Hostname: page-component-77c89778f8-sh8wx Total loading time: 0 Render date: 2024-07-19T07:59:32.385Z Has data issue: false hasContentIssue false
  • English
  • Français

Brain-stem afferents upon retinal projecting isthmo-optic and ectopic neurons of the pigeon centrifugal visual system demonstrated by retrograde transneuronal transport of rhodamine β-isothiocyanate

Published online by Cambridge University Press:  02 June 2009

Dom Miceli ,
Jacques Repérant ,
Renuka Bavikati ,
Jean-Paul Rio  and
Michel Volle
Dom Miceli
Affiliation:
Laboratoire de Neuropsychologic Expérimentale et Comparéd, Université du Québec, Trois-Rivières, Canada
Jacques Repérant
Affiliation:
Laboratoire de Neuropsychologic Expérimentale et Comparéd, Université du Québec, Trois-Rivières, Canada INSERM U-106, Hôpital de la Salpétrière, Paris, France
Renuka Bavikati
Affiliation:
Laboratoire de Neuropsychologic Expérimentale et Comparéd, Université du Québec, Trois-Rivières, Canada
Jean-Paul Rio
Affiliation:
INSERM U-106, Hôpital de la Salpétrière, Paris, France
Michel Volle
Affiliation:
Laboratoire de Neuropsychologic Expérimentale et Comparéd, Université du Québec, Trois-Rivières, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Brain-stem afferents to the n. isthmo-opticus (NIO) and ectopic neurons (EN) of the centrifugal visual system (CVS) were determined in the pigeon using the retrograde transneuronal transport of the fluorescent dye Rhodamine β-isothiocyanate (RITC) after its intraocular injection. In other experiments, either RITC was injected into various periocular tissues (controls) or the retrograde tracer Fluoro-gold (FG) was injected stereotaxically in the NIO. Following intraocular injections, the RITC retrograde labeling of cell bodies was observed contralaterally in the NIO and EN and transneuronally in layers 9/10 of the optic tectum, area ventralis-Tsai, zona peri-NIII, mesencephalic and pontine reticular formation (PRF), n. linearis caudalis-raphe, and bilaterally within a region referred to as zona peri-n.NVI (Zp-n.NVI) immediately underlying the abducens nerve nucleus. None of the above structures were labeled after RITC periocular injections. The FG labeling revealed that the tectal efferent neurons were mainly medium-sized, multipolar cells whose dendrites extended superficially to retino-recipient tectal layers 6 and 5. Quantitative measurements of the distribution of layers 9/10 RITC-labeled neurons indicated the highest densities to be localized within the ventral tectum corresponding to the representation of the dorsal retina and inferior visual field. We suggest that visual and nonvisual brain-stem afferents upon NIO and EN may play a role in the proposed mechanism of the avian CVS in attention, ground-feeding behavior, and modulation of retinal sensitivity.

Keywords

Centrifugal visual systemBrain-stem afferentsRhodamine β-isothiocyanateTransneuronal tracingPigeon
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 213 - 224
Copyright
Copyright © Cambridge University Press 1997

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

REFERENCES

Angaut, P. & Repérant, 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. & Burkhalter, A. (1983). Organization of the afferent projections to the wulst in the pigeon. Journal of Comparative Neurology 214, 103–113.CrossRefGoogle Scholar
Bagnoli, P., Grassi, S. & Magni, F. (1980). A direct connection between visual wulst and tectum opticum in the pigeon (Columba livia) demonstrated by horseradish peroxidase. Archives Italiennes de Biologie 118, 72–88.Google ScholarPubMed
Britto, L.R.G., Keyser, K.T., Lindstrom, J.M. & Karten, H.J. (1992). Immunohistochemical localization of nicotinic acetylcholine receptor subunits in the mesencephalon and diencephalon of the chick (Gallus gallus). Journal of Comparative Neurology 317, 325–340.CrossRefGoogle ScholarPubMed
Casini, G., Bingman, V.P. & Bagnoli, P. (1986). Connections of the pigeon dorsomedial forebrain studied with WGA-HRP and 3H-proline. Journal of Comparative Neurology 245, 454–470.CrossRefGoogle ScholarPubMed
Challet, E., Miceli, D., Pierre, J., Repérant, J., Masicotte, G., Herbin, M. & Vesselkin, N.P. (1996). Distribution of serotonin-immunoreactivity in the brain of the pigeon (Columba livia). Anatomy and Embryology 193, 209–227.CrossRefGoogle ScholarPubMed
Clarke, P.G.H. & Caranzano, F. (1985). Dendritic development in the isthmo-optic nucleus of chick embryos. Developmental Neuroscience 7, 161–169.CrossRefGoogle ScholarPubMed
Clarke, P.G.H. & Whitteridge, D. (1976). The projection of the retina, including the “red area,” on to the optic tectum of the pigeon. Quarterly Journal of Experimental Physiology 61, 351–358.Google Scholar
Cohen, D.H. & Pitts, L.H. (1967). The hyperstriatal region of the avian forebrain: Somatic and autonomic responses to electrical stimulation. Journal of Comparative Neurology 131, 323–336.CrossRefGoogle Scholar
Cowan, W.M. (1970). Centrifugal fibers 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 158, 232–252.Google ScholarPubMed
Crossland, W.J. (1979). Identification of tectal synaptic terminals in the avian isthmooptic nucleus. In Neural Mechanisms of Behavior in the Pigeon, ed. Granda, A.M. & Maxwell, J.H., pp. 267–286. 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
Dado, R.J., Burstein, R., Cliffer, K.D. & Giesler, G.J. Jr (1990). Evidence that Fluoro-Gold can be transported avidly through fibers of passage. Brain Research 533, 329–333.CrossRefGoogle ScholarPubMed
Dubé, L. & Parent, A. (1981). The monoamine-containing neurons in avian brain: I. A study of the brain stem of the chicken (Gallus domesticus) by means of fluorescence and acetylcholinesterase histochemistry. Journal of Comparative Neurology 196, 695–708.CrossRefGoogle Scholar
Evinger, C (1988). Extraocular motor nuclei: Location, morphology and afferents. Neuroanatomy of the Oculomotor System 3, 81–117.Google Scholar
Fritzsch, B., Crapon de, Caprona M.-D. & Clarke, P.G.H. (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
Fuxe, K. & Ljunggren, L. (1965). Cellular localization of monoamines in the upper brain stem of the pigeon. Journal of Comparative Neurology 125, 355–382.CrossRefGoogle ScholarPubMed
Galifret, Y., Condé-Courtine, F., Repérant, J. & Serviere, J. (1971). Centrifugal control in the visual system of the pigeon. Vision Research (Suppl.) 3, 185–200.CrossRefGoogle Scholar
Guglielmone, R. & Panzica, G.C. (1984). Typology, distribution and development of the catecholamine-containing neurons in the chicken brain. Cell and Tissue Research 237, 67–79.CrossRefGoogle ScholarPubMed
Güntürkün, O., Miceli, D. & Watanabe, M. (1993). Anatomy of the avian thalamofugal pathway. In Vision, Brain, and Behavior in Birds, ed. Zeigler, H.P. & Bischof, H.J., pp. 115–135. Cambridge: The MIT Press.Google Scholar
Güntürkün, O. & Remy, M. (1990). The topographical projection of the nucleus isthmi pars parvocellularis (Ipc) onto the tectum opticum in the pigeon. Neuroscience Letters 111, 18–22.Google 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
Hahmann, U. & Güntürkün, O. (1992). Visual-discrimination deficits after lesions of the centrifugal visual system in pigeons (Columba livia). Visual Neuroscience 9, 225–233.CrossRefGoogle ScholarPubMed
Hayes, B.P. & Holden, A.L. (1983). The distribution of centrifugal terminals in the pigeon retina. Experimental Brain Research 49, 189–197.Google ScholarPubMed
Hayes, B.P. & Webster, K.E. (1981). Neurons situated outside the isthmooptic nucleus and projecting to the eye in adult birds. Neuroscience Letters 26, 107–112.CrossRefGoogle Scholar
Holden, A.L. (1990). Centrifugal pathways to the retina: Which way does the "searchlight" point. Visual Neuroscience 4, 493–495.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
Hoogland, P.V., Vanderkrans, A., Koole, F.D. & Groenewegen, H.J. (1985). A direct projection from the nucleus oculomotorius to the retina in rats. Neuroscience Letters 56, 323–328.CrossRefGoogle Scholar
Huber, G.C. & Crosby, E.C. (1929). The nuclei and fiber paths of the avian diencephalon, with consideration of the telencephalic and certain mesencephalic centers and connections. Journal of Comparative Neurology 48, 1–225.CrossRefGoogle Scholar
Ikeda, H. & Gotoh, J. (1971). Distribution of monoamine-containing cells in the central nervous system of the chicken. Japanese Journal of Pharmacology 21, 763–784.CrossRefGoogle ScholarPubMed
Itaya, S.K. (1980). Retinal efferents from the pretectal area in the rat. Brain Research 201, 436–441.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
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
Kitt, C.A. & Brauth, S.E. (1980). Telencephalic projections from catecholamine cell groups in the pigeon. Society for Neuroscience Abstracts 6, 630.Google Scholar
Labandeira-Garcia, J.L. (1988). The retinopetal system in the rat. Neuroscience Research 6, 88–95.CrossRefGoogle ScholarPubMed
Lewis, J.W., Ryan, S.M., Arnold, A.P. & Butcher, L.L. (1981). Evidence for a catecholaminergic projection to area X in the zebra finch. Journal of Comparative Neurology 196, 347–354.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
Masino, T. & Knudsen, E.I. (1992). Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the barn owl. Experimental Brain Research 92, 194–208.CrossRefGoogle Scholar
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers of the pigeon retina. Science 150, 359–362.CrossRefGoogle ScholarPubMed
McGill, J.I., Powell, T.P.S. & Cowan, W.M. (1966 a). The retinal representation upon the optic tectum and the 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
Medina, L. & Reiner, A. (1994). Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. Journal of Comparative Neurology 342, 497–537.CrossRefGoogle ScholarPubMed
Meyer, C.C., Parker, D.M. & Salsen, E.A. (1976). Androgen-sensitive midbrain sites and visual attention in chicks. Nature 259, 689–690.CrossRefGoogle ScholarPubMed
Miceli, D., Gioanni, H., Repérant, J. & Peyrichoux, J. (1979). The avian visual 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. 223–244. New York: Plenum Publishing Corporation.Google Scholar
Miceli, D., Marchand, L., Repérant, J. & Rio, J.-P. (1990). Projections of the dorsolateral anterior complex and adjacent thalamic nuclei upon the visual Wulst in the pigeon. Brain Research 518, 317–323.CrossRefGoogle ScholarPubMed
Miceli, D. & Repérant, J. (1983). Hyperstriatal-tectal projections in the pigeon (Columba livia) as demonstrated by the retrograde double-label fluorescence technique. Brain Research 276, 147–153.CrossRefGoogle ScholarPubMed
Miceli, D. & Repérant, J. (1985). Telencephalic afferent projections from the diencephalon and brainstem in the pigeon. A retrograde multiple-label fluorescent study. Experimental Biology 44, 71–99.Google Scholar
Miceli, D., Repérant, J., Marchand, L. & Rio, J.-P. (1993). Retrograde transneuronal transport of the fluorescent dye Rhodamine β-isothio-cyanate from the primary and centrifugal visual system in the pigeon. Brain Research 601, 289–298.CrossRefGoogle ScholarPubMed
Miceli, D., Repérant, 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
Miceli, D., Repérant, J., Villalobos, J. & Weidner, C. (1987). Extra-telencephalic projections of the visual Wulst. A quantitative autoradiographic study in the pigeon. Journal of Brain Research and Neurobiology 28, 45–59.Google Scholar
Miles, F.A. (1972). 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
Nickla, D.L., Gottlieb, M.D., Marin, G., Rojas, X., Britto, L.R.G. & Wallman, J. (1994). The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system. Visual Neuroscience 11, 401–409.CrossRefGoogle Scholar
Pearlman, A.L. & Hughes, C.P. (1976). Functional role of efferents to the avian retina. II. Effects of reversible cooling of the isthmo-optic nucleus. Journal of Comparative Neurology 166, 123–132.CrossRefGoogle Scholar
Reiner, A., Karle, E.J., Anderson, K.D. & Medina, L. (1994). Catecholaminergic perikarya and fibers in the avian nervous system. In Phytogeny and Development of Catecholamine Systems in the CNS of Vertebrates, ed. Smeets, W.J.A.J. & Reiner, A., pp. 135–181. Cambridge: Cambridge University Press.Google Scholar
Reiner, A. & Karten, H.J. (1982). Laminar distribution of the cells of origin of the descending tectofugal pathways in the pigeon (Columba livia). Journal of Comparative Neurology 204, 165–187.CrossRefGoogle ScholarPubMed
Reiner, A. & Karten, H.J. (1983). The laminar source of efferent projections from the avian Wulst. Brain Research 275, 349–354.CrossRefGoogle ScholarPubMed
Repérant, J., Miceli, D., Vesselkin, N.P. & Molotchnikoff, S. (1989). The centrifugal visual system of vertebrates: A century-old search reviewed. International Review of Cytology 118, 115–171.CrossRefGoogle ScholarPubMed
Rogers, L.J. & Miles, F.A. (1972). Centrifugal control of the avian retina. V. Effects of lesions of the isthmo-optic nucleus on visual behaviour. Brain Research 48, 147–156.CrossRefGoogle ScholarPubMed
Shimizu, T. & Karten, H.J. (1993). The avian visual system and the evolution of the neocortex. In Vision, Brain, and Behavior in Birds, ed. Zeigler, H.P. & Bischof, H.J., pp. 103–114. Cambridge: The MIT Press.Google Scholar
Shortess, G.K. & Klose, E.F. (1977). Effects of lesions involving efferent fibers to the retina in pigeons (Columba livia). Physiology Behavior 18, 409–414.CrossRefGoogle Scholar
Sorenson, E.M. & Chiappinelli, V.A. (1992). Localization of 3H-nicotine, 125I-kappa-bungarotoxin, and 125I-alpha-bungarotoxin binding to nicotinic sites in the chicken forebrain and midbrain. Journal of Comparative Neurology 323, 1–12.CrossRefGoogle ScholarPubMed
Tohyama, M., Maeda, T, Hashimoto, J., Shrestha, G.R., Tamura, O. & Shimizu, N. (1974). Comparative anatomy of locus coeruleus. I. Organization and ascending projections of the catecholamine containing neurons in the pontine region of the bird, Melopsittacus undulatus. Journal für Hirnforsch 15, 319–330.Google ScholarPubMed
Trottier, C, Repérant, J. & Miceli, D. (1995). Anatomical evidence of a retino-thalamo-hippocampal pathway in the pigeon. Journal of Brain Research 36, 489–500.Google ScholarPubMed
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
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 neurons 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
Ward, R., Repérant, J. & Miceli, D. (1991). The centrifugal visual system: What can comparative studies tell us about its evolution and possible function? In The Changing Visual System, ed. Bagnoli, P. & Hodos, W. pp. 61–76. New York: Plenum Press.CrossRefGoogle Scholar
Weidner, C., Desroches, A.M., Repérant, J., Kirpitchnikova, E. & Miceli, D. (1989). Comparative study of the centrifugal visual system in the pigmented and glaucomatous albino quail. Biological Structures and Morphology 2, 89–93.Google Scholar
Weidner, C, Miceli, D. & Repérant, J. (1983). Orthograde axonal and transcellular transport of different fluorescent tracers in the primary visual system of the rat. Brain Research 272, 129–136.CrossRefGoogle ScholarPubMed
Weidner, C, Repérant, J., Desroches, A.-M., Miceli, D. & Vesselkin, N.P. (1987). Nuclear origin of the centrifugal visual pathway in birds of prey. Brain Research 436, 153–160.CrossRefGoogle ScholarPubMed
Wolf-Oberhollenzer, F. (1987). A study of the centrifugal projections to the pigeon retina using two fluorescent markers. Neuroscience Letters 73, 16–20.CrossRefGoogle 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 (Columba livia). Journal of Comparative Neurology 362, 489–509.CrossRefGoogle ScholarPubMed
Wynne, B. & Güntürkün, O. (1995). Dopaminergic innervation of the telencephalon of the pigeon (Columba livia): A study with antibodies against tyrosine hydroxylase and dopamine. Journal of Comparative Neurology 357, 446–464.CrossRefGoogle ScholarPubMed
Yamada, H. & Sano, Y. (1985). Immunohistochemical studies on the serotonin neuron system in the brain of the chicken (Gallus domesticus)—II. The distribution of the nerve fibers. Biogenic Amines 2, 21–36.Google Scholar
Yamada, H., Takeuchi, Y. & Sano, Y (1984). Immunohistochemical studies on the serotonin neuron system in the brain of the chicken (Gallus domesticus)—I. The distribution of the neurons somata. Biogenic Amines 1, 83–94.Google Scholar