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Cholera toxin mapping of retinal projections in pigeons (Columba livia), with emphasis on retinohypothalamic connections

Published online by Cambridge University Press:  02 June 2009

Toru Shimizu ,
Kevin Cox ,
Harvey J. Karten  and
Luiz R. G. Britto
Toru Shimizu
Affiliation:
Departments of Psychology and Surgery, University of South Florida, Tampa
Kevin Cox
Affiliation:
Department of Neurosciences, University of California, San Diego, La Jolla
Harvey J. Karten
Affiliation:
Department of Neurosciences, University of California, San Diego, La Jolla
Luiz R. G. Britto
Affiliation:
Department of Physiology and Biophysics, Institute for Biomedical Sciences, Sao Paulo State University, 05508 Sao Paulo, Brazil
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Abstract

Anterograde transport of cholera toxin subunit B (CTb) was used to study the retinal projections in birds, with an emphasis on retinohypothalamic connections. Pigeons (Columba livia) were deeply anesthetized and received unilateral intraocular injections of CTb. In addition to known contralateral retinorecipient regions, CTb-immunoreactive fibers and presumptive terminals were found in several ipsilateral regions, such as the nucleus of the basal optic root, ventral lateral geniculate nucleus, intergeniculate leaflet, nucleus lateralis anterior, area pretectalis, and nucleus pretectalis diffusus. In the hypothalamus, CTb-immunoreactive fibers were observed in at least two contralateral cell groups, a medial hypothalamic retinorecipient nucleus, and a lateral hypothalamic retinorecipient nucleus. To compare retinorecipient hypothalamic nuclei in pigeons with the mammalian suprachiasmatic nucleus, double-label experiments were conducted to study the existence of neurophysin-like immunoreactivity in the retinorecipient avian hypothalamus. The results showed that only cell bodies in the medial hypothalamic nucleus contained neurophysin-like immunoreactivity. The results demonstrate CTb to be a sensitive anterograde tracer and provide further anatomical information on the avian equivalent of the mammalian suprachiasmatic nucleus.

Keywords

Suprachiasmatic nucleusNeurophysinRetinal inputCholera toxinBirds
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 3 , May 1994 , pp. 441 - 446
Copyright
Copyright © Cambridge University Press 1994

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References

Britto, L.R.G., Keyser, K., Hamassaki, D.E., Shimizu, T. & Karten, H.J. (1989). Chemically specific retinal ganglion cells collateralize to the pars ventralis of the lateral geniculate nucleus and optic tectum in the pigeon (Columba livia). Visual Neuroscience 3, 477–482.CrossRefGoogle Scholar
Card, J.P. & Moore, R.Y. (1984). The suprachiasmatic nucleus of the golden hamster: Immunohistochemical analysis of cell and fiber distribution. Neuroscience 13, 415–431.CrossRefGoogle ScholarPubMed
Cassone, V.M. (1988). Circadian variation of [14C]2–deoxyglucose uptake within the suprachiasmatic nucleus of the house sparrow, Passer domesticus. Brain Research 459, 178–182.CrossRefGoogle ScholarPubMed
Cassone, V.M. & Moore, R.Y. (1987). Retinohypothalamic projection and suprachiasmatic nucleus of the house sparrow, Passer domesticus. Journal of Comparative Neurology 266, 171–182.CrossRefGoogle ScholarPubMed
Cooper, M.L., Pickard, G.E. & Silver, R. (1983). Retinohypothalamic pathway in the dove demonstrated by anterograde HRP. Brain Research Bulletin 10, 715–718.CrossRefGoogle ScholarPubMed
Ebihara, S. & Kawamura, H. (1981). The role of the pineal organ and the suprachiasmatic nucleus in the control of circadian locomotor rhythms in the Java sparrow, Padda oryzivora. Journal of Comparative Physiology 141, 207–214.CrossRefGoogle Scholar
Ehrlich, D. & Mark, R. (1984). An atlas of the primary visual projections in the brain of the chick Gallus gallus. Journal of Comparative Neurology 223, 592–610.CrossRefGoogle ScholarPubMed
Ericson, H. & Blomqvist, A. (1988). Tracing of neuronal connections with cholera toxin subunit B: Light and electron microscopic immu-nohistochemistry using monoclonal antibodies. Journal of Neuroscience Methods 24, 225–235.CrossRefGoogle Scholar
Gamlin, P.D.R., Reiner, A. & Karten, H.J. (1982). Substance P-containing neurons of the avian suprachiasmatic nucleus project directly to the nucleus of Edinger-Westphal. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3891–3895.CrossRefGoogle Scholar
Guiloff, G.D. (1991). Ultrastructural study of the avian ventral lateral geniculate nucleus. Visual Neuroscience 6, 119–134.CrossRefGoogle ScholarPubMed
Güntürkün, O. & Karten, H.J. (1991). An immunocytochemical analysis of the lateral geniculate complex in the pigeon (Columba livia). Journal of Comparative Neurology 314, 721–749.CrossRefGoogle ScholarPubMed
Hartwig, H.G. (1974). Electron microscopic evidence for a retinohypothalamic projection to the suprachiasmatic nucleus of Passer domesticus. Cell and Tissue Research 153, 89–99.CrossRefGoogle Scholar
Iñiguez, C, Gayoso, M.J. & Carreres, J. (1985). A versatile and simple method for staining nervous tissue using Giemsa dye. Journal of Neuroscience Methods 13, 77–86.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
Luppi, P.H., Saki, K., Salvert, D., Fort, P. & Jouvet, M. (1987). Peptidergic hypothalamic afferents to the cat nucleus raphe palli-dus as revealed by a double immunostaining technique using unconjugated cholera toxin as a retrograde tracer. Brain Research 402, 339–345.CrossRefGoogle Scholar
Mikami, S., Kawamura, K., Oksche, A. & Farner, D.S. (1976). The fine structure of the hypothalamic secretory neurons of the white-crowned sparrow, Zonotrichia leucophyrs gambelii. II. Magnocel-lular and parvocellular nuclei of the rostral hypothalamus. Cell and Tissue Research 165, 415–434.CrossRefGoogle Scholar
Moore, R.Y. (1983). Organization and function of a central nervous system circadian oscillator: The suprachiasmatic hypothalamic nucleus. Federation Proceedings 42, 2783–2789.Google ScholarPubMed
Norgren, R.B. Jr & Silver, R. (1989). Retinohypothalamic projections and the suprachiasmatic nucleus in birds. Brain, Behavior, and Evolution 34, 73–83.CrossRefGoogle ScholarPubMed
Norgren, R.B. Jr & Silver, R. (1990). Distribution of vasoactive intestinal peptide-like and neurophysin-like immunoreactive neurons and acetylcholinesterase staining in the ring dove hypothalamus with emphasis on the question of an avian suprachiasmatic nucleus. Cell and Tissue Research 259, 331–339.CrossRefGoogle ScholarPubMed
Oliver, J., Bouillé, C, Herbuté, S. & Baylé, J.D. (1978). Retrograde transport from the preoptic-anterior hypothalamic region to retinal ganglion cells in quail. Neuroscience Letters 9, 291–295.CrossRefGoogle ScholarPubMed
Panzica, G.C. (1985). Vasotocin-immunoreactive elements and neuronal typology in the suprachiasmatic nucleus of the chicken and Japanese quail. Cell and Tissue Research 242, 371–376.CrossRefGoogle ScholarPubMed
Pateromichelakis, S. (1979). Response properties of units in the lateral geniculate nucleus of the domestic chick (Gallus domesticus). Brain Research 167, 281–296.CrossRefGoogle ScholarPubMed
Remy, M. & Güntürkün, O. (1991). Retinal afferents to the optic tectum and the n. opticus principalis thalami in the pigeon. Journal of Comparative Neurology 305, 57–70.CrossRefGoogle Scholar
Rusak, B. & Zucker, I. (1979). Neural regulation of circadian rhythms. Physiological Reviews 59, 449–526.CrossRefGoogle ScholarPubMed
Shimizu, I., Yoshimoto, M., Kojima, T. & Okado, N. (1984). Development of retinohypothalamic projections in the chick embryo. Neuroscience Letters 50, 43–47.CrossRefGoogle ScholarPubMed
Shimizu, T. & Karten, H.J. (1990). Immunohistochemical analysis of the visual wulst of the pigeon (Columba livia). Journal of Comparative Neurology 300, 346–369.CrossRefGoogle ScholarPubMed
Shimizu, T., Britto, L.R.G., Karten, H.J. & Cox, K. (1991). Cholera toxin mapping of retinal projections in birds. Society for Neuroscience Abstracts 17, 651.Google Scholar
Simpson, S.M. & Follett, B.K. (1981). Pineal and hypothalamic pacemakers: Their role in regulating circadian rhythmicity in Japanese quail. Journal of Comparative Physiology 144, 381–389.CrossRefGoogle Scholar
Sofroniew, M.W. & Weindl, A. (1980). Identification of parvocellular vasopressin and neurophysin neurons in the suprachiasmatic nucleus of a variety of mammals including primates. Journal of Comparative Neurology 193, 659–675.CrossRefGoogle ScholarPubMed
Takahashi, J.S. & Menaker, M. (1979). Physiology of avian circadian pacemakers. Federation Proceedings 38, 2583–2588.Google ScholarPubMed
Takahashi, J.S. & Menaker, M. (1982). Role of the suprachiasmatic nuclei in the circadian system of the house sparrow, Passer domesticus. Journal of Neuroscience 2, 815–828.CrossRefGoogle ScholarPubMed
Vandesande, F., Dierickx, K. & DeMey, J. (1975). Identification of the vasopressin-neurophysin producing neurons of the rat suprachiasmatic nucleus. Cell and Tissue Research 156, 377–380.CrossRefGoogle Scholar
van Tienhoven, A. & Planck, R.J. (1973). The effect of light on avian reproductive activity. In Handbook of Physiology. Endocrinology II, Part I., ed. Greep, R., Astwood, E. & Geiger, S., pp. 79–107. Washington, D.C.: American Physiological Society.Google Scholar
Watts, A.G. & Swanson, L.W. (1987). Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. Journal of Comparative Neurology 258, 230–252.CrossRefGoogle ScholarPubMed
Wallman, J., Teakle, E. & Silver, R. (1991). The putative suprachiasmatic nucleus of birds responds to visual motion. Society for Neuroscience Abstracts 17, 24.Google Scholar
Yamauchi, K. & Yasuda, M. (1985). Cyto-, dendro- and fibro-architectonic studies on the chicken hypothalamus. Journals für Hirnforschung 26, 509–519.Google ScholarPubMed