Neurovestibular Compensation following Ototoxic Lesion and Labyrinthectomy

Abstract

Introduction Unilateral labyrinthectomy and intra-tympanic gentamycin have been employed in the treatment of Ménière's disease, but the efficacy of these techniques has not been well established.

Objective The objective of this study is to measure the time course of recovery from a unilateral labyrinthectomy either after ipsilateral topical treatment with gentamicin to the inner ear or without the previous insult.

Methods Twenty-nine adult Mongolian gerbils were randomized into two experimental groups. Group 1 (n = 17) received a right ear gentamicin drug-induced lesion by unilateral labyrinthectomy (UL). Group 2 (n = 12) only received a right unilateral labyrinthectomy lesion. We measured the horizontal vestibulo-ocular responses in gerbils before and after the lesion. The gerbils received an angular acceleration stimulus and their eye movements were recorded.

Results The gentamicin lesion resulted in a quicker recovery. Experimental groups underwent a similar time course of recovery. Statistical analysis showed no significant difference between the two groups. Both groups displayed adaptation to the lesion by day 21, but long-term compensation did not completely revert to the original pre-lesion state.

Conclusions In a lesion requiring both static and dynamic compensation as in UL, the need for a static compensation may alter pre-existing compensation from a previous dynamic insult and require a new compensation. A previous lesion and adaptation is not preserved for a second lesion and the subject has to re-compensate. Therefore, surgical treatment in Meniere's disease such as UL can be considered without prior gentamicin treatment. Static and dynamic compensations do not appear to be as independent as previous studies have suggested.

Keywords

vestibuloocular reflex - gerbils - vestibular - compensation

• References

• 1 Sajjadi H, Paparella MM. Meniere's disease. Lancet 2008; 372 (9636) 406-414 10.1016/s0140-6736(08)61161-7
• 2 Tassinari M, Mandrioli D, Gaggioli N, Roberti di Sarsina P. Ménière's disease treatment: a patient-centered systematic review. Audiol Neurootol 2015; 20 (3) 153-165 10.1159/000375393
• 3 Sharon JD, Trevino C, Schubert MC, Carey JP. Treatment of Menière's Disease. Curr Treat Options Neurol 2015; 17 (4) 341 10.1007/s11940-015-0341-x
• 4 Pullens B, Verschuur HP, van Benthem PP. Surgery for Ménière's disease. Cochrane Database Syst Rev 2013; 2: CD005395 10.1002/14651858.CD005395.pub3
• 5 Ghossaini SN, Wazen JJ. An update on the surgical treatment of Ménière's diseases. J Am Acad Audiol 2006; 17 (1) 38-44
• 6 De Beer L, Stokroos R, Kingma H. Intratympanic gentamicin therapy for intractable Ménière's disease. Acta Otolaryngol 2007; 127 (6) 605-612 10.1080/00016480600951475
• 7 Lyford-Pike S, Vogelheim C, Chu E, Della Santina CC, Carey JP. Gentamicin is primarily localized in vestibular type I hair cells after intratympanic administration. J Assoc Res Otolaryngol 2007; 8 (4) 497-508 10.1007/s10162-007-0093-8
• 8 Harner SGDC, Driscoll CL, Facer GW, Beatty CW, McDonald TJ. Long-term follow-up of transtympanic gentamicin for Ménière's syndrome. Otol Neurotol 2001; 22 (2) 210-214
• 9 Lange G, Maurer J, Mann W. Long-term results after interval therapy with intratympanic gentamicin for Menière's disease. Laryngoscope 2004; 114 (1) 102-105 10.1097/00005537-200401000-00018
• 10 Perez N, Martín E, García-Tapia R. Intratympanic gentamicin for intractable Meniere's disease. Laryngoscope 2003; 113 (3) 456-464 10.1097/00005537-200303000-00013
• 11 Hirvonen TPML, Minor LB, Hullar TE, Carey JP. Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla. J Neurophysiol 2005; 93 (2) 643-655
• 12 Newlands SDDS, Dara S, Kaufman GD. Relationship of static and dynamic mechanisms in vestibuloocular reflex compensation. Laryngoscope 2005; 115 (2) 191-204
• 13 Shinder ME, Perachio AA, Kaufman GD. VOR and Fos response during acute vestibular compensation in the Mongolian gerbil in darkness and in light. Brain Res 2005; 1038 (2) 183-197 10.1016/j.brainres.2005.01.043
• 14 Shinder ME, Perachio AA, Kaufman GD. Fos responses to short-term adaptation of the horizontal vestibuloocular reflex before and after vestibular compensation in the Mongolian gerbil. Brain Res 2005; 1050 (1–2) 79-93 10.1016/j.brainres.2005.05.029
• 15 Mantokoudis G, Schubert MC, Tehrani AS, Wong AL, Agrawal Y. Early adaptation and compensation of clinical vestibular responses after unilateral vestibular deafferentation surgery. Otol Neurotol 2014; 35 (1) 148-154 10.1097/MAO.0b013e3182956196
• 16 Kaufman GD. Video-oculography in the gerbil. Brain Res 2002; 958 (2) 472-487
• 17 Watanabe S, Hattori K, Koizuka I. Flexibility of vestibulo-ocular reflex adaptation to modified visual input in human. Auris Nasus Larynx 2003; 30 (Suppl): S29-S34
• 18 van Sonsbeek S, Pullens B, van Benthem PP. Positive pressure therapy for Ménière's disease or syndrome. Cochrane Database Syst Rev 2015; 3: CD008419 10.1002/14651858.CD008419.pub2
• 19 Dara S. . Neurovestibular compensation in gerbils following unilateral three canal plug and unilateral labyrinthectomy. International Space University 2003
• 20 Ushio M, Minor LB, Della Santina CC, Lasker DM. Unidirectional rotations produce asymmetric changes in horizontal VOR gain before and after unilateral labyrinthectomy in macaques. Exp Brain Res 2011; 210 (3–4) 651-660 10.1007/s00221-011-2622-2
• 21 Beraneck M, McKee JL, Aleisa M, Cullen KE. Asymmetric recovery in cerebellar-deficient mice following unilateral labyrinthectomy. J Neurophysiol 2008; 100 (2) 945-958 10.1152/jn.90319.2008
• 22 Sadeghi SG, Minor LB, Cullen KE. Dynamics of the horizontal vestibuloocular reflex after unilateral labyrinthectomy: response to high frequency, high acceleration, and high velocity rotations. Exp Brain Res 2006; 175 (3) 471-484 10.1007/s00221-006-0567-7
• 23 Lewis RF, Haburcakova C, Gong W, Makary C, Merfeld DM. Vestibuloocular reflex adaptation investigated with chronic motion-modulated electrical stimulation of semicircular canal afferents. J Neurophysiol 2010; 103 (2) 1066-1079 10.1152/jn.00241.2009
• 24 Lasker DM, Hullar TE, Minor LB. Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. III. Responses after labyrinthectomy. J Neurophysiol 2000; 83 (5) 2482-2496
• 25 Mao Y, Chen P, Li L, Huang D. Virtual reality training improves balance function. Neural Regen Res 2014; 9 (17) 1628-1634
• 26 Dieringer N. Activity-related postlesional vestibular reorganization. Ann N Y Acad Sci 2003; 1004: 50-60
• 27 Koizuka I. Adaptive plasticity in the otolith-ocular reflex. Auris Nasus Larynx 2003; 30 (Suppl): S3-S6
• 28 Harrod CG, Baker JF. The vestibulo ocular reflex (VOR) in otoconia deficient head tilt (het) mutant mice versus wild type C57BL/6 mice. Brain Res 2003; 972 (1–2) 75-83
• 29 Wu IC, Minor LB. Long-term hearing outcome in patients receiving intratympanic gentamicin for Ménière's disease. Laryngoscope 2003; 113 (5) 815-820 10.1097/00005537-200305000-00009
• 30 Shimizu N, Wood S, Kushiro K, Yanai S, Perachio A, Makishima T. Dynamic characteristics of otolith ocular response during counter rotation about dual yaw axes in mice. Neuroscience 2015; 285: 204-214 10.1016/j.neuroscience.2014.11.022
• 31 Yoder RM, Taube JS. The vestibular contribution to the head direction signal and navigation. Front Integr Nuerosci 2014; 8: 32 10.3389/fnint.2014.00032