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Using Unidirectional Rotations to Improve Vestibular System Asymmetry in Patients with Vestibular Dysfunction

A new rehabilitation method is presented for rebalancing the vestibular system in patients with asymmetric responses, which consists of unidirectional rotations toward the weaker side. By directly modifying the vestibular pathway rather than enhancing the multisensory aspects of compensation, asymmetry can be normalized within 1-2 sessions and show lasting effects.

The vestibular system provides information about head movement and mediates reflexes that contribute to balance control and gaze stabilization during ...

Stimulating the weaker side and inhibiting the stronger side, an idea originally proposed by Doctor Nayer Rassaian, has been demonstrated to decrease assymetry in individuals with vestibular imbalance. This technique provides a unique method for effectively stimulating the vestibular system in the dark and does not require complicated equipment. Unidirectional rotation could be used as a rehabilitation option for patients with an imbalance between vestibular inputs from the two sides as quantified by the vestibulo-ocular reflex.This methods requires a rotating chair and professional supervision. The critical aspect is the slow deceleration to avoid stimulation of the opposite side at the end of the unidirectional rotation. To measure the vestibulo-ocular reflex, have the participant in a rotary chair and secure the participant with the harness.Give the participant a pair of infrared goggles and fix the head in the headrest in the nose-down position at a 30-degree angle. After the participant has acclimated to the dark, have the participant look at laser targets projected on the wall at plus or minus 10-degree angles to calibrate the eye tracker. When the eye tracker has been calibrated accurately and the participant is ready, initiate a unidirectional rotation that consists of an asymmetric triangular velocity profile with an acceleration of 80 degrees per second squared over four seconds to reach a maximum velocity of 320 degrees per seconds.To keep the participant alert and distracted during the testing, ask questions or have the participant perform mental arithmetic. Can you tell me all of the cities in Australia? Sydney, Canberra, Melbourne.When the maximum velocity has been reached, slowly decelerate the rotation at 10 degrees per second squared to come to a full stop in about 30 seconds. It is critical to slow down the chair gradually to ensure that only the weaker side is simulated and that the stronger side is inhibited during the unilateral rotation. After the unidirectional rotation, have the participant remain in the chair to allow testing of the symmetry with the bidirectional sinusoidal harmonic acceleration rotation test at 0.05, 0.2, and 0.8-hertz frequencies with a peak velocity of 60 degrees per second at 40 and 70 minutes post unidirectional rotation.Here, the peak eye velocity is measure during a sinusoidal rotation test in response to the rotations in the two directions and the change in the directional preponderance 70 minutes after rehabilitation are shown. Following the unidirectional rotation, the response to the rotations and the direction of the side with the lower response was increased and the response to the rotations in the direction with the stronger response decreased resulting in a change in the directional preponderance value due to the decrease in the vestibulo-ocular reflex assymetry. Exposing subjects the unidirectional rotation during multiple sessions further decreases the directional preponderance value, an effect that is retained between sessions and that results in most of the subjects exhibiting a directional preponderance in the normal range after only two sessions.Although it is important to reach the effective peak velocity, slow declaration is critical part of rotation to ensure that the stimulation remains predominantly unidirectional. This method is safe and was well tolerated by subjects. Future studies that required to investigate how changes in the stimulation parameters, such as the peak acceleration and number of rotations, affect the efficacy and time course of the results.Some questions that we plan to investigate include, how long does this effect last and are the eye movement changes paralleled by changes in subjective symptoms, such as imbalance and disease?

Research

JoVE Journal

Behavior

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