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Distribution and structure of efferent synapses in the chicken retina

Published online by Cambridge University Press:  01 March 2009

S. H. LINDSTROM ,
N. NACSA ,
T. BLANKENSHIP ,
P. G. FITZGERALD ,
C. WELLER ,
D. I. VANEY  and
MARTIN WILSON
S. H. LINDSTROM
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
N. NACSA
Affiliation:
ARC Centre of Excellence in Vision Science, Queensland Brain Institute, University of Queensland, Brisbane, Queensland, Australia
T. BLANKENSHIP
Affiliation:
Department of Cell Biology and Human Anatomy, School of Medicine, University of California, Davis, California
P. G. FITZGERALD
Affiliation:
Department of Cell Biology and Human Anatomy, School of Medicine, University of California, Davis, California
C. WELLER
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
D. I. VANEY
Affiliation:
ARC Centre of Excellence in Vision Science, Queensland Brain Institute, University of Queensland, Brisbane, Queensland, Australia
MARTIN WILSON*
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
*
*Address correspondence and reprint requests to: Martin Wilson, Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, CA 95616. E-mail: mcwilson@ucdavis.edu
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Abstract

The visual system of birds includes an efferent projection from a visual area, the isthmo-optic nucleus in the midbrain, back to the retina. Using a combination of anterograde labeling of efferent fibers, reconstruction of dye-filled neurons, NADPH-diaphorase staining, and transmission electron microscopy, we have examined the distribution of efferent fibers and their synaptic structures in the chicken retina. We show that efferent fibers terminate strictly within the ventral retina. In two completely mapped retinas, only 2 fibers from a total of 15,359 terminated in the dorsal retina. The major synapse made by each efferent fiber is with a single efferent target amacrine cell (TC). This synapse consists of 5–25 boutons of 2 μm diameter, each with multiple active zones, pressed into the TC soma or synapsing with a basketwork of rudimentary TC dendrites in the inner nuclear layer (INL). This basketwork, which is sheathed by Muller cell processes, defines a private neuropil in the INL within which TCs were also seen to receive input from retinal neurons. In addition to the major synapse, efferent fibers typically produce several very thin processes that terminate nearby in single small boutons and for which the soma of a local amacrine cell is one of the likely postsynaptic partners. A minority of efferent fibers also give rise to a thicker process, terminating in a strongly diaphorase-positive ball about 5 μm in diameter.

Keywords

Amacrine cellIsthmo-optic nucleusAvianRetinopetalCentrifugal visual system
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 2 , March 2009 , pp. 215 - 226
Copyright
Copyright © Cambridge University Press 2009

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References

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. The Journal of Histochemistry and Cytochemistry 29, 775.Google Scholar
Blute, T.A., Lee, M.R. & Eldred, W.D. (2000). Direct imaging of NMDA-stimulated nitric oxide production in the retina. Visual Neuroscience 17, 557–566.Google Scholar
Catsicas, S., Catsicas, M. & Clarke, P.G. (1987 a). Long-distance intraretinal connections in birds. Nature 326, 186–187.Google Scholar
Catsicas, S., Thanos, S. & Clarke, P.G. (1987 b). Major role for neuronal death during brain development: Refinement of topographical connections. Proceedings of the National Academy of Sciences of the United States of America 84, 8165–8168.Google Scholar
Cellerino, A., Novelli, E. & Galli-Resta, L. (2000). Retinal ganglion cells with NADPH-diaphorase activity in the chick form a regular mosaic with a strong dorsoventral asymmetry that can be modelled by a minimal spacing rule. The European Journal of Neuroscience 12, 613–620.Google Scholar
Chmielewski, C.E., Dorado, M.E., Quesada, A., Geniz-Galvez, J.M. & Prada, F.A. (1988). Centrifugal fibers in the chick retina. A morphological study. Anatomia, Histologia, Embryologia 17, 319–327.Google Scholar
Cowan, W.M. (1970). Centrifugal fibres of the avian retina. British medical Bulletin 26, 112–118.Google Scholar
Cowan, W.M. & Powell, T.P. (1962). Centrifugal fibres to the retina in the pigeon. Nature 194, 487.CrossRefGoogle 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.Google Scholar
Dacey, D.M., Peterson, B.B., Robinson, F.R. & Gamlin, P.D. (2003). Fireworks in the primate retina: In vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27.Google Scholar
Dawson, T.M. & Snyder, S.H. (1994). Gases as biological messengers: Nitric oxide and carbon monoxide in the brain. The Journal of Neuroscience 14, 5147–5159.Google Scholar
Dogiel, A.S. (1895). Die Retina der Vogel. Archiv Mikroskopische Anatomie 44, 622–648.Google Scholar
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 Mikroskopische Anatomie 71, 14–28.Google Scholar
Fischer, A.J. & Stell, W.K. (1999). Nitric oxide synthase-containing cells in the retina, pigmented epithelium, choroid, and sclera of the chick eye. The Journal of Comparative Neurology 405, 1–14.Google Scholar
Fritzsch, B., Crapon de Caprona, 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. The Journal of Comparative Neurology 300, 405–421.Google Scholar
Goureau, O., Regnier-Ricard, F., Jonet, L., Jeanny, J.C., Courtois, Y. & Chany-Fournier, F. (1997). Developmental expression of nitric oxide synthase isoform I and III in chick retina. Journal of Neuroscience Research 50, 104–113.Google 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.Google Scholar
Holden, A.L. & Powell, T.P. (1972). The functional organization of the isthmo-optic nucleus in the pigeon. The Journal of Physiology 223, 419–447.Google Scholar
Hoshino, K., Hicks, T.P., Hirano, S. & Norita, M. (2000). Ultrastructural organization of transmitters in the cat lateralis medialis-suprageniculate nucleus of the thalamus: An immunohistochemical study. The Journal of Comparative Neurology 419, 257–270.Google Scholar
Iliakis, B., Anderson, N.L., Irish, P.S., Henry, M.A. & Westrum, L.E. (1996). Electron microscopy of immunoreactivity patterns for glutamate and gamma-aminobutyric acid in synaptic glomeruli of the feline spinal trigeminal nucleus (Subnucleus Caudalis). The Journal of Comparative Neurology 366, 465–477.Google Scholar
Li, J.L., Xiao, Q., Fu, Y.X. & Wang, S.R. (1998). Centrifugal innervation modulates visual activity of tectal cells in pigeons. Visual Neuroscience 15, 411–415.Google Scholar
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150, 359–361.Google Scholar
McGill, J.I., Powell, T.P. & Cowan, W.M. (1966). The retinal representation upon the optic tectum and isthmo-optic nucleus in the pigeon. Journal of Anatomy 100, 5–33.Google ScholarPubMed
Miles, F.A. (1972). Centrifugal control of the avian retina. 2. Receptive field properties of cells in the isthmo-optic nucleus. Brain Research 48, 93–113.Google Scholar
Mize, R.R., Whitworth, R.H., Nunes-Cardozo, B. & van der Want, J. (1994). Ultrastructural organization of GABA in the rabbit superior colliculus revealed by quantitative postembedding immunocytochemistry. The Journal of Comparative Neurology 341, 273–287.CrossRefGoogle ScholarPubMed
Montero, V.M. & Singer, W. (1984). Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat. A light and electron microscopic immunocytochemical study. Experimental Brain Research 56, 115–125.Google Scholar
Morgan, I.G., Miethke, P. & Li, Z.K. (1994). Is nitric oxide a transmitter of the centrifugal projection to the avian retina? Neuroscience Letters 168, 5–7.Google Scholar
Nalbach, H.O., Wolf-Oberhollenzer, F. & Remy, M. (1993). Exploring the image. In Vision, Brain, and Behavior in Birds, ed. Zeigler, H.P. & Bischof, H.-J., pp. 25–46. Cambridge, MA: MIT Press.Google Scholar
Nickla, D.L., Gottlieb, M.D., Marin, G., Rojas, X., Britto, L.R. & Wallman, J. (1994). The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system. Visual Neuroscience 11, 401–409.Google Scholar
Oberdorfer, M.D., Parakkal, M.H., Altschuler, R.A. & Wenthold, R.J. (1988). Ultrastructural localization of GABA-immunoreactive terminals in the anteroventral cochlear nucleus of the guinea pig. Hearing Research 33, 229–238.CrossRefGoogle ScholarPubMed
Posada, A. & Clarke, P.G. (1999). Role of nitric oxide in a fast retrograde signal during development. Brain Research. Developmental Brain Research 114, 37–42.Google Scholar
Ramón y Cajal, S. (1889). Sur la morphologie et les connexions des elements de la retine des oiseaux. Anatomischer Anzeiger 4, 111–121.Google Scholar
Ramón y Cajal, S. (1895). Sobre unos corpusculos espesciales de la retina de las aves. Actas de la Sociedad Espanola de Historia Natural 24, 128–130.Google Scholar
Ramón y Cajal, S. (1995). Histology of the Nervous System of Man and Vertebrates. New York: Oxford University Press.CrossRefGoogle Scholar
Rios, H., Lopez-Costa, J.J., Fosser, N.S., Brusco, A. & Saavedra, J.P. (2000). Development of nitric oxide neurons in the chick embryo retina. Brain Research. Developmental Brain Research 120, 17–25.Google Scholar
Sagar, S.M. (1986). NADPH diaphorase histochemistry in the rabbit retina. Brain Research 373, 153–158.Google Scholar
Sanna, P.P., Keyser, K.T., Deerink, T.J., Ellisman, M.H., Karten, H.J. & Bloom, F.E. (1992). Distribution and ontogeny of parvalbumin immunoreactivity in the chicken retina. Neuroscience 47, 745–751.Google Scholar
Sherman, S.M. & Guillery, R.W. (2002). The role of the thalamus in the flow of information to the cortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 1695–1708.CrossRefGoogle ScholarPubMed
Uchiyama, H., Aoki, K., Yonezawa, S., Arimura, F. & Ohno, H. (2004). Retinal target cells of the centrifugal projection from the isthmo-optic nucleus. The Journal of Comparative Neurology 476, 146–153.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., Ito, H. & Tauchi, M. (1995). Retinal neurones specific for centrifugal modulation of vision. Neuroreport 6, 889–892.CrossRefGoogle ScholarPubMed
Uchiyama, H., Nakamura, S. & Imazono, T. (1998). Long-range competition among the neurons projecting centrifugally to the quail retina. Visual Neuroscience 15, 417–423.Google Scholar
Uchiyama, H. & Stell, W.K. (2005). Association amacrine cells of Ramon y Cajal: Rediscovery and reinterpretation. Visual Neuroscience 22, 881–891.Google Scholar
Vaney, D.I. (2004). Type 1 nitrergic (ND1) cells of the rabbit retina: Comparison with other axon-bearing amacrine cells. The Journal of Comparative Neurology 474, 149–171.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380–385.CrossRefGoogle ScholarPubMed
Vugler, A.A., Semo, M., Joseph, A. & Jeffery, G. (2008). Survival and remodeling of melanopsin cells during retinal dystrophy. Visual neuroscience 25, 125–138.Google Scholar
Wilson, M. & Vaney, D.I. (2008). Amacrine cells. In The Senses: A Comprehensive Reference, Basbaum, A.I., Kaneko, A., Shephard, G.M. & Westheimer, G., (eds)., Vol 1, Vision 1, Masland, R. & Albright, T.D., (eds). pp. 361–368. San Diego: Academic Press.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). The Journal of Comparative Neurology 362, 489–509.Google Scholar