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GABA immunoreactivity in the nucleus isthmo-opticus of the centrifugal visual system in the pigeon: A light and electron microscopic study

Published online by Cambridge University Press:  02 June 2009

Dom Miceli ,
Jacques Repérant ,
Jean-Paul Rio  and
Monique Medina
Dom Miceli
Affiliation:
Laboratoire de Neuropsychologie Expérimental et Comparée, Université du Québec, Trois-Rivières, Canada
Jacques Repérant
Affiliation:
Laboratoire de Neuropsychologie Expérimental et Comparée, Université du Québec, Trois-Rivières, Canada INSERM U–106, Hoôpital de la Salpétrière, Paris
Jean-Paul Rio
Affiliation:
INSERM U–106, Hoôpital de la Salpétrière, Paris
Monique Medina
Affiliation:
Laboratoire d'Anatomie Comparée, M.N.H.N., Paris, France
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Abstract

The present study examined GABA immunoreactivity within the retinopetal nucleus isthmo-opticus (NIO) of the pigeon centrifugal visual system (CVS) using light- (immunohistofluorescence, peroxidase anti-peroxidase: PAP) and electron- (postembedding GABA immunogold) microscopic techniques. In some double-labeling experiments, the retrograde transport of the fluorescent dye rhodamine β−isothiocyanate (RITC) after its intraocular injection was combined with GABA immunohistofluorescence. GABA-immunoreactive (-ir) somata were demonstrated within the neuropilar zone of the NIO adjacent to the centrifugal cell laminae whereas the centrifugal neurons were always immunonegative. A quantitative ultrastructural analysis was performed which distinguished five categories of axon terminal profiles (P1–5) on the basis of various cytological criteria: type of synaptic contact (symmetrical or asymmetrical); shape, size, and density of synaptic vesicles as well as the immunolabeling (positive or negative), size of profile and appearance of hyaloplasm. Numerous GABA-ir afferents to centrifugal neurons via axon terminal types P2a, P2c, and P3 were observed which comprised 47.1% of the total input. Moreover, the data suggest that some of the P2a terminals, which make up 26.4% of the input, stem from the intrinsic GABA-ir interneurons, whereas the latter receive P1, P3, but also P2 terminal input, indicating that interneurons may contact other interneurons via type P2a axon terminals. The results also suggest that the GABA-ir P3 or the immunonegative P1b and P5 axon terminals are of extrinsic origin arising from cells in the optic tectum whereas the P2c and P4 axon terminals are associated with extra-tectal input to the NIO. The GABAergic innervation of centrifugal neurons within the NIO may be the basis for the demonstrated facilitatory effect of the centrifugal output upon ganglion cell responses. This is relevant to hypotheses regarding CVS involvement in attentional mechanisms through selective enhancement of retinal sensitivity depending on the location of meaningful or novel stimuli.

Keywords

Centrifugal visual systemNucleus isthmo-opticusPigeonGABA immunoreactivityLight and electron microscopy
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 3 , May 1995 , pp. 425 - 441
Copyright
Copyright © Cambridge University Press 1995

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References

Angaut, P. & Repérant, J. (1976). Fine structure of the optic fibre termination layers in the pigeon optic tectum: A Golgi and electron microscope study. Neuroscience 1, 93–105.CrossRefGoogle ScholarPubMed
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 expérimental 67, 63–78.Google ScholarPubMed
Angaut, P. & Sotelo, C. (1989). Synaptology of the cerebello-olivary pathway. Double labelling with anterograde axonal tracing and GABA immunocytochemistry in the rat. Brain Research 479, 361–365.CrossRefGoogle ScholarPubMed
Bagnoli, P., Gigliola, F., Alesci, R. & Erichsen, J.T. (1992). Distribution of neuropeptide Y, substance P, and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. Journal of Comparative Neurology 318, 392–414.CrossRefGoogle ScholarPubMed
Border, B.C. & Mihailoff, G.A. (1990). GABAergic neural elements in the rat basilar pons: Electron-microscopic immunochemistry. Journal of Comparative Neurology 295, 123–135.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
Colonnier, M. (1968). Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron-microscopic study. Brain Research 9, 268–287.CrossRefGoogle Scholar
Cowan, W.M. (1970). Centrifugal fibers to the avian retina. British Medical Bulletin 26, 112–118.Google Scholar
Cowan, W.M., Adamson, L. & Powell, T.P.S. (1961). An experimental study of the avian visual system. Journal of Anatomy (London) 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
Cowan, W.M. & Wenger, E. (1968). The development of the nucleus of origin of centrifugal fibers to the retina of the chick. Journal of Comparative Neurology 133, 207–240.CrossRefGoogle Scholar
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
Domenici, L., Waldvogel, H.J., Matute, C. & Streit, P. (1988). Distribution of GABA-like immunoreactivity in the pigeon brain. Neuroscience 25, 931–950.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Cowan, W.M. (1966). An electron-microscope study of normal and degenerating centrifugal fiber terminals in the pigeon retina. Zeitschrift für Zellforschung und Entwicklungsgeschichte 71, 14–28.CrossRefGoogle ScholarPubMed
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
Frumkes, T.E., Miller, R.F., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina, III: Amacrine-mediate inhibitory influences on ganglion cell receptive-field organization: A model. Journal of Neurophysiology 45, 783–804.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.Google Scholar
Granda, R.H. & Crossland, W.J. (1989). GABA-like immunoreactivity of neurons in the chicken diencephalon and mesencephalon. Journal of Comparative Neurology 287, 455–469.CrossRefGoogle ScholarPubMed
Gray, E.G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron-microscopic study. Journal of Anatomy (London) 93, 420–433.Google Scholar
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
Hàmori, J. & Takàcs, J. (1989). Two types of GABA-containing axon terminals in cerebellar glomeruli of cat: An immunogold-EM study. Experimental Brain Research 74, 471–479.CrossRefGoogle Scholar
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). Neurones situated outside the isthmo-optic nucleus and projecting to the eye in adult birds. Neuroscience Letters 26, 107–112.CrossRefGoogle Scholar
Hendrickson, A.E., Ogren, M.P., Vaughn, J.E., Barber, R.P. & Wu, J.-Y. (1983). Light- and electron-microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex: Evidence for GABAergic neurons and synapses. Journal of Neuroscience 3, 1245–1262.CrossRefGoogle ScholarPubMed
Holden, A.L. (1968). The centrifugal system running to the pigeon retina. Journal of Physiology (London) 197, 199–219.CrossRefGoogle Scholar
Holden, A.L. (1978). Centrifugal action on pigeon retinal ganglion cells. Journal of Physiology (London) 282, 8P.Google ScholarPubMed
Holden, A.L. (1982). Electrophysiology of the avian retina. Progress in Retínal Research 1, 179–196.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
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.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
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers of the pigeon retina. Science 150, 359–362.CrossRefGoogle ScholarPubMed
McCormick, D.A. (1992). Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Progress in Neurobiology 39, 337–388.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 Scholar
McGill, J.I., Powell, T.P.S. & Cowan, W.M. (1966 6). 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., 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., Peyrichoux, J. & Repérant, J. (1975). The retino-thalamohyperstriatal pathway in the pigeon, Columba livia. Brain Research 100, 125–131.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., Marchand, L. & Rio, J.-P. (1993). Retrograde transneuronal transport of the fluorescent dye Rhodamine β–isothiocyanate from the primary and centrifugal visual systems in the pigeon. Brain Research 601, 289–298.Google Scholar
Miceli, D., Repérant, J., Villalobos, J. & Weidner, C. (1987). Extratelencephalic projections of the visual Wulst. A quantitative autoradiographic study in the pigeon. Journal of Brain Research and Neurobiology 28, 45–59.Google Scholar
Miceli, D., Rio, J.P., Repérant, J., Marchand, L. & Medina, M. (1992). Pontine oculomotor input to the centrifugal visual system may modulate retinal sensitivity related to gaze. Association for Research in Vision and Ophthalmology 33, 2591.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
Mize, R.R. (1988). Immunocytochemical localization of gammaaminobutyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–187.CrossRefGoogle ScholarPubMed
Mugnaini, E. (1970). The relation between cytogenesis and the formation of different types of synaptic contacts. Brain Research 17, 169–179.CrossRefGoogle Scholar
Mugnaini, E. & Oertel, W.H. (1985). An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In Handbook of Chemical Neuroanatomy: GABA and Neuropeptides in the CNS, Vol. IV, ed. Björk-Lund, A. & Hökfelt, T., pp. 437–609. Amsterdam: Elsevier.Google Scholar
O'Leary, D.D.M. & Cowan, W.M. (1982). Further studies on the development of the isthmo-optic nucleus with special reference to the occurrence and fate of ectopic and ipsilaterally projecting neurons. Journal of Comparative Neurology 212, 399–416.CrossRefGoogle Scholar
Ottersen, O.P. (1989). Quantitative electron-microscopic immunocytochemistry of neuroactive amino acids. Anatomy and Embryology 180, 1–15.CrossRefGoogle ScholarPubMed
Ottersen, O.P. & Storm-Mathisen, J. (1984). Glutamate and GABA containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. Journal of Comparative Neurology 229, 374–392.Google Scholar
Ottersen, O.P. & Storm-Mathisen, J. (1985). Neurons containing or accumulating transmitter amino acids. In Handbook of Chemical Neuroanatomy: Classical Transmitters and Transmitter Receptor in the CNS, Vol. III, ed. Björklund, A., Hökfelt, T. & Kuhar, M.J., pp. 141–245. Amsterdam: Elsevier.Google Scholar
Palay, S.L. & Chan-Palay, V. (1975). A guide to the synaptic analysis of the neuropil. In Cold Spring Harbor Symposia on Quantitative Biology. The Synapse, vol. 40, pp. 1–16. Michigan: Cold Spring Harbor.Google Scholar
Pasik, P., Molinar-Rode, R. & Pasik, T. (1990). Chemically specified systems in the dorsal lateral geniculate nucleus of mammals. In Vision and the Brain, ed. Cohen, B. & Bodis-Wollner, I., pp. 43–83. New York: Raven Press Ltd.Google Scholar
Pearlman, A.L. & Hughes, C.P. (1973). Functional role of efferents to the avian retina: Effects of reversible cooling of the isthmo-optic nucleus. Journal of Comparative Neurology 166, 123–132.CrossRefGoogle Scholar
Peters, A., Palay, S.L. & Webster, H. de F. (1976). The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia, London, Toronto: W.B. Saunders Company.Google Scholar
Pinard, R., Benfares, J. & Lanoir, J. (1991). Electron-microscopic study of GABA-immunoreactive neuronal processes in the superficial gray layer of the rat superior colliculus: Their relationships with degenerating retinal nerve endings. Journal of Neurocytology 20, 262–276.CrossRefGoogle ScholarPubMed
Raffin, J.P. & Repérant, J. (1975). Étude expérimentale de la spécificité des projections visuelles d'embryons et de poussins de Gallus domesticus. L. microphtalmes et monophtalmes. Archives d'anatomie microscopique et de morphologie expérimentale 64, 93–111.Google Scholar
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
Repèrant, J., Peyrichoux, J. & Rio, J.-P. (1981). Fine structure of the superficial layers of the viper optic tectum: A Golgi and electronmicroscopic study. Journal of Comparative Neurology 199, 393–417.CrossRefGoogle Scholar
Ribak, C.E., Vaughn, J.E. & Roberts, E. (1979). The GABA neurons and their axon terminals in rat corpus striatum demonstrated by GAD immunocytochemistry. Journal of Comparative Neurology 187, 261–284.CrossRefGoogle ScholarPubMed
Ribak, C.E., Vaughn, J.E., Saito, K., Barber, B. & Roberts, E. (1976). Immunocytochemical localization of glutamate decarboxylase in rat substantia nigra. Brain Research 116, 287–298.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.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
Soghomonian, J.-J., Pinard, R. & Lanoir, J. (1989). GABA innervation in adult rat oculomotor nucleus: A radioautographic and immunocytochemical study. Journal of Neurocytology 18, 319–331.CrossRefGoogle ScholarPubMed
Somogyi, P. (1989). Synaptic organization of GABAergic neurons and GABAA receptors in the lateral geniculate nucleus and visual cortex. In Neural Mechanisms of Visual Perception, ed. Lam, D.K. & Gilbert, L.D., pp. 35–92. Texas: Portfolio Pub.Google Scholar
Somogyi, P., Hodgson, A.J., Chubb, I.W., Penke, B. & Erdei, A. (1985). Antisera to gammo−aminobutyric acid. II. Immunocytochemical application to the central nervous system. Journal of Histochemistry and Cytochemistry 33, 240–248.CrossRefGoogle ScholarPubMed
Sorenson, E.M., Parkinson, D., Dahl, J.L. & Chiappinelli, V.A. (1989). Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. Journal of Comparative Neurology 281, 641–657.Google Scholar
Sotelo, C., Gotow, T. & Wassef, M. (1986). Localization of glutamicacid-decarboxylase-immunoreactive axon terminals in the inferior olive of the rat, with special emphasis on anatomical relations between GABAergic synapses and dendrodendritic gap junctions. Journal of Comparative Neurology 252, 32–50.CrossRefGoogle ScholarPubMed
Sternberger, L.A., Hardy, P.H. Jr., Cuculis, J. & Meyer, H.G. (1970). The unlabeled antibody enzyme method of immunohistochemistry: Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antiperoxidase) and its use in identification of spirochetes. Journal of Histochemistry and Cytochemistry 18, 315–334.Google Scholar
Tappaz, M.L., Bosler, O., Paut, L. & Berod, A. (1985). Glutamate decarboxylase-immunoreactive boutons in synaptic contacts with hypothalamic dopaminergic cells: A light- and electron-microscopic study combining immunocytochemistry and radioautography. Neuroscience 16, 111–122.CrossRefGoogle ScholarPubMed
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.Google 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., 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
Veenman, C.L. & Reiner, A. (1994). The distribution of GABA-containing perikarya, fibers, and terminals in the forebrain and midbrain of pigeons, with particular reference to the basal ganglia and its projection targets. Journal of Comparative Neurology 339, 209–250.Google 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., 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.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.Google Scholar