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Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow

Published online by Cambridge University Press:  02 June 2009

Douglas R. Wylie
Affiliation:
Department of Psychology, Queen's University at Kingston, Kingston, Ontario, Canada, K7L 3N6
Barrie J. Frost
Affiliation:
Department of Psychology, Queen's University at Kingston, Kingston, Ontario, Canada, K7L 3N6

Abstract

Previous electrophysiological studies have shown that neurons in the nucleus of the basal optic root (nBOR) of the pigeon respond best to wholefield stimuli moving slowly in a particular direction in the contralateral visual field. In this study, we have found that some nBOR neurons respond to wholefield stimulation of both eyes. These binocular neurons have spatially separate receptive fields in both visual fields. Some binocular neurons prefer the same direction of wholefield motion in both eyes, and thus respond best to wholefield visual motion which would result from translation movements of the bird, either ascent, descent, or forward and backward motion. Other neurons prefer opposite directions of wholefield motion in each eye and therefore respond optimally to wholefield visual motion simulating rotational movements of the bird, either roll or yaw. These binocular neurons may play a crucial part in the locomotor behavior of the pigeon by providing visual information distinguishing translational and rotational movements.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

Brecha, N., Karten, H.J. & Hunt, S.P. (1980). Projections of the nucleus of basal optic root in the pigeon: an autoradiographic and horseradish perioxidase study. Journal of Comparative Neurology 189, 615670.CrossRefGoogle Scholar
Britto, L.G.R., Natal, C.L. & Macondes, A. M. (1981). The accessory optic system in pigeons: receptive-field properties of identified neurons. Brain Research 206, 149154.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, 171180.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, 268278.CrossRefGoogle ScholarPubMed
Fite, K.V., Brecha, N., Karten, H.J. & Hunt, S.P. (1981). Displaced ganglion cells and the accessory optic system of the pigeon. Journal of Comparative Neurology 195, 279288.CrossRefGoogle ScholarPubMed
Fite, K.V., Reiner, T. & Hunt, S. (1979). Optokinetic nystagmus and the accessory optic system of pigeon and turtle. Brain, Behavior, and Evolution 16, 192202.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. 177196. 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., Jeannerod, M. & Lee, D., pp. 415449. Dordrecht: Martinus Nijhoft.CrossRefGoogle Scholar
Frost, B.J., Cavanaugh, P. & Morgan, B. (1988). Deep tectal cells in pigeons respond to kinematograms. Journal of Comparative Physiology A 162, 639647.CrossRefGoogle ScholarPubMed
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 (in press).CrossRefGoogle Scholar
Gamlin, P. D. R. & Cohen, D. H. (1988). Retinal projections to the pretectum in the pigeon (Columba livia). Journal of Comparative Neurology 269, 117.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 (Columbia livia). Experimental Brain Research 57, 4960.CrossRefGoogle ScholarPubMed
Gioanni, H., Rey, J., Villalobos, J., Richard, D. & Dalbera, A. (1983 a). Optokinetic nystagmus in the pigeon (Columbia livia), II: Role of the pretectal nucleus of the accessory optic system (AOS). Experimental Brain Research 50, 237247.Google Scholar
Gioanni, H., Rey, J., Villalobos, J. & Dalbera, A. (1983 b). Optokinetic nystagmus in the pigeon (Columba livia), III: Role of the nucleus ectomamillaris (nEM): interactions in the accessory optic system (AOS). Experimental Brain Research 50, 248258.Google ScholarPubMed
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, 20912121.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Cynader, M.S. (1984). Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. Journal of Neurophysiology 51, 276293.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Cynader, M.S. (1986). Response properties of single units in the accessory optic system of the dark-reared cat. Developmental Brain Research 27, 199210.CrossRefGoogle Scholar
Hoffmann, K.-P., Distler, C., Krikson, R.G. & Mader, W. (1988). Physiological and anatomical identification of the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in monkeys. Experimental Brain Research 69, 635644.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Schoppmann, A. (1981). A quantitative analysis of the direction-specific responses of neurons in the cat's nucleus of the optic tract. Experimental Brain Research 42, 146157.CrossRefGoogle ScholarPubMed
Howard, I.P. & Simpson, W.A. (1989). Human optokinetic nystagmus is linked to the stereoscopic system. Experimental Brain Research 78, 309314.CrossRefGoogle Scholar
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba Livia). Baltimore: Johns Hopkins Press.Google Scholar
Karten, H.J., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon (Columbia livia). Proceedings of the National Academy of Science of the U.S.A. 74, 17521756.CrossRefGoogle ScholarPubMed
Leonard, C.S., Simpson, J.I. & Graf, W. (1988). Spatial organization of visual messages of the rabbit's cellebellar flocculus, I: Typology of inferior olive neurons of the dorsal cap of Kooy. Journal of Neurophysiology 60, 20732096.CrossRefGoogle Scholar
Manteuffel, G. (1987). Binocular afferents to the salamander pretecturn mediate rotation sensitivity of cells selective for visual background motions. Brain Research 422, 381383.CrossRefGoogle Scholar
Martin, G.R. & Young, S.R. (1983). The retinal binocular field of the pigeon (Columba Livia: English racing homer). Vision Research 23, 911915.CrossRefGoogle ScholarPubMed
McKenna, O. & Wallman, J. (1981). Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose. Brain Research 210, 455460.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, 330342.CrossRefGoogle ScholarPubMed
Morgan, B. & Frost, B. (1981). Visual response properties of neurons in the nucleus of the basal optic root of pigeons. Experimental Brain Research 42, 184188.CrossRefGoogle Scholar
Mustari, M.J. & Fuchs, A.F. (1989). Response properties of single units in the lateral terminal nucleus (LTN) of the behaving primate. Journal of Neurophysiology 61, 12071220.CrossRefGoogle ScholarPubMed
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, 529540.CrossRefGoogle ScholarPubMed
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 16791688.CrossRefGoogle Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 1341.CrossRefGoogle ScholarPubMed
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988). The accessory optic system of rabbit, II: Spatial organization of direction selectivity. Journal of Neurophysiology 60, 20552072.CrossRefGoogle ScholarPubMed
Soodak, R.E. & Simpson, J.I. (1988) The accessory optic system of rabbit, I: Basic visual response properties. Journal of Neurophysiology 60, 20372054.CrossRefGoogle ScholarPubMed
Volchan, E., Rocha-Miranda, C.E., Picanco-Diniz, C.W., Zins-Meisser, B., Bernares, R.F. & Franca, J.G. (1989). Visual response properties of pretectal units in the nucleus of the optic tract of the opossum. Experimental Brain Research 78, 380386.CrossRefGoogle ScholarPubMed
Wallman, J., McKenna, O.C., Bums, S., Velez, J. & Weinstein, B. (1981). Relation of the accessory optic system and pretectum to optokinetic responses in chickens. In Progress in Oculomotor Research, ed. Fuchs, A. & Becker, W., pp. 435442. North Holland: Elsevier.Google Scholar
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, 215226.CrossRefGoogle ScholarPubMed
Wylie, D.R. & Frost, B.J. (1990 a). The visual response properties of neurons in the nucleus of the basal optic root of the pigeon: a quantative analysis. Experimental Brain Research (in press).CrossRefGoogle Scholar
Wylie, D.R. & Frost, B.J. (1990 b). Distinguishing rotation from translation: neurons in pigeon vestibulocerebellum specify different patterns of wholefield motion. Society for Neuroscience Abstracts 16, 1314.Google Scholar