Effects of Visual Input Changes on Canal and Otolith- Dependent Vestibulo-Ocular Reflexes: A Review Study
Abstract
Background and Aim: There is an integration between visual and vestibular systems. Changes in visual inputs can result in different changes in the Vestibulo-Ocular Reflex (VOR). This review study investigate the changes in VOR due to changes in visual inputs. In this regard, the effects of different conditions such as visual deprivation, changes in visual acuity, visual-vestibular conflict, and binocular vision dysfunction on VOR were assessed.
Recent Findings: Changes in visual inputs and visual-vestibular conflicts can lead to different changes in VOR.
Conclusion: The changes in VOR effects vary from slight to severe transformation dependent on the time course, severity and duration of changes in visual inputs.
[1] Thakar A. Does spectacle use lead to vestibular suppression? J Laryngol Otol. 2016;130(11):1033-8. [DOI:10.1017/S0022215116009051]
[2] Bronstein AM, Patel M, Arshad Q. A brief review of the clinical anatomy of the vestibular-ocular connections-how much do we know? Eye (Lond). 2015;29(2):163-70. [DOI:10.1038/eye.2014.262]
[3] Rinaudo CN, Schubert MC, Figtree WVC, Todd CJ, Migliaccio AA. Human vestibulo-ocular reflex adaptation is frequency selective. J Neurophysiol. 2019;122(3):984-93. [DOI:10.1152/jn.00162.2019]
[4] Schubert MC, Migliaccio AA. New advances regarding adaptation of the vestibulo-ocular reflex. J Neurophysiol. 2019;122(2):644-58. [DOI:10.1152/jn.00729.2018]
[5] Jones GM. Plasticity in the adult vestibulo-ocular reflex arc. Philos Trans R Soc Lond B Biol Sci. 1977;278(961):319-34. [DOI:10.1098/rstb.1977.0045]
[6] Willis JR, Vitale SE, Agrawal Y, Ramulu PY. Visual impairment, uncorrected refractive error, and objectively measured balance in the United States. JAMA Ophthalmol. 2013;131(8):1049-56. [DOI:10.1001/jamaophthalmol.2013.316]
[7] Kömpf D, Piper HF. Eye movements and vestibulo-ocular reflex in the blind. J Neurol. 1987;234(5):337-41. [DOI:10.1007/BF00314291]
[8] Leigh RJ, Zee DS. Eye movements of the blind. Invest Ophthalmol Vis Sci. 1980;19(3):328-31.
[9] Berthoz A, Jeannerod M, Vital-Durand F, Oliveras JL. Development of vestibulo-ocular responses in visually deprived kittens. Exp Brain Res. 1975;23(4):425-42. [DOI:10.1007/BF00238024]
[10] Harris LR, Cynader M. The eye movements of the darkreared cat. Exp Brain Res. 1981;44(1):41-56. [DOI:10.1007/BF00238748]
[11] Collewijn H. Optokinetic and vestibulo-ocular reflexes in dark-reared rabbits. Exp Brain Res. 1977;27(3-4):287-300. [DOI:10.1007/BF00235504]
[12] Chihara Y, Iwasaki S, Ushio M, Fujimoto C, Kashio A, Kondo K, et al. Ocular vestibular-evoked myogenic potentials (oVEMPs) require extraocular muscles but not facial or cochlear nerve activity. Clin Neurophysiol. 2009;120(3):581-7. [DOI:10.1016/j.clinph.2008.12.030]
[13] Bayram A, Kalkan M, Ünsal N, Kale A, Küçük B, Mutlu C. Does blindness affect ocular vestibular evoked myogenic potentials? Am J Otolaryngol. 2018;39(3):290-2. [DOI:10.1016/j.amjoto.2018.03.010]
[14] Rosengren SM, McAngus Todd NP, Colebatch JG. Vestibular-evoked extraocular potentials produced by stimulation with bone-conducted sound. Clin Neurophysiol. 2005;116(8):1938-48. [DOI:10.1016/j.clinph.2005.03.019]
[15] Chihara Y, Iwasaki S, Ushio M, Murofushi T. Vestibularevoked extraocular potentials by air-conducted sound: another clinical test for vestibular function. Clin Neurophysiol. 2007;118(12):2745-51. [DOI:10.1016/j.clinph.2007.08.005]
[16] Huang YC, Yang TL, Young YH. Feasibility of ocular vestibular-evoked myogenic potentials (oVEMPs) recorded with eyes closed. Clin Neurophysiol. 2012;123(2):376-81. [DOI:10.1016/j.clinph.2011.06.024]
[17] Todai JK, Congdon SL, Sangi-Haghpeykar H, Cohen HS. Ocular vestibular evoked myogenic potentials in response to three test positions and two frequencies. Laryngoscope. 2014;124(6):E237-40. [DOI:10.1002/lary.24487]
[18] González EG, Shi R, Tarita-Nistor L, Mandelcorn ED, Mandelcorn MS, Steinbach MJ. Image Stabilization in Central Vision Loss: The Horizontal Vestibulo-Ocular Reflex. Vision (Basel). 2018;2(2):19. [DOI:10.3390/vision2020019]
[19] Jha RH, Singh NK, Kumar P. Video Head Impulse Test in Persons with Blindness: Feasibility and Outcomes. J Am Acad Audiol. 2022;33(3):116-24. [DOI:10.1055/s-0041-1739534]
[20] Abstracts of the 31st Bárány Society Meeting, Madrid, Spain, May 9-11, 2022. J Vestib Res. 2022;32(s1):SI-S327. [DOI:10.3233/VES-220211]
[21] Judge PD, Rodriguez AI, Barin K, Janky KL. Impact of Target Distance, Target Size, and Visual Acuity on the Video Head Impulse Test. Otolaryngol Head Neck Surg. 2018;159(4):739-42. [DOI:10.1177/0194599818779908]
[22] Li C, Layman AJ, Geary R, Anson E, Carey JP, Ferrucci L, et al. Epidemiology of vestibulo-ocular reflex function: data from the Baltimore Longitudinal Study of Aging. Otol Neurotol. 2015;36(2):267-72. [DOI:10.1097/MAO.0000000000000610]
[23] van Dooren TS, Lucieer FMP, Janssen AML, Kingma H, van de Berg R. The Video Head Impulse Test and the Influence of Daily Use of Spectacles to Correct a Refractive Error. Front Neurol. 2018;9:125. [DOI:10.3389/fneur.2018.00125]
[24] Wu TY, Wang YX, Li XM. Applications of dynamic visual acuity test in clinical ophthalmology. Int J Ophthalmol. 2021;14(11):1771-8. [DOI:10.18240/ijo.2021.11.18]
[25] Gonshor A, Jones GM. Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol. 1976;256(2):361-79. [DOI:10.1113/jphysiol.1976.sp011329]
[26] Gonshor A, Jones GM. Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol. 1976;256(2):381-414. [DOI:10.1113/jphysiol.1976.sp011330]
[27] Wedtgrube A, Bockisch CJ, Straumann D, Tarnutzer AA. Prolonged Static Whole-Body Roll-Tilt and Optokinetic Stimulation Significantly Bias the Subjective Postural Vertical in Healthy Human Subjects. Front Neurol. 2020;11:595975. [DOI:10.3389/fneur.2020.595975]
[28] Castro P, Hussain S, Mohamed OG, Kaski D, Arshad Q, Bronstein AM, et al. Visuospatial orientation: Differential effects of head and body positions. Neurosci Lett. 2022;775:136548. [DOI:10.1016/j.neulet.2022.136548]
[29] Iranfar S, Jalilvand Karimi L, Shaabani M, Sharifian Alborzi M, Akbarzadeh Baghban A. [Subjective visual vertical test: the effect of preset angle and visual background]. J Rehab Med. 2013;2(2):47-54. Persian.
[30] Ito M, Shiida T, Yagi N, Yamamoto M. The cerebellar modification of rabbit’s horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation. Proc Jpn Acad Ser B Phys Biol Sci. 1974;50(1):85-9. [DOI:10.2183/pjab1945.50.85]
[31] Jones GM, Davies P. Adaptation of cat vestibulo-ocular reflex to 200 days of optically reversed vision. Brain Res. 1976;103(3):551-4. [DOI:10.1016/0006-8993(76)90454-6]
[32] Robinson DA. Adaptive gain control of vestibuloocular reflex by the cerebellum. J Neurophysiol. 1976;39(5):954-69. [DOI:10.1152/jn.1976.39.5.954]
[33] Miles FA, Eighmy BB. Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. J Neurophysiol. 1980;43(5):1406-25. [DOI:10.1152/jn.1980.43.5.1406]
[34] Freedman W, Carroll JR, McElligott JG. Comparison of vestibulo-ocular reflex (VOR) modification methods in cats. Vision Res. 1990;30(10):1525-8. [DOI:10.1016/0042-6989(90)90034-I]
[35] Miles FA, Fuller JH. Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. Brain Res. 1974;80(3):512-6. [DOI:10.1016/0006-8993(74)91035-X]
[36] Demer JL, Goldberg J, Jenkins HA, Porter FI. Vestibulo-ocular reflex during magnified vision: adaptation to reduce visual-vestibular conflict. Aviat Space Environ Med. 1987;58(9 Pt 2):A175-9.
[37] Demer JL, Porter FI, Goldberg J, Jenkins HA, Schmidt K. Adaptation to telescopic spectacles: vestibulo-ocular reflex plasticity. Invest Ophthalmol Vis Sci. 1989;30(1):159-70.
[38] Gauthier GM, Robinson DA. Adaptation of the human vestibuloocular reflex to magnifying lenses. Brain Res. 1975;92(2):331-5. [DOI:10.1016/0006-8993(75)90279-6]
[39] Istl-Lenz Y, Hydén D, Schwarz DW. Response of the human vestibulo-ocular reflex following long-term 2x magnified visual input. Exp Brain Res. 1985;57(3):448-55. [DOI:10.1007/BF00237831]
[40] Collewijn H, Martins AJ, Steinman RM. Compensatory eye movements during active and passive head movements: fast adaptation to changes in visual magnification. J Physiol. 1983;340:259-86. [DOI:10.1113/jphysiol.1983.sp014762]
[41] Michaelides E, Schutt CA. The correlation between the vestibulo-ocular reflex and multi-focal ocular correction: implications for vestibular compensation. Am J Otolaryngol. 2014;35(5):572-6. [DOI:10.1016/j.amjoto.2014.06.003]
[42] Cannon SC, Leigh RJ, Zee DS, Abel LA. The effect of the rotational magnification of corrective spectacles on the quantitative evaluation of the VOR. Acta Otolaryngol. 1985;100(1-2):81-8. [DOI:10.3109/00016488509108591]
[43] Carcaud J, França de Barros F, Idoux E, Eugène D, Reveret L, Moore LE, et al. Long-Lasting Visuo-Vestibular Mismatch in Freely-Behaving Mice Reduces the Vestibulo-Ocular Reflex and Leads to Neural Changes in the Direct Vestibular Pathway. eNeuro. 2017;4(1):ENEURO.0290-16.2017. [DOI:10.1523/ENEURO.0290-16.2017]
[44] Crane BT, Demer JL. Effect of adaptation to telescopic spectacles on the initial human horizontal vestibuloocular reflex. J Neurophysiol. 2000;83(1):38-49. [DOI:10.1152/jn.2000.83.1.38]
[45] Kheradmand A, Zee DS. Cerebellum and ocular motor control. Front Neurol. 2011;2:53. [DOI:10.3389/fneur.2011.00053]
[46] Miles FA, Lisberger SG. Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci. 1981;4:273-99. [DOI:10.1146/annurev.ne.04.030181.001421]
[47] Sehizadeh M. Monocular adaptation of vestibulo-ocular reflex (VOR). [Master’s thesis]. Waterloo, Ontario, Canada: University of Waterloo; 2005.
[48] Viirre E, Cadera W, Vilis T. The pattern of changes produced in the saccadic system and vestibuloocular reflex by visually patching one eye. J Neurophysiol. 1987;57(1):92-103. [DOI:10.1152/jn.1987.57.1.92]
[49] Griffin JR, Grisham JD. Normal binocular vision. Binocular anomalies, Diagnosis and vision therapy. 4th ed. Boston, MA: Butterworth-Heinemann; 2002. p. 3, 6.
[2] Bronstein AM, Patel M, Arshad Q. A brief review of the clinical anatomy of the vestibular-ocular connections-how much do we know? Eye (Lond). 2015;29(2):163-70. [DOI:10.1038/eye.2014.262]
[3] Rinaudo CN, Schubert MC, Figtree WVC, Todd CJ, Migliaccio AA. Human vestibulo-ocular reflex adaptation is frequency selective. J Neurophysiol. 2019;122(3):984-93. [DOI:10.1152/jn.00162.2019]
[4] Schubert MC, Migliaccio AA. New advances regarding adaptation of the vestibulo-ocular reflex. J Neurophysiol. 2019;122(2):644-58. [DOI:10.1152/jn.00729.2018]
[5] Jones GM. Plasticity in the adult vestibulo-ocular reflex arc. Philos Trans R Soc Lond B Biol Sci. 1977;278(961):319-34. [DOI:10.1098/rstb.1977.0045]
[6] Willis JR, Vitale SE, Agrawal Y, Ramulu PY. Visual impairment, uncorrected refractive error, and objectively measured balance in the United States. JAMA Ophthalmol. 2013;131(8):1049-56. [DOI:10.1001/jamaophthalmol.2013.316]
[7] Kömpf D, Piper HF. Eye movements and vestibulo-ocular reflex in the blind. J Neurol. 1987;234(5):337-41. [DOI:10.1007/BF00314291]
[8] Leigh RJ, Zee DS. Eye movements of the blind. Invest Ophthalmol Vis Sci. 1980;19(3):328-31.
[9] Berthoz A, Jeannerod M, Vital-Durand F, Oliveras JL. Development of vestibulo-ocular responses in visually deprived kittens. Exp Brain Res. 1975;23(4):425-42. [DOI:10.1007/BF00238024]
[10] Harris LR, Cynader M. The eye movements of the darkreared cat. Exp Brain Res. 1981;44(1):41-56. [DOI:10.1007/BF00238748]
[11] Collewijn H. Optokinetic and vestibulo-ocular reflexes in dark-reared rabbits. Exp Brain Res. 1977;27(3-4):287-300. [DOI:10.1007/BF00235504]
[12] Chihara Y, Iwasaki S, Ushio M, Fujimoto C, Kashio A, Kondo K, et al. Ocular vestibular-evoked myogenic potentials (oVEMPs) require extraocular muscles but not facial or cochlear nerve activity. Clin Neurophysiol. 2009;120(3):581-7. [DOI:10.1016/j.clinph.2008.12.030]
[13] Bayram A, Kalkan M, Ünsal N, Kale A, Küçük B, Mutlu C. Does blindness affect ocular vestibular evoked myogenic potentials? Am J Otolaryngol. 2018;39(3):290-2. [DOI:10.1016/j.amjoto.2018.03.010]
[14] Rosengren SM, McAngus Todd NP, Colebatch JG. Vestibular-evoked extraocular potentials produced by stimulation with bone-conducted sound. Clin Neurophysiol. 2005;116(8):1938-48. [DOI:10.1016/j.clinph.2005.03.019]
[15] Chihara Y, Iwasaki S, Ushio M, Murofushi T. Vestibularevoked extraocular potentials by air-conducted sound: another clinical test for vestibular function. Clin Neurophysiol. 2007;118(12):2745-51. [DOI:10.1016/j.clinph.2007.08.005]
[16] Huang YC, Yang TL, Young YH. Feasibility of ocular vestibular-evoked myogenic potentials (oVEMPs) recorded with eyes closed. Clin Neurophysiol. 2012;123(2):376-81. [DOI:10.1016/j.clinph.2011.06.024]
[17] Todai JK, Congdon SL, Sangi-Haghpeykar H, Cohen HS. Ocular vestibular evoked myogenic potentials in response to three test positions and two frequencies. Laryngoscope. 2014;124(6):E237-40. [DOI:10.1002/lary.24487]
[18] González EG, Shi R, Tarita-Nistor L, Mandelcorn ED, Mandelcorn MS, Steinbach MJ. Image Stabilization in Central Vision Loss: The Horizontal Vestibulo-Ocular Reflex. Vision (Basel). 2018;2(2):19. [DOI:10.3390/vision2020019]
[19] Jha RH, Singh NK, Kumar P. Video Head Impulse Test in Persons with Blindness: Feasibility and Outcomes. J Am Acad Audiol. 2022;33(3):116-24. [DOI:10.1055/s-0041-1739534]
[20] Abstracts of the 31st Bárány Society Meeting, Madrid, Spain, May 9-11, 2022. J Vestib Res. 2022;32(s1):SI-S327. [DOI:10.3233/VES-220211]
[21] Judge PD, Rodriguez AI, Barin K, Janky KL. Impact of Target Distance, Target Size, and Visual Acuity on the Video Head Impulse Test. Otolaryngol Head Neck Surg. 2018;159(4):739-42. [DOI:10.1177/0194599818779908]
[22] Li C, Layman AJ, Geary R, Anson E, Carey JP, Ferrucci L, et al. Epidemiology of vestibulo-ocular reflex function: data from the Baltimore Longitudinal Study of Aging. Otol Neurotol. 2015;36(2):267-72. [DOI:10.1097/MAO.0000000000000610]
[23] van Dooren TS, Lucieer FMP, Janssen AML, Kingma H, van de Berg R. The Video Head Impulse Test and the Influence of Daily Use of Spectacles to Correct a Refractive Error. Front Neurol. 2018;9:125. [DOI:10.3389/fneur.2018.00125]
[24] Wu TY, Wang YX, Li XM. Applications of dynamic visual acuity test in clinical ophthalmology. Int J Ophthalmol. 2021;14(11):1771-8. [DOI:10.18240/ijo.2021.11.18]
[25] Gonshor A, Jones GM. Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol. 1976;256(2):361-79. [DOI:10.1113/jphysiol.1976.sp011329]
[26] Gonshor A, Jones GM. Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol. 1976;256(2):381-414. [DOI:10.1113/jphysiol.1976.sp011330]
[27] Wedtgrube A, Bockisch CJ, Straumann D, Tarnutzer AA. Prolonged Static Whole-Body Roll-Tilt and Optokinetic Stimulation Significantly Bias the Subjective Postural Vertical in Healthy Human Subjects. Front Neurol. 2020;11:595975. [DOI:10.3389/fneur.2020.595975]
[28] Castro P, Hussain S, Mohamed OG, Kaski D, Arshad Q, Bronstein AM, et al. Visuospatial orientation: Differential effects of head and body positions. Neurosci Lett. 2022;775:136548. [DOI:10.1016/j.neulet.2022.136548]
[29] Iranfar S, Jalilvand Karimi L, Shaabani M, Sharifian Alborzi M, Akbarzadeh Baghban A. [Subjective visual vertical test: the effect of preset angle and visual background]. J Rehab Med. 2013;2(2):47-54. Persian.
[30] Ito M, Shiida T, Yagi N, Yamamoto M. The cerebellar modification of rabbit’s horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation. Proc Jpn Acad Ser B Phys Biol Sci. 1974;50(1):85-9. [DOI:10.2183/pjab1945.50.85]
[31] Jones GM, Davies P. Adaptation of cat vestibulo-ocular reflex to 200 days of optically reversed vision. Brain Res. 1976;103(3):551-4. [DOI:10.1016/0006-8993(76)90454-6]
[32] Robinson DA. Adaptive gain control of vestibuloocular reflex by the cerebellum. J Neurophysiol. 1976;39(5):954-69. [DOI:10.1152/jn.1976.39.5.954]
[33] Miles FA, Eighmy BB. Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. J Neurophysiol. 1980;43(5):1406-25. [DOI:10.1152/jn.1980.43.5.1406]
[34] Freedman W, Carroll JR, McElligott JG. Comparison of vestibulo-ocular reflex (VOR) modification methods in cats. Vision Res. 1990;30(10):1525-8. [DOI:10.1016/0042-6989(90)90034-I]
[35] Miles FA, Fuller JH. Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. Brain Res. 1974;80(3):512-6. [DOI:10.1016/0006-8993(74)91035-X]
[36] Demer JL, Goldberg J, Jenkins HA, Porter FI. Vestibulo-ocular reflex during magnified vision: adaptation to reduce visual-vestibular conflict. Aviat Space Environ Med. 1987;58(9 Pt 2):A175-9.
[37] Demer JL, Porter FI, Goldberg J, Jenkins HA, Schmidt K. Adaptation to telescopic spectacles: vestibulo-ocular reflex plasticity. Invest Ophthalmol Vis Sci. 1989;30(1):159-70.
[38] Gauthier GM, Robinson DA. Adaptation of the human vestibuloocular reflex to magnifying lenses. Brain Res. 1975;92(2):331-5. [DOI:10.1016/0006-8993(75)90279-6]
[39] Istl-Lenz Y, Hydén D, Schwarz DW. Response of the human vestibulo-ocular reflex following long-term 2x magnified visual input. Exp Brain Res. 1985;57(3):448-55. [DOI:10.1007/BF00237831]
[40] Collewijn H, Martins AJ, Steinman RM. Compensatory eye movements during active and passive head movements: fast adaptation to changes in visual magnification. J Physiol. 1983;340:259-86. [DOI:10.1113/jphysiol.1983.sp014762]
[41] Michaelides E, Schutt CA. The correlation between the vestibulo-ocular reflex and multi-focal ocular correction: implications for vestibular compensation. Am J Otolaryngol. 2014;35(5):572-6. [DOI:10.1016/j.amjoto.2014.06.003]
[42] Cannon SC, Leigh RJ, Zee DS, Abel LA. The effect of the rotational magnification of corrective spectacles on the quantitative evaluation of the VOR. Acta Otolaryngol. 1985;100(1-2):81-8. [DOI:10.3109/00016488509108591]
[43] Carcaud J, França de Barros F, Idoux E, Eugène D, Reveret L, Moore LE, et al. Long-Lasting Visuo-Vestibular Mismatch in Freely-Behaving Mice Reduces the Vestibulo-Ocular Reflex and Leads to Neural Changes in the Direct Vestibular Pathway. eNeuro. 2017;4(1):ENEURO.0290-16.2017. [DOI:10.1523/ENEURO.0290-16.2017]
[44] Crane BT, Demer JL. Effect of adaptation to telescopic spectacles on the initial human horizontal vestibuloocular reflex. J Neurophysiol. 2000;83(1):38-49. [DOI:10.1152/jn.2000.83.1.38]
[45] Kheradmand A, Zee DS. Cerebellum and ocular motor control. Front Neurol. 2011;2:53. [DOI:10.3389/fneur.2011.00053]
[46] Miles FA, Lisberger SG. Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci. 1981;4:273-99. [DOI:10.1146/annurev.ne.04.030181.001421]
[47] Sehizadeh M. Monocular adaptation of vestibulo-ocular reflex (VOR). [Master’s thesis]. Waterloo, Ontario, Canada: University of Waterloo; 2005.
[48] Viirre E, Cadera W, Vilis T. The pattern of changes produced in the saccadic system and vestibuloocular reflex by visually patching one eye. J Neurophysiol. 1987;57(1):92-103. [DOI:10.1152/jn.1987.57.1.92]
[49] Griffin JR, Grisham JD. Normal binocular vision. Binocular anomalies, Diagnosis and vision therapy. 4th ed. Boston, MA: Butterworth-Heinemann; 2002. p. 3, 6.
| Files | ||
| Issue | Vol 32 No 2 (2023) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/avr.v32i2.12165 | |
| Keywords | ||
| Vestibulo-ocular reflex visual inputs refractive errors head impulse test | ||
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How to Cite
1.
Heravian Shandiz J, Mazloom M, Jafarzadeh S. Effects of Visual Input Changes on Canal and Otolith- Dependent Vestibulo-Ocular Reflexes: A Review Study. Aud Vestib Res. 2023;32(2):90-97.
