Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T21:28:05.177Z Has data issue: false hasContentIssue false

Visual and vestibular reflexes that stabilize gaze in the chameleon

Published online by Cambridge University Press:  02 June 2009

Henri Gioanni
Affiliation:
Laboratoire de Neurochimie-Anatomie, Université Pierre et Marie Curie
Mohamed Bennis
Affiliation:
Laboratoire de Cytologie, 7–9 Quai St Bernard 75005 Paris, France Laboratoire de Neurosciences, Université Cadi Ayyad, Marrakech, Morocco
Annie Sansonetti
Affiliation:
Laboratoire de Neurochimie-Anatomie, Université Pierre et Marie Curie

Abstract

Spontaneous eye movements as well as visual, vestibular, and proprioceptive cervical reflexes which contribute to gaze stabilization were investigated in the chameleon using the magnetic search-coil technique. The oculomotor range of each eye was very large (180 deg horizontally × 80 deg vertically). Spontaneous ocular saccades were independent in the two eyes and could have very large amplitudes. The fast phases of nystagmus during the stabilization reflexes were also independent in the eyes. In the head-restrained condition, optokinetic nystagmus (OKN) had a low gain in both horizontal and vertical planes (0.35 at 5 deg/s) and showed little binocular interaction. The vestibulo-ocular reflex (VOR) exhibited a low gain (0.2–0.3 from 0.05–1 Hz) and a high-phase lead at low frequency (140 deg at 0.05 Hz). Rotation of the animal in the presence of a visible surround increased the overall gain of gaze stabilization to 0.4–0.5 (P < 0.01) and considerably reduced the phase lead (38 deg at 0.05 Hz). In the head-free condition, head and eye reflexes were active simultaneously during both optokinetic and vestibular stimulation, but nystagmic head movements appeared only occasionally with a rather loose eye-head coordination. During optokinetic stimulation, eye movements contributed more than head movements to gaze stabilization, whereas, during vestibular or visuo-vestibular stimulation, the relative contribution of eye and head responses varied with stimulus frequency. When the head was freed, overall gain for gaze stabilization increased from 0.35 to 0.45 (P < 0.05) for optokinetic stimulation at 5 deg/s and from 0.2–0.3 to 0.4–0.75 (P < 0.001) for vestibular stimulation at 0.05–1 Hz. Optimal gaze stabilization (gain of 0.8) was only obtained with combined visual and vestibular stimulation in the free-head condition. Cervical stimulation provoked a compensatory cervico-ocular reflex (COR) with a gain of 0.2–0.4 as well as ocular saccades, which were especially numerous in the presence of a visual surround. The direction of these saccades alternated between compensatory and anti-compensatory.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Armengol, J.A., Prada, F., Ambrosiani, J. & Genis-Galvez, J.M. (1988). The photoreceptors of the chameleon retina (Chamaleo chamaleo). A Golgi study. Journal für Hirnforschung 29, 403–409.Google ScholarPubMed
Baker, J., Goldberg, J., Peterson, B. & Schor, R. (1982). Oculomotor reflexes after semicircular canal plugging in cats. Brain Research 252, 151–155.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Freedman, W. (1980). Cervico-ocular reflex in the normal adult. Acta Ololaryngologica (Stockholm) 89, 487–496.CrossRefGoogle ScholarPubMed
Barmack, N.H., Nastos, M.A. & Pettorossi, V.E. (1981). The horizontal and vertical cervico-ocular reflexes of the rabbit. Brain Research 224, 261–278.CrossRefGoogle ScholarPubMed
Barnes, G.R. & Forbat, L.N. (1979). Cervical and vestibular afferent control of oculomotor response in man. Acta Ololaryngologica (Stockholm) A88, 79–87.CrossRefGoogle ScholarPubMed
Bennis, M. (1991). Etude neurocytochimique des médiateurs dans le cerveau d'un reptile, le caméléon; voies visuelles et oculomotricité. Thesis, Faculté des Sciences, Lab. Neurosciences, University of Cadi Ayyad, Marrakech, Morocco.Google Scholar
Bennis, M., Sansonetti, A. & Gioanni, H. (1990). Stabilisation du regard chez le caméléon: Reflexes visuels et vestibulaires. Comptes Rendus Hebdomadaires des Séances de I' Académie des Sciences, Série D, Sciences Naturelles 311, 369–375.Google Scholar
Berthoz, A. (1989). Cooperation and substitution between the saccadic system and vestibular origin reflexes: Should we revise the notion of reflex? Revue Neurologique 145, 513–526.Google ScholarPubMed
Bloch, S., Rivaud, S. & Martinoya, C. (1984). Comparing frontal and lateral viewing in the pigeon. III. Different patterns of eye movements for binocular and monocular fixation. Behavioural Brain Research 13, 173–182.CrossRefGoogle ScholarPubMed
Brandt, Th., Dichgans, J. & Buchele, W. (1974). Motion habituation: Inverted self-motion perception and optokinetic after-nystagmus. Experimental Brain Research 21, 337–352.CrossRefGoogle ScholarPubMed
Bronstein, A.M. & Hood, J.D. (1986). The cervico-ocular reflex in normal subjects and patients with absent vestibular function. Brain Research 373, 399–408.CrossRefGoogle ScholarPubMed
Büttner, U., WAESPE, W. & Henn, V. (1976). Duration and direction of optokinetic after-nystagmus as a function of stimulus exposure time in the monkey. Archiv fur Psychiatrie und Nervenkrankeiten 222, 281–291.CrossRefGoogle ScholarPubMed
Cohen, B., Matsuo, V. & Raphan, T. (1977). Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. Journal of Physiology 270, 321–344.CrossRefGoogle ScholarPubMed
Collewijn, H. (1969). Optokinetic eye movements in the rabbit, input-output relations. Vision Research 9, 117–132.CrossRefGoogle ScholarPubMed
Collewijn, H. (1972). An analog model of the rabbit's optokinetic system. Brain Research 36, 71–88.CrossRefGoogle ScholarPubMed
Collewijn, H. (1977). Eye and head movements in freely moving rabbits. Journal of Physiology 266, 471–498.CrossRefGoogle ScholarPubMed
Collewijn, H. & Noorduin, H. (1972). Vertical and torsional optokinetic eye movements in the rabbit. Pflügers Archives 332, 87–95.CrossRefGoogle ScholarPubMed
Collewijn, H., Winterson, B.J. & Van Der Steen, J. (1980). Post-rotatory nystagmus and optokinetic after nystagmus in the rabbit, linear rather than exponential decay. Experimental Brain Research 40, 330–338.CrossRefGoogle ScholarPubMed
Crommelinck, M., Roucoux, A. & Veraart, C. (1982). The relation of neck muscles activity to horizontal eye position in the alert cat. II. Head free. In Physiological and Pathological Aspects of Eye Movements, ed. Roucoux, A. & Crommelinck, M., pp. 379384. The Hague: W. Junk Publishers.CrossRefGoogle Scholar
Dieringer, N., Cochran, S.L. & Precht, W. (1983). Differences in the central organization of gaze stabilizing reflexes between frog and turtle. Journal of Comparative Physiology 153, 495–508.CrossRefGoogle Scholar
Erickson, R.G. & Barmack, N.H. (1980). A comparison of the horizontal and vertical optokinetic reflexes of the rabbit. Experimental Brain Research 40, 448–456.CrossRefGoogle ScholarPubMed
Fite, K.V. (1968). Two types of optomotor response in the domestic pigeon. Journal of Comparative Psychology 66, 308–314.Google ScholarPubMed
Flanders, M. (1985). Visually guided head movement in the African chameleon. Vision Research 25, 935–942.CrossRefGoogle ScholarPubMed
Flanders, M. (1988). Head movement coordination in the African chameleon. Neuroscience 24, 511–517.CrossRefGoogle ScholarPubMed
Fuller, J.H. (1980). The dynamic neck-eye reflex in mammals. Experimental Brain Research 41, 29–35.CrossRefGoogle ScholarPubMed
Fuller, J.H. (1981). Eye and head movements during vestibular stimulation in the alert rabbit. Brain Research 205, 363–381.CrossRefGoogle ScholarPubMed
Fuller, J.H. (1985). Eye and head movements in the pigmented rat. Vision Research 25, 1121–1128.CrossRefGoogle ScholarPubMed
Fuller, J.H. (1987). Head movements during optokinetic stimulation in the alert rabbit. Experimental Brain Research 65, 593–604.CrossRefGoogle ScholarPubMed
Gioanni, H. (1988 a). Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic eye (OKN) and head (OCR) reflexes. Experimental Brain Research 69, 567–582.CrossRefGoogle ScholarPubMed
GIoanni, H. (1988 b). Stabilizing gaze reflexes in the pigeon (Columba livia). II. Vestibulo-ocular (VOR) and vestibulo-collic (closed-loop VCR) reflexes. Experimental Brain Research 69, 583–593.CrossRefGoogle ScholarPubMed
Grantyn, A. & Berthoz, A. (1987). Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties. Experimental Brain Research 66, 339–354.CrossRefGoogle ScholarPubMed
Gresty, M.A. (1975). Eye, head and body movements of the guinea pig in response to optokinetic stimulation and sinusoidal oscillation in yaw. Pflügers Archives 353, 201–214.CrossRefGoogle ScholarPubMed
Gresty, M.A. (1976). A reexamination of “neck reflex” eye movements in the rabbit. Acta Ololaryngologica (Stockholm) 81, 386–394.CrossRefGoogle ScholarPubMed
Hardy, O. & Mirenowicz, J. (1991). Transient increase of contraversive saccade parameters following kainic acid injection in the parabigeminal area of guinea pig. Experimental Brain Research 85, 616–620.CrossRefGoogle ScholarPubMed
Harkness, L. (1977). Chameleon uses accommodation cues to judge distance. Nature 267, 346–349.CrossRefGoogle Scholar
Harkness, L. & Bennet-Clark, H.C. (1978). The deep fovea as a focus indicator. Nature 272, 814–816.CrossRefGoogle ScholarPubMed
Hertzler, D.R. & Hayes, W.N. (1969). Effects of monocular vision and midbrain transection on movement detection in the turtle. Journal of Comparative Physiology and Psychology 67, 473–478.CrossRefGoogle ScholarPubMed
Hess, B.J.H., Precht, W., Reber, A. & Cazin, L. (1985). Horizontal optokinetic ocular nystagmus in the pigmented rat. Neuroscience 15, 97–107.CrossRefGoogle ScholarPubMed
Jürgens, R. & Meroner, T. (1989). Interaction between cervico-ocu-lar and vestibulo-ocular reflexes in normal adults. Experimental Brain Research 77, 381–390.CrossRefGoogle ScholarPubMed
Kasai, T. & Zee, D.S. (1978). Eye-head coordination in labyrinthine defective human beings. Brain Research 144, 123–141.CrossRefGoogle ScholarPubMed
Kennedy, H., Courjon, J.H. & Flandrin, J.M. (1982). Vestibulo-ocular reflex and optokinetic nystagmus in adult cats reared in strobo-scopic illumination. Experimental Brain Research 48, 279–287.CrossRefGoogle ScholarPubMed
Kirmse, W. (1988). Foveal and ambient visuomotor control in chameleons (Squamata); Experimental results and comparative review. Zoologische Jahrbucher, Abteilung für Allgemeine Zoologie und Physiologie der Tiere 92, 341–350.Google Scholar
Kopp, J. & Manteuffel, G. (1984). Quantitative analysis of salamander horizontal head nystagmus. Brain, Behavior, and Evolution 25, 187–196.CrossRefGoogle ScholarPubMed
Markner, C. & Hoffmann, K.P. (1985). Variability in the effects of monocular deprivation on the optokinetic reflex of the non-deprived eye in the cat. Experimental Brain Research 61, 117–127.CrossRefGoogle ScholarPubMed
Mates, J.W.B. (1978). Eye movements of African chameleon: Spontaneous saccade timing. Science 199, 1087–1089.CrossRefGoogle ScholarPubMed
Mirenowicz, J. & Hardy, O. (1992). Characteristics of saccades induced by neck torsions: Reexamination in the normal guinea pig. Brain Research 592, 1–7.CrossRefGoogle ScholarPubMed
Outerbridge, J.S. & Melvill, Jones G. (1971). Reflex vestibular control of head movement in man. Aerospace Medicine 42, 935–940.Google ScholarPubMed
Peterson, B.W., Goldberg, J., Bilotto, G. & Fuller, J.H. (1985). Cervico-collic reflex: Its dynamic properties and interaction with vestibular reflexes. Journal of Neurophysiology 54, 90–109.CrossRefGoogle Scholar
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions on Bio-medical Electronics 10, 137–145.Google ScholarPubMed
Rochon-Duvigneaud, A. (1943). Les yeux et la vision des vertébrés. Paris: Masson et Cie.Google Scholar
Tauber, E.S. & Atkin, A. (1968). Optomotor responses to monocular stimulation: Relation to visual system organization. Science 160, 1365–1367.CrossRefGoogle ScholarPubMed
Van Die, G.C. & Collewijn, H. (1986). Control of human optokinetic nystagmus by the central and peripheral retina: Effects of partial visual-field masking, scotopic vision, and central retinal scotoma. Brain Research 383, 185–194.CrossRefGoogle Scholar
Vidal, P.P., Roucoux, A. & Berthoz, A. (1982). Horizontal eye position-related activity in neck muscles of the alert cat. Experimental Brain Research 46, 448–453.CrossRefGoogle ScholarPubMed
Wallman, J. & Velez, J. (1985). Directional asymmetries of optokinetic nystagmus: Developmental changes and relation to the accessory optic system and to the vestibular system. Journal of Neuroscience 5, 317–329.CrossRefGoogle Scholar
Wallman, J., Velez, J., Weinstein, B. & Green, A.E. (1982). Avian vestibuloocular reflex: Adaptative plasticity and developmental changes. Journal of Neurophysiology 48, 952–967.CrossRefGoogle ScholarPubMed
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptative Radiation. Bloomfield Hills, Michigan: The Cranbrook Press.Google Scholar