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The pigeon optokinetic system: Visual input in extraocular muscle coordinates

Published online by Cambridge University Press:  02 June 2009

Douglas R. W. Wylie  and
Barrie J. Frost
Douglas R. W. Wylie
Affiliation:
Department of Psychology, University of Alberta, Edmonton, Alberta, Canada T6G 2E1
Barrie J. Frost
Affiliation:
Department of Psychology, Queen's University, Kingston, Ontario, Canada K7L 3N6
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Abstract

The generation of compensatory eye movements in response to rotational head movements involves the transformation of visual-optokinetic and vestibular signals into commands controlling the appropriate eye muscles. Previously, it has been shown that the three systems (optokinetic, vestibular, and eye muscle) share a similar three-dimensional reference frame. In this report, we suggest that a peculiarity in the structure of the horizontal recti in pigeons demonstrates that the optokinetic system is organized with respect to the eye muscles rather than the vestibular canals. Measurements of the orientation of the plane for each of the lateral and medial recti were obtained. These were compared with the direction preferences of optokinetic neurons responsive to horizontal motion, namely “back” units in the nucleus of the basal optic root (nBOR), “forward” units in the pretectal nucleus lentiformis mesencephali (LM), and “vertical axis” (VA) Purkinje cells in the flocculus. The average direction preference of LM neurons excited in response to forward (temporal to nasal) visual motion, and VA Purkinje cells in response to optokinetic motion in the ipsilateral visual field was approximately parallel to the visual horizontal. This corresponded to the orientation of the medial rectus, which was also approximately parallel to the visual horizontal. The average direction preference of nBOR neurons excited in response to backward (nasal to temporal) visual motion, and VA Purkinje cells in response to optokinetic motion in the contralateral visual field was approximately 20–30 deg down from the visual horizontal. The orientation of the lateral rectus was also approximately 20–30 deg down from the visual horizontal. These data suggest that the incoming optokinetic signals are organized with respect to the outgoing extraocular muscle commands.

Keywords

OptokineticAccessory optic systemVestibular canalsEye musclesVestibulocerebellum
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 945 - 953
Copyright
Copyright © Cambridge University Press 1996

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References

Baldo, M.V. (1990). The spatial arrangement of the semicircular canals of the pigeon. Brazilian Journal of Medical and Biological Research 23, 914–917.Google ScholarPubMed
Brecha, N., Karten, H.J. & Hunt, S.P. (1980). Projections of the nucleus of basal optic root in the pigeon: An autoradiographic and horseradish peroxidase study. Journal of Comparative Neurology 189, 615–670.CrossRefGoogle ScholarPubMed
Britto, L.G.R., Natal, C.L. & Marcondes, A.M. (1981). The accessory optic system in pigeons: Receptive field properties of identified neurons. Brain Research 206, 149–154.CrossRefGoogle ScholarPubMed
Burns, S. & Wallman, J. (1981). Relation of single unit properties to the oculomotor function of the nucleus of the basal optic root (AOS) in chickens. Experimental Brain Research 42, 171–180.CrossRefGoogle Scholar
Clarke, P.G.H. (1977). Some visual and other connections to the cerebellum of the pigeon. Journal of Comparative Neurology 174, 535–552.CrossRefGoogle Scholar
Davies, M.N.O. & Green, P.R. (1988). Head-bobbing during walking, running and flying: Relative motion perception in the pigeon. Journal of Experimental Biology 138, 71–91.CrossRefGoogle 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.Google ScholarPubMed
Ezure, K. & Graf, W. (1984). A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral and frontal-eyed animals. I. Orientation of semicircular canals and extraocular muscles. Neuroscience 12, 85–93.CrossRefGoogle ScholarPubMed
Friedman, M.B. (1975). Visual control of head movements during avian locomotion. Nature 225, 67–69.CrossRefGoogle Scholar
Frost, B.J. (1978). Moving background patterns alter directionally specific responses of pigeon tectal neurons. Brain Research 151, 599–603.CrossRefGoogle ScholarPubMed
Frost, B.J. (1982). Mechanisms for discriminating object motion from self-induced motion in the pigeon. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, J.W., pp. 177–196. Cambridge: MIT Press.Google Scholar
Frost, B.J. (1985). Neural mechanisms for detecting object motion and figure-ground boundaries contrasted with self-motion detecting systems. In Brain Mechanisms of Spatial Vision, ed. Ingle, D.J., Jean-Nerod, M., & Lee, D., pp. 415–449. Dordrecht: Martinus Nijhoff.CrossRefGoogle Scholar
Frost, B.J. (1993). Subcortical analysis of visual motion: Relative motion, figure-ground discrimination and self-induced optic flow. In Visual Motion and Its Role in the Stabilization of Gaze, ed. Miles, F.A. & Wallman, J., pp 159–175. Amsterdam: Elsevier.Google Scholar
Frost, B.J., Wylie, D.R. & Wang, Y-C. (1990). The processing of object and self-motion in the tectofugal and accessory optic pathways of birds. Vision Research 30, 1677–1688.CrossRefGoogle ScholarPubMed
Frost, B.J., Wylie, D.R. & Wang, Y-C. (1994). The analysis of motion in the visual systems of birds. In Perception and Motor Control in Birds, ed. Green, P. & Davies, M., pp. 249–266. Berlin: Springer-Verlag.Google Scholar
Gioanni, H. (1988). Stabilizing gaze reflexes in the pigeon (Columbalivia). I. Horizontal and vertical optokinetic eye (OKN) and head (OCR) reflexes. Experimental Brain Research 69, 567–582.CrossRefGoogle Scholar
Gioanni, H., Rey, J., Villalobos, J. & Dalbera, A. (1984). Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic, vestibular and visuo-vestibular stimulations in the alert pigeon (Columba livia). Experimental Brain Research 51, 49–60.Google Scholar
Graf, W. & Simpson, J.I. (1981). The relations between the semicircular canals, the optic axis, and the extraocular muscle in lateral-eyed and frontal-eyed animals. In Progress in Oculomotor Research. Developments in Neuroscience, Vol. 12, ed. Fuchs, A. & Becker, W., pp. 409–417. Amsterdam: Elsevier.Google Scholar
Graf, W., Simpson, J.I. & Leonard, C.S. (1988). Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. Journal of Neurophysiology 60, 2091–2121.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Cynader, M.S. (1982). Electrophysiology of the medial terminal nucleus of accessory optic system in the cat. Journal of Neurophysiology 51, 276–293.CrossRefGoogle Scholar
Kano, M-S., Kano, M. & Maekawa, K. (1990). Receptive field organization of climbing fiber afferents responding to optokinetic stimulation in the cerebellar nodulus and flocculus of the pigmented rabbit. Experimental Brain Research 82, 499–512.CrossRefGoogle ScholarPubMed
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba Livia). Baltimore, Maryland: Johns Hopkins Press.Google Scholar
Knudsen, E.I., Du Lac, S. & Esterly, S.D. (1987). Computational maps in the brain. Annual Review of Neuroscience 10, 41–65.CrossRefGoogle ScholarPubMed
Leonard, C.S., Simpson, J.I. & Graf, W. (1988). Spatial organization of visual messages of the rabbit's cerebellar flocculus. I. Typology of inferior olive neurons of the dorsal cap of Kooy. Journal of Neurophysiology 60, 2073–2090.CrossRefGoogle ScholarPubMed
Masino, T. & Knudsen, E.I. (1990). Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl. Nature 345, 434–437.CrossRefGoogle ScholarPubMed
McKenna, O. & Wallman, J. (1981). Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose. Brain Research 210, 455–460.CrossRefGoogle ScholarPubMed
McKenna, O. & Wallman, J. (1985). Functional postnatal changes in avian brain regions responsive to retinal slip: A 2-deoxy-D-glucose study. Journal of Neuroscience 5, 330–342.CrossRefGoogle ScholarPubMed
Morgan, B. & Frost, B.J. (1981). Visual response properties of neurons in the nucleus of the basal optic root of pigeons. Experimental Brain Research 42, 184–188.CrossRefGoogle Scholar
Nalbach, H-O., Wolf-Oberhollenzer, F. & Kirschfeld, K. (1990). The pigeon's eye viewed through an ophthalmoscopic microscope: Orientation of retinal landmarks and significance of eye movements. Vision Research 30, 529–540.CrossRefGoogle ScholarPubMed
Nye, P. (1969). The monocular eye movements of the pigeon. Vision Research 9, 133–144.CrossRefGoogle ScholarPubMed
Owen, B.M. & Lee, D.N. (1986). Establishing a frame of reference. In Motor Development in Children: Aspects of Coordination and Control, ed. Wade, M.G. & Whiting, H.T.A. Dordrecht: Martinus Nijhoff.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.CrossRefGoogle ScholarPubMed
Simpson, J.I. (1989). Maps and Reference Frames in the Brain. Tin-bergen Professor Lecture, Erasmus University, Feb. 9, 1989.Google Scholar
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988 a). The pretectal nuclear complex and the accessory optic system. In Neuroanatomy of the Oculomotor System, ed. Buttner-Ennever, J.A., pp. 335–364. Amsterdam: Elsevier.Google Scholar
Simpson, J.I. & Graf, W. (1981). Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Annals of the New York Academy of Sciences 374, 20–30.CrossRefGoogle ScholarPubMed
Simpson, J.I. & Graf, W. (1985). The selection of reference frames by nature and its investigators. In Adaptive Mechanisms in Gaze Control: Facts and Theories, ed. Berthoz, A. & Melvill-Jones, G., pp. 3–16. Amsterdam: Elsevier.Google Scholar
Simpson, J.I., Graf, W. & Leonard, C. (1981). The coordinate system of visual climbing fibres to the flocculus. In Progress in Oculomotor Research, ed. Fuchs, A.F. & Becker, W., pp. 475–484. Amsterdam: Elsevier.Google Scholar
Simpson, J.I., Graf, W. & Leonard, C. (1989 a). Three-dimensional representation of retinal image movement by climbing fiber activity. In The Olivocerebellar System in Motor Control: Experimental Brain Research Supplement, Vol. 17, ed. Strata, P., pp. 323–327. Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988 b). The accessory optic system of rabbit. II. Spatial organization of direction selectivity. Journal of Neurophysiology 60, 2055–2072.CrossRefGoogle ScholarPubMed
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988 c). The accessory optic system: Analyzer of self-motion. Annals of the New York Academy of Science 545, 170–179.CrossRefGoogle ScholarPubMed
Simpson, J.I., Van Der Steen, J., Tan, J., Graf, W. & Leonard, C.S. (1989 b). Representations of ocular rotations in the cerebellar flocculus of the rabbit. In Progress in Brain Research, Vol. 80, ed. Allum, J.H.J. & Hulliger, M., pp. 213–223. Amsterdam: Elsevier.Google Scholar
Van Der Steen, J., Simpson, J.I. & Tan, J. (1994). Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus. Journal of Neurophysiology 72, 31–46.CrossRefGoogle ScholarPubMed
Wallman, J., McKenna, O.C., Burns, S., Velez, J. & Weinstein, B. (1981). Relation of the accessory optic system and pretectum to optokinetic responses in chickens. In Progress in Oculomotor Research, Developmental Neuroscience, Vol. 12, ed. Fuchs, A.F. & Becker, W., pp. 435–442. Amsterdam: Elsevier.Google Scholar
Wilson, V.J., Anderson, J.A. & Felix, D. (1974). Unit and field potential activity evoked in pigeon vestibulocerebellum by stimulation of individual semicircular canals. Experimental Brain Research 19, 142–157.CrossRefGoogle ScholarPubMed
Wilson, V.J. & Felpel, L.P. (1972). Specificity of semicircular canal input to neurons in the pigeon vestibular nuclei. Journal of Neurophysiology 35, 253–264.CrossRefGoogle ScholarPubMed
Winterson, B.J. & Brauth, S.E. (1985). Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia). Experimental Brain Research 60, 215–226.CrossRefGoogle ScholarPubMed
Wolf-Oberhollenzer, F. & Kirschfeld, K. (1994). Motion sensitivity in the nucleus of the basal optic root of the pigeon. Journal of Neurophysiology 71, 1559–1573.CrossRefGoogle ScholarPubMed
Wylie, D.R. (1991). Neural mechanisms distinguishing self-translation and self-rotation in the pigeon. Unpublished Ph.D. Dissertation, Queen's University at Kingston.Google Scholar
Wylie, D.R. & Frost, B.J. (1990 a). Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Visual Neuroscience 5, 489–495.CrossRefGoogle ScholarPubMed
Wylie, D.R. & Frost, B.J. (1990 b). Visual response properties of neurons in the nucleus of the basal optic root of the pigeon: A quantitative analysis. Experimental Brain Research 82, 327–336.CrossRefGoogle ScholarPubMed
Wylie, D.R. & Frost, B.J. (1993). Responses of pigeon vestibulocer-ebellar neurons to optokinetic stimulation: II. The 3-dimensional reference frame of rotation neurons in the flocculus. Journal of Neurophysiology 70, 2647–2659.CrossRefGoogle ScholarPubMed
Wylie, D.R., Kripalani, T-K. & Frost, B.J. (1993). Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation: I. Functional organization of neurons discriminating between translational and rotational visual flow. Journal of Neurophysiology 70, 2632–2646.CrossRefGoogle ScholarPubMed
Yakushin, S., Dai, M., Suzuki, J-I., Raphan, T. & Cohen, B. (1995). Semicircular canal contributions to the three-dimensional veslibuloocular reflex: A model based approach. Journal of Neurophysiology 74, 2722–2737.CrossRefGoogle Scholar