Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T00:46:03.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Visual telencephalon modulates directional selectivity of accessory optic neurons in pigeons

Published online by Cambridge University Press:  02 June 2009

Luiz R.G. Britto ,
Odival C. Gasparotto  and
Dânia E. Hamassaki
Luiz R.G. Britto
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences Sāo Paulo State University (USP), Sāo Paulo, SP, Brazil
Odival C. Gasparotto
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences Sāo Paulo State University (USP), Sāo Paulo, SP, Brazil
Dânia E. Hamassaki
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences Sāo Paulo State University (USP), Sāo Paulo, SP, Brazil
Get access Rights & Permissions [Opens in a new window]

Abstract

The directional selectivity of units within the nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) was studied before and after lesions of the visual telencephalon (visual Wulst) in urethane-anesthetized pigeons. In intact pigeons, most nBOR units preferred upward motion with a temporal component or downward motion with a nasal component. The ipsilateral and bilateral telencephalic lesions generated a dramatic reduction in the number of cells with optimal responses to upward motion. The overall distribution of preferred directions was still bimodal following ipsilateral or bilateral Wulst lesions, with most units showing best responses to a straight temporal or to downward-nasal directions. The contralateral Wulst lesions produced, instead, a marked reduction in downward preferences. The nBOR units which were studied in these cases showed mainly upward-temporal and upward-nasal responses. These data suggest an involvement of the visual Wulst in the determination of the dictional selectivity of nBOR neurons in the pigeon. Specifically, the responses of nBOR units to upward motion appeared to depend on the integrity of the telencephalic descending systems which impinge, in both direct and indirect ways, upon that AOS nucleus. Taken together with data for the mammalian AOS, the present results indicate that nonretinal afferents to AOS nuclei have an important role in the functional organization of that subcortical visual pathway.

Keywords

Accessory optic systemDirection selectivitySubcortical visual pathwaysVisual cortexVisual system
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 1 , January 1990 , pp. 3 - 10
Copyright
Copyright © Cambridge University Press 1990

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

Azevedo, T.A., Cukiert, A. & Britto, L.R.G. (1983). A pretectal projection upon the accessory optic nucleus in the pigeon: an anatomical and electrophysiological study. Neuroscience Letters 43, 13–18.Google Scholar
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. Journal of Physiology 173, 377–407.CrossRefGoogle ScholarPubMed
Berson, D.M. & Graybiel, A.M. (1980). Some cortical and subcortical fiber projections to the accessory optic nuclei in the cat. Neuroscience 5, 2203–2217.Google Scholar
Brecha, N. & Karten, H.J. (1981). Organization of the avian accessory optic system. Annals of the New York Academy of Sciences 374, 215–229.CrossRefGoogle ScholarPubMed
Brecha, N., Karten, H.J. & Hunt, S.P. (1980). Projections of the nucleus of the basal optic root in the pigeon: an autoradiographic and horseradish peroxidase study. Journal of Comparative Neurology 189, 615–670.CrossRefGoogle ScholarPubMed
Britto, L.R.G., Hamassaki, D.E. & Gasparotto, O.C. (1988). The visual Wulst modulates the directional selectivity of accessory optic units in the pigeon. Society for Neuroscience Abstracts 14, 990.Google Scholar
Britto, L.R.G., 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 (accessory optic system) in chickens. Experimental Brain Research 42, 171–180.Google Scholar
Emmerton, J. (1983). Functional morphology of the visual system. In Physiology and Behavior of the Pigeon, ed. Abs, M., pp. 221–244. London: Academic Press.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 ScholarPubMed
Fite, K.V. (1985). Pretectal and accessory optic visual nuclei of fish, amphibia, and reptiles: theme and variations. Brain Behavior and Evolution 26, 71–90.Google Scholar
Gamlin, P.D.R. & Cohen, D.H. (1988). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 18–46.Google Scholar
Giolli, R.A., Peterson, G.M., Ribak, C.E., McDonald, H.M., Blanks, R.H.I. & Fallon, J.H. (1985). GABAergic neurons comprise a major cell type in rodent visual relay nuclei: an immunocytochemical study of pretectal and accessory optic nuclei. Experimental Brain Research 61, 194–203.Google Scholar
Giolli, R.A., Torigoe, Y. & Blanks, R.H.I. (1988). Nonretinal projections to the medial terminal accessory optic nucleus in rabbit and rat: a retrograde and anterograde transport study. Journal of Comparative Neurology 269, 73–86.Google Scholar
Gottlieb, M.D. & McKenna, O.C. (1986). Light- and electron- microscopic study of an avian pretectal nucleus, the lentiform nucleus of the mesencephalon, magnocellular division. Journal of Comparative Neurology 248, 133–145.Google Scholar
Grasse, K.L. & Cynader, M.S. (1982). Electrophysiology of medial terminal nucleus of accessory optic system in the cat. Journal of Neurophysiology 48, 490–504.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, 276–293.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, 199–210.Google Scholar
Grasse, K.L. & Cynader, M.S. (1987). The accessory optic system of the monocularly deprived cat. Brain Research 428, 229–241.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Cynader, M.S. (1988). The effect of visual cortex lesions on vertical optokinetic nystagmus in the cat. Brain Research 455, 385–389.CrossRefGoogle ScholarPubMed
Grasse, K.L., Cyndaer, M.S. & Douglas, R.M. (1984). Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions. Experimental Brain Research 55, 69–80.CrossRefGoogle ScholarPubMed
Grueerg, E.R. & Grasse, K.L. (1984). Basal optic complex in the frog (Rana pipiens): a physiological and HRP study. Journal of Neurophysiology 51, 998–1010.Google Scholar
Hayes, B.P. & Holden, A.L. (1983). The distribution of displaced ganglion cells in the retina of the pigeon. Experimental Brain Research 49, 181–188.Google ScholarPubMed
Hodos, W., Erichsen, J.T., Bessette, B.B. & Phillips, S.J. (1984). Head orientation in pigeons: postural, locomotor, and visual determinants. Society for Neuroscience Abstracts 10, 397.Google Scholar
Hoffmann, K.-P. (1982). Cortical versus subcortical contributions to the optokinetic reflex in the cat. In Functional Basis of Ocular Motility Disorders, ed. Lennerstrand, G., Zee, D.S. & Keller, E.L., pp. 303–310. Oxford: Pergamon Press.Google Scholar
Karten, H.J. (1979). Visual lemniscal pathways in birds. In Neural Mechanisms of Behavior in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 409–430. New York: Plenum Press.Google Scholar
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia), 185 pp. Baltimore: Johns Hopkins Press.Google Scholar
Karten, H.J., Hodos, W., Nauta, W.J.H. & Revzin, A.M. (1973). Neuronal connections of the “visual Wulst” of the avian telencephalon. Experimental studies in the pigeon (Columbia livia) and owl (Speotyto cunicularia). Journal of Comparative Neurology 150, 253–276.Google Scholar
Leresche, N., Hardy, O. & Jassik-Gerschenfeld, D. (1982). Influence des aires telencephaliques (Wulst) sur la selective directionnelle des cellules tectales chez le Pigeon. Comptes Rendus Academie Sciences Paris 294, 833–836.Google Scholar
Leresche, N., Hardy, O. & Jassik-Gerschenfeld, D. (1983). Receptive-field properties of single cells in the pigeon's optic tectum during cooling of the “visual Wulst.” Brain Research 267, 225–236.Google Scholar
Marcotte, R.R. & Updyke, B.V. (1982). Cortical visual areas of the cat project differentially onto the nuclei of the accessory optic system. Brain Research 242, 205–217.Google Scholar
McKenna, O.C. & Wallman, J. (1985). Accessory optic system and pretectum of birds: comparison with those of other vertebrates. Brain Behavior and Evolution 26, 91–116.CrossRefGoogle ScholarPubMed
Miceli, D., Gioanni, H., Reperant, J. & Peyrichoux, J. (1979). The avian Wulst, I: An anatomical study of afferent and efferent pathways. II: An electrophysiological study of the functional properties of single neurons. In Neural Mechanisms of Behavior in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 223–254. New York: Plenum Press.Google Scholar
Miceli, D., Reperant, J., Villalobos, J. & Dionne, L. (1987). Extratelencephalic projections of the avian visual Wulst. A quantitative autoradiographic study in the pigeon (Columbia livia). Journal fur Hirnforschung 28, 45–57.Google Scholar
Morgan, B. & Frost, B.J. (1981). Visual response characteristics of neurons in nucleus of basal optic root of pigeons. Experimental Brain Research 42, 181–188.Google Scholar
Natal, C.L. & Britto, L.R.G. (1987). The pretectal nucleus of the optic tract modulates the direction selectivity of accessory optic neurons in rats. Brain Research 419, 320–323.Google Scholar
Natal, C.L. & Britto, L.R.G. (1988). The rat accessory optic system: effects of cortical lesions on the directional selectivity of units within the medial terminal nucleus. Neuroscience Letters 91, 154–159.CrossRefGoogle ScholarPubMed
Oyster, C.W. & Barlow, H.B. (1967). Direction-selective units in rabbit retina: distribution of preferred directions. Science 155, 841–842.Google Scholar
Oyster, C.W., Takahashi, E. & Collewijn, H. (1972). Direction- selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Research 12, 183–193.CrossRefGoogle ScholarPubMed
Reiner, A. & Karten, H.J. (1983). The laminar source of efferent projections from the avian Wulst. Brain Research 275, 349–354.Google Scholar
Rio, J.P. (1979). The nucleus of the basal optic root in the pigeon: an electron-microscope study. Archives d'Anatomie Microscopique et de Morphologie Experimentale 68, 17–27.Google ScholarPubMed
Rio, J.P., Villalobos, J., Miceli, D. & Reperant, J. (1983). Efferent projections of the visual Wulst upon the nucleus of the basal optic root in the pigeon. Brain Research 271, 145–151.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.Google Scholar
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988). The pretectal nuclear complex and the accessory optic system. In Neuroanatomy of the Oculomotor System, ed. Buettner-Ennever, J.A., pp. 335–364. Amsterdam: Elsevier Science Publishers.Google Scholar
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, 2055–2072.CrossRefGoogle ScholarPubMed
Soodak, R.E. & Simpson, J.I. (1988). The accessory optic system of rabbit, I: Basic visual response properties. Journal of Neurophysiology 60, 2037–2054.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.Google Scholar
Weber, J.T. (1985). Pretectal complex and accessory optic system of primates. Brain Behavior and Evolution 26, 117–140.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, 215–226.Google Scholar
Zee, D.S., Tusa, R.J., Butler, P.H., Herdman, S.J. & Gucer, G. (1986). The acute and chronic effects of bilateral occipital lobectomies on eye movements in the monkey. In Adaptative Processes in Visual and Oculomotor Systems, ed. Keller, E.L. & Zee, D.S., pp. 267–274. Oxford: Pergamon Press.Google Scholar