Summary
The dynamics of the horizontal vestibuloocular reflex (VOR) were determined in the dark prior to and at various time periods after unilateral removal of the vestibular nerve. One chronic group, consisting of cats that were operated at the age of 6 weeks or as adults, was studied 10.5 to 22 months later; an adult-operated group was measured 1–244 days postoperatively (p.o.). Between measurements cats were kept in a normal environment.
In control animals the VOR gain was close to unity only up to certain stimulus velocities which varied amongst cats; thereafter a sharp drop in gain occurred probably due to saturation of central and peripheral neuronal responses. Therefore, VOR gains in lesioned animals were compared to the control responses yielding high gain. It is only at these small stimulus amplitudes that the two labyrinths maximally interact and, therefore, one would expect the largest changes. The gain was computed after correction for the ocular imbalance induced by the lesion. Immediately after the lesion a drop in gain to stimulations in both directions was noted; the reduction was larger for the VOR evoked on rotation to the lesioned side. Contrary to control animals, no partial response saturation occurred in lesioned animals but, following rotation to the lesioned side, complete saturation was noted with larger stimuli. Ocular balance was greatly improved within the first 3–4 days p.o. as indicated by the strong reduction of nystagmus.
The time course of p.o. adaptive gain changes could be divided into three stages: in the initial stage (1–5 days p.o.) no improvement was visible; between p.o. days 5–10 one group of cats showed an abrupt increase in gain while it remained low in others. Response symmetry showed no consistent change in either group; the 3rd stage starting p.o. day 10 and extending throughout the observation period (22 months) is characterized by slowly developing changes reducing significantly response asymmetry. The incremental gain was higher in the young than in the adult-operated chronic cats.
Compared to controls the phase plot of the VOR of lesioned animals shows a parallel shift of ca. 10 ° towards larger lead over the frequency range tested (0.05–1.0 Hz) independent of direction of rotation or p.o. stages.
All lesioned animals showed a clear failure to hold eye position in the dark even in the chronic stage; a drift with an exponentially decreasing velocity of ca. 2–4 °/s was typical. The direction of the drift could be to the lesioned as well as to the intact side. The eyes seem to approach a new null point which is shifted towards the lesioned side.
In conclusion on data show that while ocular balance recovers quite well and fast after unilateral lesions the VOR dynamics show some adaptive plasticity but also significant long-term deficits when measured in the dark and with the head fixed. Obviously, the striking recovery observed in the freely moving animal must be aided by other sensory systems.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Abend WK (1977) Functional organization of the superior vestibular nucleus of the squirrel monkey. Brain Res 132: 65–84
Abend WK (1978) Response to constant angular accelerations of neurons in the monkey superior vestibular nucleus. Exp Brain Res 31: 459–473
Baarsma EA, Collewijn H (1975) Changes in compensatory eye movements after unilateral labyrinthectomy in the rabbit. Arch Otorhinolaryngol 211: 219–230
Barmack NH, Pettorossi VE (1981) The influence of unilateral horizontal canal plugs on the horizontal vestibuloocular reflex of the rabbit. In: Flohr H, Precht W (eds) Lesion-induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg New York, pp 231–239
Barmack NH, Simpson JI (1980) Effects of microlesions of dorsal cap of inferior olive of rabbits on optokinetic and vestibuloocular reflexes. J Neurophysiol 43: 182–206
Baker R, Highstein S (1978) Vestibular projections to medial rectus subdivision of oculomotor nucleus. J Neurophysiol 41: 1629–1646
Bechterew W von (1883) Ergebnisse der Durchschneidung des N. acusticus, nebst Erörterung der Bedeutung der semicirculären Kanäle für das Körpergleichgewicht. Pflügers Arch 30: 312–347
Berthoz A, Jeannerod M, Vital-Durand F, Oliveras JL (1975) Development of vestibuloocular responses in visually deprived kittens. Exp Brain Res 23: 425–442
Blanks RHI, Estes MS, Markham CH (1975) Physiological characteristics of vestibular first order canal neurons in the cat. II. Responses to constant angular acceleration. J Neurophysiol 38: 1250–1268
Bond HW, Ho P (1970) Solid miniature silver-silver chloride electrodes for chronic implantations. Electroencephalogr Clin Neurophysiol 28: 206–208
Carpenter RHS (1972) Cerebellectomy and transfer function of the vestibuloocular reflex in the decerebrate cat. Proc R Soc Lond [Biol] 181: 353–374
Carpenter MB, Fabrega H, Glinsmann W (1959) Physiological deficits occurring with lesions of labyrinth and fastigial nuclei. J Neurophysiol 22: 222–234
Courjon JH, Flandrin JM, Jeannerod M, Schmid R (1982) The role of the flocculus in vestibular compensation after hemilabyrinthectomy. Brain Res 239: 251–257
Courjon JH, Jeannerod M, Ossuzio I, Schmid R (1977) The role of vision in compensation after hemilabyrinthectomy in the cat. Exp Brain Res 28: 235–248
Dichgans J, Bizzi E, Morasso P, Tagliasco V (1973) Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys. Exp Brain Res 18: 548–562
Donaghy M (1980) The cat's vestibulo-ocular reflex. J Physiol (Lond) 300: 337–351
Flandrin JM, Jeannerod M (1981) Effects of unilateral superior colliculus ablation on oculomotor and vestibulo-ocular responses in the cat. Exp Brain Res 42: 73–80
Flohr H, Bienhold H, Abeln W, Macskovics I (1981) Concepts of vestibular compensation. In: Flohr H, Precht W (eds) Lesion-induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg New York, pp 153–172
Fluur E (1960) Vestibular compensation after labyrinthine destruction. Acta Otolaryngol (Stockh) 52: 367–375
Gauthier GM, Robinson DA (1975) Adaptation of the human vestibulo-ocular reflex to magnifying lenses. Brain Res 92: 331–335
Gernandt BE, Thulin CA (1952) Vestibular connections of the brain stem. Am J Physiol 171: 121–127
Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semi-circular canals of the squirrel monkey. I. Resting discharge and response to constant angular acceleration. J Neurophysiol 34: 635–660
Groen JJ, Lowenstein O, Vendrik AJH (1952) The mechanical analysis of the responses from the end-organs of the horizontal semicircular canal in the isolated elasmobranch labyrinth. J Physiol (Lond) 117: 329–346
Haddad GM, Friendlich AR, Robinson DA (1977) Compensation of nystagmus after VIIth nerve lesions in vestibulo-cerebellectomized cats. Brain Res 135: 192–196
Harris LR, Cynader M (1981) Modification of the balance and gain of the vestibulo-ocular reflex in the cat. Exp Brain Res 44: 57–70
Horn E (1981) An ontogenetic approach to vestibular compensation mechanisms. In: Flohr H, Precht W (eds) Lesion-induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg New York, pp 173–183
Ito M, Shiida T, Yagi N, Yamamoto M (1974) The cerebellar modification of rabbit's horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation. Proc Jpn Acad 50: 85–89
Jeannerod M, Courjon JH, Flandrin JM, Schmid R (1981) Supravestibular control of vestibular compensation after hemilabyrinthectomy in the cat. In: Flohr H, Precht W (eds) Lesion-induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg New York, pp 208–220
Jensen DW (1979) Reflex control of acute postural asymmetry and compensatory symmetry after a unilateral vestibular lesion. Neuroscience 4: 1059–1073
Kasahara M, Uchino Y (1974) Bilateral semicircular canal inputs to neurons in cat vestibular nuclei. Exp Brain Res 20: 285–296
Keller EL, Precht W (1979) Adaptive modification of central vestibular neurons in response to visual stimulation through reversing prisms. J Neurophysiol 42: 896–911
Landers PH, Taylor A (1975) Transfer function analysis of the vestibulo-ocular reflex in the conscious cat. In: Lennerstrand G, Bach-y-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon Press, Oxford, pp 505–508
Llinás R, Walton K, Hillman DE, Sotelo C (1975) Inferior olive: Its role in motor learning. Science 190: 1230–1231
Maioli C, Precht W, Ried S (1982) Vestibulo-ocular and optokinetic reflex compensation following hemilabyrinthectomy in the cat. In: Roucoux A, Crommelinck M (eds) Physiological and pathological aspects of eye movements. W Junk Publ., The Hague, pp 201–208
Mano N, Oshima T, Shimazu H (1968) Inhibitory commissural fibers interconnecting the bilateral vestibular nuclei. Brain Res 8: 378–382
Markham CH (1968) Midbrain and contralateral labyrinth influences on brain stem vestibular neurons in the cat. Brain Res 9: 312–333
Markham CH, Yagi T, Curthoys IS (1977) The contribution of the contralateral labyrinth to the second order vestibular neuronal activity in the cat. Brain Res 138: 99–109
Melvill Jones G (1977) Plasticity in the adult vestibulo-ocular reflex arc. Philos Trans R Soc Lond [Biol] 278: 319–334
Melvill Jones G, Davies P (1976) Adaptation of cat vestibulo-ocular reflex to 200 days of optically reversed vision. Brain Res 103: 551–554
Melvill Jones G, Milsum JH (1970) Characteristics of neural transmission from the semicircular canal to the vestibular nuclei of cats. J Physiol (Lond) 209: 295–316
Miles FA, Eighmy BB (1980) Long-term adaptive changes in primate vestibulo-ocular reflex. I. Behavioral observations. J Neurophysiol 43: 1406–1425
Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: A new hypothesis. Ann Rev Neurosci 4: 273–299
Mittermaier R (1950) Über die Ausgleichsvorgänge im Vestibularapparat. Z Laryng Rhinol 29: 487–585
Money KE, Scott JW (1962) Functions of separate sensory receptors of nonauditory labyrinth of the cat. Am J Physiol 202: 1211–1220
Moran WB (1974) The changes in phase lag during sinusoidal angular rotation following labyrinthectomy in the cat. Laryngoscope 84: 1707–1728
O-Uchi T, Igarashi M, Kubo T (1981) Effect of frontal-eye-field lesion on eye-head coordination in squirrel monkeys. In: Cohen B (ed) Vestibular and oculomotor physiology. New York Academy of Sciences, New York, pp 656–673
Petrosini L, Troiani D (1979) Vestibular compensation after hemilabyrinthectomy: Effects of trigeminal neurotomy. Physiol Behav 22: 133–137
Precht W (1974) Characteristics of vestibular neurons after acute and chronic labyrinthine destruction. In: Kornhuber HH (ed) Handbook of sensory physiology, vol VI/2. Springer, Berlin Heidelberg New York, pp 451–462
Precht W (1979) Vestibular mechanisms. Annu Rev Neurosci 2: 265–289
Precht W, Maioli C, Dieringer N, Cochran S (1981) Mechanisms of compensation of the vestibulo-ocular reflex after vestibular neurotomy. In: Flohr H, Precht W (eds) Lesion-induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg New York, pp 221–230
Precht W, Shimazu H, Markham CH (1966) A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J Neurophysiol 29: 996–1010
Robinson DA (1974) The effect of cerebellectomy on the cat's vestibulo-ocular integrator. Brain Res 71: 195–207
Robinson DA (1976) Adaptive gain control of vestibulo-ocular reflex by the cerebellum. J Neurophysiol 39: 954–969
Robles SS, Anderson JH (1978) Compensation of vestibular deficits in the cat. Brain Res 147: 183–187
Ruttin E (1926) Funktionsprüfung des Vestibularapparates. In: Denker A, Kahler O (Hrsg) Handbuch der Hals-, Nasen- und Ohrenheilkunde. Springer, Berlin Heidelberg New York, S 995
Schaefer KP, Meyer DL (1973) Compensatory mechanisms following labyrinthine lesions in the guinea pig. A simple model of learning. In: Zippel HP (ed) Memory and transfer of information. Plenum Press, New York London, pp 203–232
Schaefer KP, Meyer DL (1974) Compensation of vestibular lesions. In: Kornhuber HH (ed) Handbook of sensory physiology, vol VI/2. Springer, Berlin Heidelberg New York, pp 463–490
Shimazu H, Precht W (1965) Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. J Neurophysiol 28: 991–1013
Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29: 467–492
Shinoda Y, Yoshida K (1974) Dynamic characteristics of responses to horizontal head angular acceleration in vestibulo-ocular pathway in the cat. J Neurophysiol 37: 653–673
Skavenski AA, Robinson DA (1973) Role of abducens neurons in vestibulo-ocular reflex. J Neurophysiol 36: 724–738
Trincker D (1965) Physiologie des Gleichgewichtsorgans. In: Berendes J, Link R, Zöllner F (Hrsg) Hals-Nasen-Ohren-Heilkunde, vol III, part 1. Thieme, Stuttgart
Wolfe JW, Kos CM (1977) Nystagmic responses of the rhesus monkey to rotational stimulation following unilateral labyrinthectomy: Final report. Trans Am Acad Ophthalmol Otolaryngol 84: 38–45
Wolfe JW, Engelken EJ, Kos CN (1978) Low-frequency harmonic acceleration as a test of labyrinthine function: Basic methods and illustrative cases. Trans Am Acad Ophthalmol Otolaryngol 86: 130–142
Zuckerman H (1967) The physiological adaptation to unilateral semicircular canal inactivation. McGill Med J 36: 8–13
Author information
Authors and Affiliations
Additional information
Supported by grants nos. 3.505.79 and 3.616.80 from the Swiss National Science Foundation and the Dr. Eric Slack-Gyr Foundation
Rights and permissions
About this article
Cite this article
Maioli, C., Precht, W. & Ried, S. Short- and long-term modifications of vestibulo-ocular response dynamics following unilateral vestibular nerve lesions in the cat. Exp Brain Res 50, 259–274 (1983). https://doi.org/10.1007/BF00239190
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00239190