Advertisement

Experimental Brain Research

, Volume 50, Issue 2–3, pp 259–274 | Cite as

Short- and long-term modifications of vestibulo-ocular response dynamics following unilateral vestibular nerve lesions in the cat

  • C. Maioli
  • W. Precht
  • S. Ried
Article

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.

Key words

Vestibuloocular reflex Functional recovery Vestibular nerve lesion Nystagmus 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abend WK (1977) Functional organization of the superior vestibular nucleus of the squirrel monkey. Brain Res 132: 65–84Google Scholar
  2. Abend WK (1978) Response to constant angular accelerations of neurons in the monkey superior vestibular nucleus. Exp Brain Res 31: 459–473Google Scholar
  3. Baarsma EA, Collewijn H (1975) Changes in compensatory eye movements after unilateral labyrinthectomy in the rabbit. Arch Otorhinolaryngol 211: 219–230Google Scholar
  4. 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 231–239Google Scholar
  5. Barmack NH, Simpson JI (1980) Effects of microlesions of dorsal cap of inferior olive of rabbits on optokinetic and vestibuloocular reflexes. J Neurophysiol 43: 182–206Google Scholar
  6. Baker R, Highstein S (1978) Vestibular projections to medial rectus subdivision of oculomotor nucleus. J Neurophysiol 41: 1629–1646Google Scholar
  7. Bechterew W von (1883) Ergebnisse der Durchschneidung des N. acusticus, nebst Erörterung der Bedeutung der semicirculären Kanäle für das Körpergleichgewicht. Pflügers Arch 30: 312–347Google Scholar
  8. Berthoz A, Jeannerod M, Vital-Durand F, Oliveras JL (1975) Development of vestibuloocular responses in visually deprived kittens. Exp Brain Res 23: 425–442Google Scholar
  9. 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: 1250–1268Google Scholar
  10. Bond HW, Ho P (1970) Solid miniature silver-silver chloride electrodes for chronic implantations. Electroencephalogr Clin Neurophysiol 28: 206–208Google Scholar
  11. Carpenter RHS (1972) Cerebellectomy and transfer function of the vestibuloocular reflex in the decerebrate cat. Proc R Soc Lond [Biol] 181: 353–374Google Scholar
  12. Carpenter MB, Fabrega H, Glinsmann W (1959) Physiological deficits occurring with lesions of labyrinth and fastigial nuclei. J Neurophysiol 22: 222–234Google Scholar
  13. Courjon JH, Flandrin JM, Jeannerod M, Schmid R (1982) The role of the flocculus in vestibular compensation after hemilabyrinthectomy. Brain Res 239: 251–257Google Scholar
  14. Courjon JH, Jeannerod M, Ossuzio I, Schmid R (1977) The role of vision in compensation after hemilabyrinthectomy in the cat. Exp Brain Res 28: 235–248Google Scholar
  15. 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: 548–562Google Scholar
  16. Donaghy M (1980) The cat's vestibulo-ocular reflex. J Physiol (Lond) 300: 337–351Google Scholar
  17. Flandrin JM, Jeannerod M (1981) Effects of unilateral superior colliculus ablation on oculomotor and vestibulo-ocular responses in the cat. Exp Brain Res 42: 73–80Google Scholar
  18. 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 153–172Google Scholar
  19. Fluur E (1960) Vestibular compensation after labyrinthine destruction. Acta Otolaryngol (Stockh) 52: 367–375Google Scholar
  20. Gauthier GM, Robinson DA (1975) Adaptation of the human vestibulo-ocular reflex to magnifying lenses. Brain Res 92: 331–335Google Scholar
  21. Gernandt BE, Thulin CA (1952) Vestibular connections of the brain stem. Am J Physiol 171: 121–127Google Scholar
  22. 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: 635–660Google Scholar
  23. 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: 329–346Google Scholar
  24. Haddad GM, Friendlich AR, Robinson DA (1977) Compensation of nystagmus after VIIth nerve lesions in vestibulo-cerebellectomized cats. Brain Res 135: 192–196Google Scholar
  25. Harris LR, Cynader M (1981) Modification of the balance and gain of the vestibulo-ocular reflex in the cat. Exp Brain Res 44: 57–70Google Scholar
  26. 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 173–183Google Scholar
  27. 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: 85–89Google Scholar
  28. 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 208–220Google Scholar
  29. Jensen DW (1979) Reflex control of acute postural asymmetry and compensatory symmetry after a unilateral vestibular lesion. Neuroscience 4: 1059–1073Google Scholar
  30. Kasahara M, Uchino Y (1974) Bilateral semicircular canal inputs to neurons in cat vestibular nuclei. Exp Brain Res 20: 285–296Google Scholar
  31. Keller EL, Precht W (1979) Adaptive modification of central vestibular neurons in response to visual stimulation through reversing prisms. J Neurophysiol 42: 896–911Google Scholar
  32. 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 505–508Google Scholar
  33. Llinás R, Walton K, Hillman DE, Sotelo C (1975) Inferior olive: Its role in motor learning. Science 190: 1230–1231Google Scholar
  34. 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 201–208Google Scholar
  35. Mano N, Oshima T, Shimazu H (1968) Inhibitory commissural fibers interconnecting the bilateral vestibular nuclei. Brain Res 8: 378–382Google Scholar
  36. Markham CH (1968) Midbrain and contralateral labyrinth influences on brain stem vestibular neurons in the cat. Brain Res 9: 312–333Google Scholar
  37. 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: 99–109Google Scholar
  38. Melvill Jones G (1977) Plasticity in the adult vestibulo-ocular reflex arc. Philos Trans R Soc Lond [Biol] 278: 319–334Google Scholar
  39. Melvill Jones G, Davies P (1976) Adaptation of cat vestibulo-ocular reflex to 200 days of optically reversed vision. Brain Res 103: 551–554Google Scholar
  40. Melvill Jones G, Milsum JH (1970) Characteristics of neural transmission from the semicircular canal to the vestibular nuclei of cats. J Physiol (Lond) 209: 295–316Google Scholar
  41. Miles FA, Eighmy BB (1980) Long-term adaptive changes in primate vestibulo-ocular reflex. I. Behavioral observations. J Neurophysiol 43: 1406–1425Google Scholar
  42. Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: A new hypothesis. Ann Rev Neurosci 4: 273–299Google Scholar
  43. Mittermaier R (1950) Über die Ausgleichsvorgänge im Vestibularapparat. Z Laryng Rhinol 29: 487–585Google Scholar
  44. Money KE, Scott JW (1962) Functions of separate sensory receptors of nonauditory labyrinth of the cat. Am J Physiol 202: 1211–1220Google Scholar
  45. Moran WB (1974) The changes in phase lag during sinusoidal angular rotation following labyrinthectomy in the cat. Laryngoscope 84: 1707–1728Google Scholar
  46. 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 656–673Google Scholar
  47. Petrosini L, Troiani D (1979) Vestibular compensation after hemilabyrinthectomy: Effects of trigeminal neurotomy. Physiol Behav 22: 133–137Google Scholar
  48. 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 451–462Google Scholar
  49. Precht W (1979) Vestibular mechanisms. Annu Rev Neurosci 2: 265–289Google Scholar
  50. 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 221–230Google Scholar
  51. Precht W, Shimazu H, Markham CH (1966) A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J Neurophysiol 29: 996–1010Google Scholar
  52. Robinson DA (1974) The effect of cerebellectomy on the cat's vestibulo-ocular integrator. Brain Res 71: 195–207Google Scholar
  53. Robinson DA (1976) Adaptive gain control of vestibulo-ocular reflex by the cerebellum. J Neurophysiol 39: 954–969Google Scholar
  54. Robles SS, Anderson JH (1978) Compensation of vestibular deficits in the cat. Brain Res 147: 183–187Google Scholar
  55. Ruttin E (1926) Funktionsprüfung des Vestibularapparates. In: Denker A, Kahler O (Hrsg) Handbuch der Hals-, Nasen- und Ohrenheilkunde. Springer, Berlin Heidelberg New York, S 995Google Scholar
  56. 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 203–232Google Scholar
  57. 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 463–490Google Scholar
  58. Shimazu H, Precht W (1965) Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. J Neurophysiol 28: 991–1013Google Scholar
  59. Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29: 467–492Google Scholar
  60. Shinoda Y, Yoshida K (1974) Dynamic characteristics of responses to horizontal head angular acceleration in vestibulo-ocular pathway in the cat. J Neurophysiol 37: 653–673Google Scholar
  61. Skavenski AA, Robinson DA (1973) Role of abducens neurons in vestibulo-ocular reflex. J Neurophysiol 36: 724–738Google Scholar
  62. Trincker D (1965) Physiologie des Gleichgewichtsorgans. In: Berendes J, Link R, Zöllner F (Hrsg) Hals-Nasen-Ohren-Heilkunde, vol III, part 1. Thieme, StuttgartGoogle Scholar
  63. 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: 38–45Google Scholar
  64. 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: 130–142Google Scholar
  65. Zuckerman H (1967) The physiological adaptation to unilateral semicircular canal inactivation. McGill Med J 36: 8–13Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • C. Maioli
    • 1
  • W. Precht
    • 1
  • S. Ried
    • 1
  1. 1.Institute for Brain ResearchUniversity of ZürichZürichSwitzerland

Personalised recommendations