Skip to main content
Log in

The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Latencies of normal and adapted feline vestibulo-ocular reflex (VOR) were studied in five cats by applying ± 20°/s horizontal head velocity steps (4000°/s2 acceleration) and measuring the elicited horizontal or vertical reflex eye responses. Normal VOR latency was 13.0 ms ± 1.9 SD. Short-term adaptation was then accomplished by using 2 h of paired horizontal sinusoidal vestibular stimulation and phase-synchronized vertical optokinetic stimulation (cross-axis adaptation). For long-term adaptation, cats wore ×0.25 or ×2.2 magnifying lenses for 4 days. The cats were passively rotated for 2 h/day and allowed to walk freely in the laboratory or their cages for the remainder of the time. The latency of the early (primary) adaptive response was 15.2ms±5.2 SD for crossaxis adaptation and 12.5 ms±3.9 SD for lens adaptation. This short-latency response appeared within 30 min after beginning the adaptation procedure and diminished in magnitude overnight. A late (secondary) adaptive response with latency of 76.8 ms±7.0 SD for cross-axis adaptation and 68.1 ms±8.8 SD for lens adaptation appeared after approximately 2 h of adaptation. It had a more gradual increase in magnitude than the primary response and did not diminish in magnitude overnight. These data suggest that brainstem VOR pathways are a site of learning for adaptive VOR modification, since the primary latency is short and has a similar latency to that of the normal VOR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Baker J, Goldberg J, Peterson B (1985) Spatial and temporal response properties of the vestibulocollic reflex in decerebrate cats. J Neurophysiol 54:735–756

    Google Scholar 

  • Baker R, Weiser M, McElligott J (1988) Adaptive gain control of the vestibulo-ocular reflex in goldfish. I. Hemi-cerebellectomy. Soc Neurosci Abstr 14:72.6

    Google Scholar 

  • Baker R, Pastor E, Weiser M, McElligott J (1989) The latency and gain of the horizontal vestibulo-ocular reflex in goldfishes determined by vestibular and position velocity steps during learning and memory. Soc Neurosci Abstr 15:324.9

    Google Scholar 

  • Blanks R, Curthoys I, Markham C (1972) Planar relationships of semicircular canals in the cat. Am J Physiol 223:55–62

    Google Scholar 

  • Bond H, Ho P (1970) Solid miniature silver-silver chloride electrodes for chronic implantation. Electroencephalogr Clin Neurophysiol 29:206–208

    Google Scholar 

  • Cohen B, Suzuki J, Bender M (1964) Eye movements from semicircular nerve stimulation in the cat. Ann Otol Rhinol Laryngol 75:153–165

    Google Scholar 

  • Collewijn H, Martins A, Steinman R (1983) Compensatory eye movements during active and passive head movements: fast adaptation to changes in visual magnification. J Physiol (Lond) 340:259–286

    Google Scholar 

  • Demer J, Robinson D (1982) Effects of reversible lesions and stimulation of olivocerebellar system on vestibuloocular reflex plasticity. J Neurophysiol 47:1084–1107

    Google Scholar 

  • Dufosse M, Ito M, Miyashita Y (1978) Diminution and reversal of eye movements induced by local stimulation of rabbit cerebellar flocculus after partial destruction of the inferior olive. Exp Brain Res 33:139–141

    Google Scholar 

  • Fetter M, Zee DS, Proctor LR (1988) Effect of lack of vision and of occipital lobectomy upon recovery from unilateral labyrinthectomy in rhesus monkey. J Neurophysiol 59:394–407

    Google Scholar 

  • Fuchs A, Kimm J (1975) Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38:1140–1161

    Google Scholar 

  • Ghelarducci B, Ito M, Yagi N (1975) Impulse discharges from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation. Brain Res 87:66–72

    Google Scholar 

  • Gonshor A, Melvill-Jones G (1976a) Extreme vestibulooccular adaptation induced by prolonged optical reversal of vision. J Physiol (Lond) 256:381–414

    Google Scholar 

  • Gonshor A, Melvill-Jones G (1976b) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J Physiol (Lond) 256:361–379

    Google Scholar 

  • Haddad G, Friendlich A, Robinson D (1980) The effect of lesions of the dorsal cap of the inferior olive and the vestibulo-ocular and optokinetic systems of the cat. Brain Res 185:265–275

    Google Scholar 

  • Harrison R, Baker J, Isu N, Wickland C, Peterson B (1986) Dynamics of adaptive change in vestibulo-ocular reflex direction. I. Rotations in the horizontal plane. Brain Res 371:162–165

    Google Scholar 

  • Houk J, Singh S, Fisher C, Barto A (1991) An adaptive sensorimotor network inspired by the anatomy and physiology of the cerebellum. In: Miller W, Sutton R, Werbos P (eds) Neural networks for control. MIT, Cambridge Mass

    Google Scholar 

  • Ito M (1982) Cerebellar control of the vestibulo-ocular reflex around the flocculus hypothesis. Annu Rev Neurosci 5:275–296

    Google Scholar 

  • Ito M (1984) The cerebellum and neural control. Raven, New York

    Google Scholar 

  • Ito M, Miyashita (1975) The effects of chronic destruction of inferior olive upon visual modification of the horizontal vestibuloocular reflex of rabbits. Proc Jpn Acad 51:716–760

    Article  Google Scholar 

  • Ito M, Shiida T, Yagi N, Yamamoto M (1974a) Visual influence on rabbit horizontal vestibulo-ocular reflex presumably effected via the cerebellar flocculus. Brain Res 65:170–174

    Google Scholar 

  • Ito M, Shiida T, Yagi N, Yamamoto M (1974b) 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

    Google Scholar 

  • Judge S, Richmond B, Chu F (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535–538

    Google Scholar 

  • Khater T, Peterson B, Baker J (1990) Dynamics of adaptive change in human vestibulo-ocular reflex direction. J Vestib Res 1:23–39

    Google Scholar 

  • Lisberger S (1984) The latency of pathways containing the site of motor learning in the monkey vestibulo-ocular reflex. Science 225:74–76

    Google Scholar 

  • Lisberger S (1988a) The neural basis for motor learning in the vestibulo-ocular reflex in monkeys. Trends Neurosci 11:147–152

    Google Scholar 

  • Lisberger S (1988b) The neural basis for learning of simple motor skills. Science 242:728–735

    Google Scholar 

  • Lisberger S, Pavelko T (1988) Brain stem neurons in modified pathways for motor learning in the primate vestibulo-ocular reflex. Science 242:771–773

    Google Scholar 

  • Lisberger S, Miles F, Optican L, Eighmy B (1981) Optokinetic response in monkey: underlying mechanisms and their sensitivity to long-term adaptive changes in VOR. J Neurophysiol 45:869–890

    Google Scholar 

  • Lisberger S, Miles F, Zee D (1984) Signals used to compute errors in monkey vestibulo-ocular reflex: possible role of flocculus. J Neurophysiol 52:1140–1153

    Google Scholar 

  • Michnovicz J, Bennett M (1987) Effects of rapid cerebellectomy on adaptive gain control of the vestibulo-ocular reflex in alert goldfish. Exp Brain Res 66:287–294

    Google Scholar 

  • Miles F, Braitman D (1980) Long-term adaptive changes in primate VOR. II. Electrophysiological observations on semicircular canal primary afferents. J Neurophysiol 43:1426–1436

    Google Scholar 

  • Miles F, Eighmy B (1980) Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. J Neurophysiol 43:1406–1425

    Google Scholar 

  • Miles F, Fuller J (1974) Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. Brain Res 80:512–516

    Google Scholar 

  • Miles F, Lisberger S (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273–299

    Google Scholar 

  • Miles F, Braitman D, Dow B (1980a) Long-term adaptive changes in primate VOR. IV. Electrophysiological observations in flocculus of adapted monkeys. J Neurophysiol 43:1477–1493

    Google Scholar 

  • Miles F, Fuller J, Braitman J, Dow B (1980b) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437–1476

    Google Scholar 

  • Peterson B, Baker J, Houk J (1991) A model of adaptive control of vestibuloocular reflex based on properties of cross-axis adaptation. Ann NY Acad Sci 627:319–337

    Google Scholar 

  • Robinson D (1964) The mechanics of human saccadic eye movement. J Physiol (Lond) 175:245–264

    Google Scholar 

  • Robinson D (1965) The mechanics of human smooth pursuit eye movement. J Physiol (Lond) 180:569–591

    Google Scholar 

  • Robinson D (1976) Adaptive gain control of the vestibuloocular reflex by the cerebellum. J Neurophysiol 39:954–969

    Google Scholar 

  • Sato Y, Kawasaki T (1987) Target neurons of floccular caudal zone inhibition in y-group nucleus of vestibular nuclear complex. J Neurophysiol 57:460–480

    Google Scholar 

  • Sato Y, Kawasaki T (1990) Operational unit responsible for planespecific control of eye movement by cerebellar flocculus in cat J Neurophysiol 64:551–564

    Google Scholar 

  • Schairer J, Bennet M (1981) Cerebellectomy in goldfish prevents adaptive gain control of the VOR without affecting the optokinetic system. In: Gualtierotti T (ed) Vestibular function and morphology. Springer, Berlin Heidelberg New York, pp 463–477

    Google Scholar 

  • Schultheis L, Robinson D (1981) Directional plasticity of the vestibulo-ocular reflex in the cat. Ann NY Acad Sci 374:504–512

    Google Scholar 

  • Snyder L, King W (1988) Vertical vestibuloocular reflex in cat: asymmetry and adaptation. J Neurophysiol 59:279–298

    Google Scholar 

  • Snyder L, King W (1989) Modulation of gaze velocity purkinje (GVP) cells during vestibulo-ocular reflex (VOR) with near and far visual targets. Soc Neurosci Abstr 324.8

  • Snyder L, King W (1991) The response of gaze velocity purkinje (GVP) cells to sustained velocity (1-2s) does not predict their response immediately after a rapid head acceleration. Soc Neurosci Abstr 337.9

  • Watanabe E (1984) Neuronal events correlated with long term adaptation of the horizontal vestibulo-ocular reflex in the primate flocculus. Brain Res 297:169–174

    Google Scholar 

  • Weiser M, Pastor A, Baker R (1989) Monocular adaptive gain control of the vestibulo-ocular reflex in the goldfish. Soc Neurosci Abstr 324.10

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khater, T.T., Quinn, K.J., Pena, J. et al. The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation. Exp Brain Res 94, 16–32 (1993). https://doi.org/10.1007/BF00230467

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00230467

Key words

Navigation