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Tectal neurons that participate in centrifugal control of the quail retina: A morphological study by means of retrograde labeling with biocytin

Published online by Cambridge University Press:  02 June 2009

Hiroyuki Uchiyama ,
Naoyuki Yamamoto  and
Hironobu Ito
Hiroyuki Uchiyama
Affiliation:
Department of Information and Computer Science, Faculty of Engineering, Kagoshima University, Kagoshima 890, Japan Intelligence and Synthesis, PRESTO, Research Development Corporation of Japan, Japan
Naoyuki Yamamoto
Affiliation:
Department of Anatomy, Nippon Medical School, Tokyo 113, Japan
Hironobu Ito
Affiliation:
Department of Anatomy, Nippon Medical School, Tokyo 113, Japan Department of Fisheries and Ocean Sciences, University of Alaska, Fairbanks, Alaska
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Abstract

An avian retinopetal nucleus, the isthmo-optic nucleus (ION), is known to receive predominant inputs from the ipsilateral optic tectum. We injected biocytin into the ION in the Japanese quail, and retrogradely labeled tectal neurons projecting to the isthmo-optic (IO) neurons, or the tecto-IO neurons, with an extraordinary Golgi-like quality. Somata of the tecto-IO neurons were located in layer 9 of the tectum. The tecto-IO neurons did not have apical dendrites extending into superficial retino-recipient layers (layers 2–7), but had descending dendrites ramified in layers 9–12. They also possessed short ascending dendrites ramifying in the upper half of layer 9. This dendritic morphology suggests that main input to the tecto-IO neurons may not be of retinal origin. The tecto-IO neurons were spatially arranged in a regular pattern. Distances between neighboring tecto-IO neurons were 50–100 μm. The dendrites of each tecto-IO neuron were not widely dispersed in the horizontal plane, and were confined in a vertically oriented column of 100–200 μm diameter. They possessed axon collaterals extending horizontally in layers 12 and 13. The estimated total number of the tecto-IO neurons was approximately 7000–10,000, which is almost identical to the total cell number of the IO neurons. To label a small number of the tecto-IO terminals, biocytin was injected into a confined area of the optic tectum. The tecto-IO fibers densely arborized in a restricted space of the ION, which is comparable to the dimension of dendritic arborization of individual IO neurons. It is suggested that single tecto-IO neurons may make contact with single IO neurons. IO neurons are known to make synaptic contact with single target cells (association cells of Cajal) in the retina (Uchiyama & Ito, 1993; Uchiyama et al., 1995). The arborization pattern of the tecto-IO neurons' dendrites indicates that the tecto-IO neurons receive very local information in sensory and sensorimotor coordinate space. The morphology of the tecto-IO terminals suggests that the spatially confined information that drives the tecto-IO neurons is sent in parallel to single IO neurons, and then further to single retinal association cells of Cajal. Cellular-level restricted projection patterns of the tecto-isthmo-retinal system may reflect its function for centrifugal control of retinal function.

Keywords

TectumRetinaIsthmo-optic nucleusBirdBiocytin
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 1119 - 1127
Copyright
Copyright © Cambridge University Press 1996

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References

Angaut, P. & Reperant, J. (1978). A light and electron microscopic study of the nucleus isthmo-opticus in the pigeon. Archives d'anatomie microscopique et de morphologie expérimentale 67, 63–78.Google ScholarPubMed
Bagnoli, P., Francesconi, W. & Magni, F. (1982). Visual wulst-optic tectum relationships in birds: A comparison with the mammalian corticotectal system. Archives Italiennes de Biologie 120, 212–235.Google ScholarPubMed
Brecha, N. (1978). Some observations on the organization of the avian optic tectum: Afferent nuclei and their tectal projections. Ph.D. Thesis, SUNY at Stony Brook, New York.Google Scholar
Bugbee, N.M. (1979). The basal ganglia-tectal pathway: Its role in visually-guided behavior in the pigeon (Columba livia). Ph.D. Thesis, University of Maryland, Maryland.Google Scholar
Cowan, W.M. (1970). Centrifugal fibres to the avian retina. British Medical Bulletin 26, 112–118.CrossRefGoogle Scholar
Cowan, W.M., Adamson, L. & Powell, T.P.S. (1961). An experimental study of the avian visual system. Journal of Anatomy 95, 545–563.Google ScholarPubMed
Cowan, W.M. & Powell, T.P.S. (1963). Centrifugal fibres in the avian visual system. Proceedings of the Royal Society B 158, 232–252.Google ScholarPubMed
Crossland, W.J. (1979). Identification of tectal synaptic terminals in the avian isthmo-optic nucleus. In Neural Mechanisms and Behavior in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 267–285. New York: Plenum Press.Google Scholar
Crossland, W.J. & Hughes, C.P. (1978). Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Research 145, 239–256.CrossRefGoogle ScholarPubMed
Fritzsch, B., Crapon, d.C.M.D. & Clarke, P.G. (1990). Development of two morphological types of retinopetal fibers in chick embryos, as shown by the diffusion along axons of a carbocyanine dye in the fixed retina. Journal of Comparative Neurology 300, 405–421.CrossRefGoogle ScholarPubMed
Gamlin, P.D. & Cohen, D.H. (1988). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 18–46.CrossRefGoogle ScholarPubMed
Güntürkün, O. (1987). A Golgi study of the isthmic nuclei in the pigeon (Columba livia). Cell and Tissue Research 248, 439–448.CrossRefGoogle ScholarPubMed
Holden, A.L. (1968). The centrifugal system running to the pigeon retina. Journal of Physiology 197, 199–219.CrossRefGoogle Scholar
Holden, A.L. & Powell, T.P.S. (1972). The functional organization of the isthmo-optic nucleus in the pigeon. Journal of Physiology (London) 223, 419–447.CrossRefGoogle ScholarPubMed
Hunt, S.P. & Brecha, N. (1984). The avian optic tectum: A synthesis of morphology and biochemistry. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 619–648. New York: Plenum.CrossRefGoogle Scholar
Ikushima, M., Watanabe, M. & Ito, H. (1986). Distribution and morphology of retinal ganglion cells in the Japanese quail. Brain Research 376, 320–334.CrossRefGoogle ScholarPubMed
Karten, H.J. & Dubbeldam, J.L. (1973). The organization and projections of the paleostriatal complex in the pigeon (Columba livia). Journal of Comparative Neurology 148, 61–90.CrossRefGoogle ScholarPubMed
Karten, H.J., Hodos, W., Nauta, W.J.H. & Revzin, A.M. (1973). Neural connections of the “visual Wulst” of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). Journal of Comparative Neurology 150, 253–278.CrossRefGoogle ScholarPubMed
Knudsen, E.I., Cohen, Y.E. & Masino, T. (1995). Characterization of a forebrain gaze field in the archistriatum of the barn owl: Microstimulation and anatomical connections. Journal of Neuroscience 15, 5139–5151.CrossRefGoogle ScholarPubMed
Marin, G., Bodnarenko, S., McKenna, O. & Wallman, J. (1988). Neurons projecting to the retina: Afferents and possible functions. Society for Neuroscience Abstracts 14, 992.Google Scholar
Marin, G., Letelier, J.C. & Wallman, J. (1990). Saccade-related responses of centrifugal neurons projecting to the chicken retina. Experimental Brain Research 82, 263–270.CrossRefGoogle Scholar
McGill, J.I., Powell, T.P.S. & Cowan, W.M. (1966 a). The retinal representation upon the optic tectum and isthmo-optic nucleus in the pigeon. Journal of Anatomy 100, 5–33.Google ScholarPubMed
McGill, J.I., Powell, T.P.S. & Cowan, W.M. (1966 b). The organization of the projection of the centrifugal fibres to the retina in the pigeon. Journal of Anatomy 100, 35–49.Google Scholar
Miceli, D., Reperant, J., Rio, J.P. & Medina, M. (1995). GABA immunoreactivity in the nucleus isthmo-opticus of the centrifugal visual system in the pigeon: A light and electron microscopic study. Visual Neuroscience 12, 425–441.CrossRefGoogle Scholar
Miles, F.A. (1972 a). Centrifugal control of the avian retina. II. Receptive field properties of cells in the isthmo-optic nucleus. Brain Research 48, 93–113.CrossRefGoogle ScholarPubMed
Miles, F.A. (1972 b). Centrifugal control of the avian retina. III. Effects of electrical stimulation of the isthmo-optic tract on the receptive field properties of retinal ganglion cells. Brain Research 48, 115–129.CrossRefGoogle Scholar
Reiner, A., Brauth, S.E. & Karten, H.J. (1984). Evolution of the amniote basal ganglia. Trends in Neuroscience 7, 320–325.CrossRefGoogle Scholar
Reiner, A., Brecha, N.C. & Karten, H.J. (1982 a). Basal ganglia pathways to the tectum: The afferent and efferent connections of the lateral spiriform nucleus of pigeon. Journal of Comparative Neurology 208, 16–36.CrossRefGoogle Scholar
Reiner, A., Karten, H.J. & Brecha, N.C. (1982 b). Enkephalinmediated basal ganglia influences over the optic tectum: Immunohistochemistry of the tectum and the lateral spiriform nucleus in pigeon. Journal of Comparative Neurology 208, 37–53.CrossRefGoogle ScholarPubMed
Ritchie, T.L.C. (1979). Intratelencephalic visual connections and their relationship to the archistriatum in the pigeon (Columba livia). Ph.D. Thesis, University of Virginia, Charlottesville, VA.Google Scholar
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Uchiyama, H. & Barlow, R.B. (1994). Centrifugal inputs enhance responses of retinal ganglion cells in the Japanese quail without changing their spatial coding properties. Vision Research 34, 2189–2194.CrossRefGoogle ScholarPubMed
Uchiyama, H. & Ito, H. (1993). Target cells for the isthmo-optic fibers in the retina of the Japanese quail. Neuroscience Letters 154, 35–38.CrossRefGoogle ScholarPubMed
Uchiyama, H., Ito, H. & Tauchi, M. (1995). Retinal neurones specific for centrifugal modulation of vision. Neuroreport 6, 889–892.CrossRefGoogle ScholarPubMed
Uchiyama, H., Matsutani, S. & Watanabe, M. (1987). Activation of the isthmo-optic neurons by the visual Wulst stimulation. Brain Research 406, 322–325.CrossRefGoogle ScholarPubMed
Uchiyama, H. & Watanabe, M. (1985). Tectal neurons projecting to the isthmo-optic nucleus in the Japanese quail. Neuroscience Letters 58, 381–385.CrossRefGoogle Scholar
Wallenberg, A. (1898). Das mediale opticusbündel der Taube. Neurologisches Zentralblatt 17, 532–537.Google Scholar
Woodson, W., Reiner, A., Anderson, K. & Karten, H.J. (1991). Distribution, laminar location, and morphology of tectal neurons projecting to the isthmo-optic nucleus and the nucleus isthmi, pars parvocellularis in the pigeon (Columba livia) and chick (Gallus domesticus): A retrograde labelling study. Journal of Comparative Neurology 305, 470–488.CrossRefGoogle Scholar
Woodson, W., Shimizu, T., Wild, J.M., Schimke, J., Cox, K. & Karten, H.J. (1995). Centrifugal projections upon the retina—an anterograde tracing study in the pigeon (Columbia livia). Journal of Comparative Neurology 362, 489–509.CrossRefGoogle Scholar
Zeier, H. & Karten, H.J. (1971). The archistriatum of the pigeon: Organization of afferent and efferent connections. Brain Research 31, 313–326.CrossRefGoogle ScholarPubMed