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The area centralis in the chicken retina contains efferent target amacrine cells

Published online by Cambridge University Press:  01 March 2009

CYNTHIA WELLER ,
SARAH H. LINDSTROM ,
WILLEM J. DE GRIP  and
MARTIN WILSON
CYNTHIA WELLER
Affiliation:
College of Biological Sciences, Department of Neurobiology, Physiology and Behavior, University of California, Davis, California
SARAH H. LINDSTROM
Affiliation:
College of Biological Sciences, Department of Neurobiology, Physiology and Behavior, University of California, Davis, California
WILLEM J. DE GRIP
Affiliation:
Department of Biochemistry, Nijmegen Centre for Molecular Life Sciences, Radboud University of Nijmegen Medical Centre, Nijmegen, The Netherlands
MARTIN WILSON*
Affiliation:
College of Biological Sciences, Department of Neurobiology, Physiology and Behavior, University of California, Davis, California
*
*Address correspondence and reprint requests to: Martin Wilson, Division of Biological Sciences, Department of Neurobiology, Physiology and Behavior, University of California, Davis, CA 95616. E-mail: [email protected]
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Abstract

The retinas of birds receive a substantial efferent, or centrifugal, input from a midbrain nucleus. The function of this input is presently unclear, but previous work in the pigeon has shown that efferent input is excluded from the area centralis, suggesting that the functions of the area centralis and the efferent system are incompatible. Using an antibody specific to rods, we have identified the area centralis in another species, the chicken, and mapped the distribution of the unique amacrine cells that are the postsynaptic partners of efferent fibers. Efferent target amacrine cells are found within the chicken area centralis and their density is continuous across the border of the area centralis. In contrast to the pigeon retina then, we conclude that the chicken area centralis receives efferent input. We suggest that the difference between the two species is attributable to the presence of a fovea within the area centralis of the pigeon and its absence from that of the chicken.

Keywords

AvianCentrifugalRhodopsinParvalbuminVision
Type
Brief Communication
Information
Visual Neuroscience , Volume 26 , Issue 2 , March 2009 , pp. 249 - 254
Copyright
Copyright © Cambridge University Press 2009

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References

Binggeli, R.L. & Paule, W.J. (1969). The pigeon retina: Quantitative aspects of the optic nerve and ganglion cell layer. The Journal of Comparative Neurology 137, 1–18.CrossRefGoogle ScholarPubMed
Bruhn, S.L. & Cepko, C.L. (1996). Development of the pattern of photoreceptors in the chick retina. The Journal of Neuroscience 16, 1430–1439.CrossRefGoogle ScholarPubMed
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 Science USA 84, 8165–8168.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Clarke, P.G., Gyger, M. & Catsicas, S. (1996). A centrifugally controlled circuit in the avian retina and its possible role in visual attention switching. Visual Neuroscience 13, 1043–1048.CrossRefGoogle ScholarPubMed
Clarke, P.G. & 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 and Cognate Medical Sciences 61, 351–358.CrossRefGoogle Scholar
Cowan, W.M. & Powell, T.P. (1963). Centrifugal fibres in the avian visual system. Proceedings of the Royal Society. B: 158, 232–252.Google Scholar
De Grip, W.J. (1982). Purification of bovine rhodopsin over concanavalin A–sepharose. Methods in Enzymology 81, 197–207.CrossRefGoogle ScholarPubMed
De Grip, W.J., Daemen, F.J. & Bonting, S.L. (1980). Isolation and purification of bovine rhodopsin. Methods in Enzymology 67, 301–320.CrossRefGoogle ScholarPubMed
Degrip, W.J. & Boveegeurts, P.H.M. (1979). Synthesis and properties of alkylglucosides with mild detergent action—Improved synthesis and purification of beta-1-octyl-glucose, beta-1-nonyl-glucose and beta-1-decyl-glucose—Synthesis of beta-1-undecylglucose and beta-1-dodecylmaltose. Chemistry and Physics of Lipids 23, 321–335.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Ehrlich, D. (1981). Regional specialization of the chick retina as revealed by the size and density of neurons in the ganglion cell layer. The Journal of Comparative Neurology 195, 643–657.Google Scholar
Fischer, A.J., Seltner, R.L., Poon, J. & Stell, W.K. (1998). Immunocytochemical characterization of quisqualic acid- and N-methyl-D-aspartate-induced excitotoxicity in the retina of chicks. The Journal of Comparative Neurology 393, 1–15.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, 1–14.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Foster, R.G., Garcia-Fernandez, J.M., Provencio, I. & DeGrip, W.J. (1993). Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. Journal of Comparative Physiology. A172: 33–45.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Galifret, Y. (1968). Les diverses aires fonctionnelles de la retine du Pigeon. Zeitschrift für Zellforschung und mikroskopische Anatomie 86, 535–545.CrossRefGoogle Scholar
Geusz, M.E., Foster, R.G., DeGrip, W.J. & Block, G.D. (1997). Opsin-like immunoreactivity in the circadian pacemaker neurons and photoreceptors of the eye of the opisthobranch mollusc Bulla gouldiana. Cell and Tissue Research 287, 203–210.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 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.CrossRefGoogle ScholarPubMed
Jacob, V., Rothermel, A., Wolf, P. & Layer, P.G. (2005). Rhodopsin, violet and blue opsin expressions in the chick are highly dependent on tissue and serum conditions. Cells, Tissues, Organs 180, 159–168.CrossRefGoogle ScholarPubMed
Li, W.C., Hu, J. & Wang, S.R. (1999). Tectal afferents monosynaptically activate neurons in the pigeon isthmo-optic nucleus. Brain Research Bulletin 49, 203–208.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Morris, V.B. (1982). An afoveate area centralis in the chick retina. The Journal of Compartive Neurology 210, 198–203.CrossRefGoogle ScholarPubMed
Morris, V.B. & Shorey, C.D. (1967). An electron microscope study of types of receptor in the chick retina. The Journal of Comparative Neurology 129, 313–340.Google Scholar
Okano, T., Fukada, Y., Artamonov, I.D. & Yoshizawa, T. (1989). Purification of cone visual pigments from chicken retina. Biochemistry 28, 8848–8856.Google Scholar
Partida, G.J., Lee, S.C., Haft-Candell, L., Nichols, G.S. & Ishida, A.T. (2004). DARPP-32-like immunoreactivity in AII amacrine cells of rat retina. The Journal of Comparative Neurology 480, 251–263.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. (1896). Nouvelles contributions à l'étude histologique de la rétine. Journal de l'Anatomie et de la Physiologie 32, 481–543.Google Scholar
Rothermel, A., Willbold, E., deGrip, W.J., Layer, P.G. (1997). Pigmented epithelium induces complete retinal reconstitution from dispersed embryonic chick retinae in reaggregation culture. Proceedings of the Royal Society. B: Biological Sciences 264, 1293–1302.CrossRefGoogle ScholarPubMed
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
Slonaker, J.R. (1897). A comparative study of the area of acute vision in vertebrates. Journal of Morphology 13, 445–502.Google Scholar
Straznicky, C. & Chehade, M. (1987). The formation of the area centralis of the retinal ganglion cell layer in the chick. Development 100, 411–420.CrossRefGoogle ScholarPubMed
Takao, M., Yasui, A. & Tokunaga, F. (1988). Isolation and sequence determination of the chicken rhodopsin gene. Vision Research 28, 471–480.Google Scholar
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.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.Google Scholar
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., Yamamoto, N. & Ito, H. (1996). Tectal neurons that participate in centrifugal control of the quail retina: A morphological study by means of retrograde labeling with biocytin. Visual Neuroscience 13, 1119–1127.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Institute of Science.Google 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.CrossRefGoogle ScholarPubMed
Yazulla, S. (1974). Intraretinal differentiation in the synaptic organization of the inner plexiform layer of the pigeon retina. The Journal of Comparative Neurology 153, 309–324.Google Scholar