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Role of the cervico-ocular reflex in the “flying” pigeon: Interactions with the optokinetic reflex

Published online by Cambridge University Press:  23 June 2004

M. MAURICE  and
H. GIOANNI
M. MAURICE
Affiliation:
Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, UMR 7060, CNRS-Université René Descartes, 45 rue des Saints-Pères, 75270 Paris, Cedex 06, France
H. GIOANNI
Affiliation:
Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, UMR 7060, CNRS-Université René Descartes, 45 rue des Saints-Pères, 75270 Paris, Cedex 06, France
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Abstract

We studied the cervico-ocular reflex (COR) alone and in combination with the optokinetic (OKN) reflex in head-fixed pigeons. We analyzed these responses in two behavioral conditions: (1) animals were hung in a harness (“resting” condition); and (2) animals were additionally submitted to a frontal airflow that provoked a flight posture (“flying” condition). In both conditions, cervical stimulation provoked a slow phase of very low gain (around 0.05) in the opposite direction to that of the stimulation and fast phases triggered near the head–body alignment in the same direction as the stimulation. The slow phase showed a phase lag of 20 deg at 0.5 Hz. The gain of the slow phase was not modified by the velocity, amplitude, or frequency of the stimuli. This gain was not changed by the presence of a fixed visual surround.

When cervical stimuli (0.05–0.5 Hz) were added to an optokinetic stimulation (30 deg/s) in the “resting” condition, the slow phase velocity (SPV) of the optokinetic reflex was modulated with a time course close to that produced by the cervico-ocular reflex alone. The SPV was alternately increased and decreased round the SPV level corresponding to the steady-state OKN. In the “flying” condition, optokinetic-cervical stimulation provoked an eye beating field and a strong SPV modulation synchronized with the position of the cervical stimulation. The number of nystagmic beats (OKN) and the amplitude and velocity of the fast phases were modulated in correlation with the SPV. Consequently, the optokinetic response was increased or decreased according to whether the cervical stimuli were in the reverse direction or in the same direction as the optokinetic stimulation, respectively.

These data are interpreted as an improvement of gaze stabilization by the COR. This mechanism is context dependent, since it is strongly reinforced during the flight.

Keywords

Cervico-ocular reflexOptokinetic reflexNeck proprioceptionFlight behaviorBirds
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 2 , March 2004 , pp. 167 - 180
Copyright
2004 Cambridge University Press

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References

REFERENCES

Anastasopoulos, D. & Mergner, T. (1982). Canal-neck interaction in vestibular nuclear neurons of the cat. Experimental Brain Research 46, 269–280.CrossRefGoogle Scholar
Anastasopoulos, D., Mandellos, D., Kostadima, V., & Pettorossi, V.E. (2002). Eye position signals modify vestibulo- and cervico-ocular fast phases during passive yaw rotations in humans. Experimental Brain Research 145, 480–488.CrossRefGoogle Scholar
André-Deshays, C., Berthoz, A., & Revel, M. (1988). Eye-head coupling in humans. I. Simultaneous recording of isolated motor units in dorsal neck muscles and horizontal eye movements. Experimental Brain Research 69, 399–406.CrossRefGoogle Scholar
André-Deshays, C., Revel, M., & Berthoz, A. (1991). Eye-head coupling in humans. II. Phasic components. Experimental Brain Research 84, 359–366.CrossRefGoogle Scholar
Barlow, H.B. & Freedman, W. (1980). Cervico-ocular reflex in the normal adult. Acta Otolaryngologica (Stockholm) 89, 487–496.CrossRefGoogle Scholar
Barmack, N.H., Nastos, M.A., & Pettorossi, V.E. (1981). The horizontal and vertical cervico-ocular reflexes of the rabbit. Brain Research 224, 361–278.CrossRefGoogle Scholar
Barmack, N.H., Errico, P., Ferraresi, A., & Pettorossi, V.E. (1989). Interactions of cervico-ocular and vestibulo-ocular fast phase signals in the control of eye position in rabbits. Journal of Physiology 410, 213–225.CrossRefGoogle Scholar
Barnes, G.R. & Forbat, L.N. (1979). Cervical and vestibular afferent control of oculomotor response in man. Acta Otolaryngologica (Stockholm) A 88, 79–87.CrossRefGoogle Scholar
Bilo, D. (1992). Optocollic reflexes and neck flexion-related activity of flight control muscles in the airflow-stimulated pigeon. In The Head–Neck Sensory Motor System, ed. Berthoz, A., Graf, W.M. & Vidal, P.P., pp. 96–100. Oxford: Oxford University Press.CrossRef
Bilo, D. & Bilo, A. (1978). Wind stimuli control vestibular and optokinetic reflexes in the pigeon. Naturwissenschaften 65, 161–162.CrossRefGoogle Scholar
Bilo, D. & Bilo, A. (1983). Neck flexion related activity of flight control muscles in the flow-stimulated pigeon. Journal of Comparative Physiology 153, 111–122.CrossRefGoogle Scholar
Bohmer, A. & Henn, V. (1983). Horizontal and vertical vestibulo-ocular and cervico-ocular reflexes in the monkey during high frequency rotation. Brain Research 277, 241–248.CrossRefGoogle Scholar
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 Scholar
Bronstein, A.M., Mossman, S., & Luxon, L.M. (1991). The neck-eye reflex in patients with reduced vestibular and optokinetic function. Brain 114, 1–11.Google Scholar
Denia, A., Lau, C.G.Y., Kim, Y.H., & Honrubia, V. (1979). Static cervico-ocular reflex in optokinetic reflex interaction in rabbits. Journal of Comparative Physiology 134, 11–15.CrossRefGoogle Scholar
Dichgans, J., Bizzi, E., Morasso, P., & Tagliasco, V. (1973). Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys. Experimental Brain Research 18, 548–562.Google Scholar
Erichsen, J.T., Hodos, W., Evinger, C., Bessette, B.B., & Phillips, S.J. (1989). Head orientation in pigeons: Postural, locomotor and visual determinants. Brain, Behavior, and Evolution 33, 268–278.CrossRefGoogle Scholar
Fuller, J.H. (1980). The dynamic neck-eye reflex in mammals. Experimental Brain Research 41, 29–35.CrossRefGoogle Scholar
Frost, B.J. (1978). The optokinetic basis of head bobbing in the pigeon. Journal of Experimental Biology 74, 187–195.Google Scholar
Gdowski, G.T., Belton, T., & McRea, T. (2001). The neurophysiological substrate for the cervico-ocular reflex in the squirrel monkey. Experimental Brain Research 147, 89–97.Google Scholar
Gioanni, H. & Sansonetti, A. (1999). Characteristics of slow and fast phases of the optocollic reflex (OCR) in head free pigeons (Columba livia). Influence of flight behaviour. European Journal of Neuroscience 11, 155–166.Google Scholar
Gioanni, H., Sansonetti, A., & Bennis, M. (1997). Characteristics of cervico-ocular responses in the chameleon. Visual Neuroscience 14, 1175–1184.CrossRefGoogle Scholar
Grantyn, A. & Berthoz, A. (1987). Reticulospinal 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 Scholar
Grantyn, A., Ong-Meang Jacques, V., & Berthoz, A. (1987). Reticulospinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase. Experimental Brain Research 66, 355–377.Google Scholar
Gresty, M.A. (1976). A reexamination of “neck reflex” eye movements in the rabbit. Acta Otolaryngologica (Stocklolm) 81, 386–394.CrossRefGoogle Scholar
Gurfinkel, V.S. & Levik, Y.S. (1993). The suppression of cervico-ocular response by the haptokinetic information about the contact with a rigid, immobile object. Experimental Brain Research 95, 359–364.Google Scholar
Heimbrand, S., Bronstein, A.M., Gresty, M.A., & Faldon, M.E. (1996). Optically induced plasticity of the cervico-ocular reflex in patients with bilateral absence of vestibular function. Experimental Brain Research 112, 372–380.Google Scholar
Hikosaka, O. & Maeda, M. (1973). Cervical effects on abducens motoneurons and their interaction with vestibulo-ocular reflex. Experimental Brain Research 18, 512–530.Google Scholar
Hikosaka, O., Igusa, Y., & Imai, H. (1978). Firing pattern of prepositus hypoglossi and adjacent reticular neurons related to vestibular nystagmus in the cat. Brain Research 144, 395–403.CrossRefGoogle Scholar
Huygen, P.L.M., Verhagen, W.I.M., & Nicolasen, M.G.M. (1991). Cervico-ocular reflex enhancement in labyrinthine-defective and normal subjects. Experimental Brain Research 87, 457–464.Google Scholar
Jurgens, R. & Mergner, T. (1989). Interaction between cervico-ocular and vestibulo-ocular reflexes in normal adults. Experimental Brain Research 77, 381–390.CrossRefGoogle Scholar
Kasai, T. & Zee, D.S. (1978). Eye-head coordination in labyrinthine-defective human beings. Brain Research 48, 279–287.CrossRefGoogle Scholar
Lestienne, F., Whittington, D.A., & Bizzi, E. (1981). Single cell recording from the pontine reticular formation in monkey: Behavior of preoculomotor neurons during eye-head coordination. In Progress in Oculomotor Research. Developments in Neuroscience, Vol. 12, ed. Fuchs, A.F. & Becker, W., pp. 325–333. Amsterdam, Holland: Elsevier/North-Holland Biomedical Press.
Lestienne, F., Vidal, P.P., & Berthoz, A. (1984). Gaze changing behaviour in head restrained monkey. Experimental Brain Research 53, 349–356.CrossRefGoogle Scholar
Lopez-Barneo, J., Darlot, C., Berthoz, A., & Baker, R. (1982). Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. Journal of Neurophysiology 47, 329–352.Google Scholar
Maurice, M. & Gioanni, H. (2004). Eye-neck coupling during optokinetic responses in head-fixed pigeons (Columba livia); Influence of the flying behaviour. Neuroscience 125(2), 521–531.CrossRefGoogle Scholar
Meier, R.K. & Dieringer, N. (1993). The role of compensatory eye and head movements in the rat for image stabilization and gaze orientation. Experimental Brain Research 96, 54–64.CrossRefGoogle Scholar
Meiry, J.L. (1972). Vestibular and proprioceptive stabilization of eye movements. In The Control of Eye Movements, ed. Bach-y-Rita, P., Collins, C.C. & Hyde, J.E., pp. 483–496. New York: Academic Press.
Mergner, T., Siebold, C., Schweigart, G., & Becker, W. (1991). Human perception of horizontal head and trunk rotation in space during vestibular and neck stimulation. Experimental Brain Research 85, 389–404.Google Scholar
Mirenowicz, J. & Hardy, O. (1992). Characteristics of saccades induced by neck torsions: A re-examination in the normal guineapig. Brain Research 592, 1–7.CrossRefGoogle Scholar
Nakamura, T. & Bronstein, A.M. (1993). Perception of neck rotation assessed by “remembered saccades”. NeuroReport 4, 237–239.CrossRefGoogle Scholar
Nakamura, T. & Bronstein, A.M. (1995). The perception of neck and head angular displacement in normal and labyrinthine-defective subjects. A quantitative study using a ‘remembered saccade’ technique. Brain 118, 1157–1168.Google Scholar
Peterson, B.W. (1988). Cervicocollic and cervicoocular reflex. In Control of Head Movement, ed. Peterson, B.W. & Richmond, F.J., pp. 90–99. New York: Oxford University Press.
Pettorossi, V.E., Manni, E., Errico, P., Ferraresi, A., & Bortolami, R. (1997). Otolithic and extraocular muscle proprioceptive influences on the spatial organization of the vestibulo- and cervico-ocular quick phases. Acta Otolaryngologica 117, 139–142.CrossRefGoogle Scholar
Rioult-Pedotti, M.S. & Dieringer, N. (1988). The cervico-ocular reflex in intact and chronically labyrinthectomized frogs. Neuroscience Letters 90, 135–140.CrossRefGoogle Scholar
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions on Biomedical Electronics 10, 137–145.Google Scholar
Roucoux, A., Vidal, P.P., Veraart, C., Crommelinck, M., & Berthoz, A. (1982). The relation of neck muscles activity to horizontal eye position in the alert cat. I Head fixed. In Physiological and Pathological Aspects of Eye Movements, ed. Roucoux, A. & Crommelinck, M., pp. 371–378. Dr W. The Hague, Holland: Junk Publishers.CrossRef
Roucoux, A., Crommelinck, M., & Decostre, M.F. (1989). Neck muscle activity in eye-head coordinated movements. Progress in Brain Research 80, 351–362.CrossRefGoogle Scholar
Sawyer, R.N., Jr., Thurston, S.E., Becker, K.R., Ackley, C.V., Seidman, S.H., & Leigh, R.J. (1994). The cervico-ocular reflex of normal human subjects in response to transient and sinusoidal trunk rotations. Journal of Vestibular Research 4, 245–249.Google Scholar
Skliut, I.A., Likhachev, S.A., & Skliut, M.I. (1999). The role of cervical proprioceptive afferentation in compensatory mechanisms of vestibular dysfunction. 1. Passive cervico-ocular reflex in unilateral labyrinthine lesion. Vestnik Otorinolaringologii 2, 34–38.Google Scholar
Troje, N.F. & Frost, B.J. (2000). Head-bobbing in pigeons: How stable is the hold phase? Journal of Experimental Biology 203, 935–940.Google 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 Scholar
Vidal, P.P., Corvisier, J., & Berthoz, A. (1983). Eye and neck motor signals in periabducens reticular neurons of the alert cat. Experimental Brain Research 53, 16–28.Google Scholar