Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-25T04:43:47.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Regional distribution of nitrergic neurons in the inner retina of the chicken

Published online by Cambridge University Press:  19 April 2011

MARTIN WILSON ,
NICK NACSA ,
NATHAN S. HART ,
CYNTHIA WELLER  and
DAVID I. VANEY
MARTIN WILSON*
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
NICK NACSA
Affiliation:
ARC Centre of Excellence in Vision Science, Queensland Brain Institute, The University of Queensland, Brisbane, Australia School of Biomedical Sciences, The University of Queensland, Brisbane, Australia
NATHAN S. HART
Affiliation:
School of Biomedical Sciences, The University of Queensland, Brisbane, Australia
CYNTHIA WELLER
Affiliation:
Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, California
DAVID I. VANEY
Affiliation:
ARC Centre of Excellence in Vision Science, Queensland Brain Institute, The University of Queensland, Brisbane, Australia School of Biomedical Sciences, The University of Queensland, Brisbane, Australia
*
†Address correspondence and reprint requests to: Martin Wilson, Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, UC Davis, Davis, CA 95616. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Using both NADPH diaphorase and anti-nNOS antibodies, we have identified—from retinal flatmounts—neuronal types in the inner retina of the chicken that are likely to be nitrergic. The two methods gave similar results and yielded a total of 15 types of neurons, comprising 9 amacrine cells, 5 ganglion cells, and 1 centrifugal midbrain neuron. Six of these 15 cell types are ubiquitously distributed, comprising 3 amacrine cells, 2 displaced ganglion cells, and a presumed orthotopic ganglion cell. The remaining nine cell types are regionally restricted within the retina. As previously reported, efferent fibers of midbrain neurons and their postsynaptic partners, the unusual axon-bearing target amacrine cells, are entirely confined to the ventral retina. Also confined to the ventral retina, though with somewhat different distributions, are the “bullwhip” amacrine cells thought to be involved in eye growth, an orthotopic ganglion cell, and two types of large axon-bearing amacrine cells whose dendrites and axons lie in stratum 1 of the inner plexiform layer (IPL). Intracellular fills of these two cell types showed that only a minority of otherwise morphologically indistinguishable neurons are nitrergic. Two amacrine cells that branch throughout the IPL are confined to an equatorial band, and one small-field orthotopic ganglion cell that branches in the proximal IPL is entirely dorsal. These findings suggest that the retina uses different processing on different regions of the visual image, though the benefit of this is presently obscure.

Keywords

NADPH diaphoraseAmacrine cellGanglion cellNitric oxide
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 3 , May 2011 , pp. 205 - 220
Copyright
Copyright © Cambridge University Press 2011

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

Ahmad, I., Leinders-Zufall, T., Kocsis, J.D., Shepherd, G.M., Zufall, F. & Barnstable, C.J. (1994). Retinal ganglion cells express a cGMP-gated cation conductance activatable by nitric oxide donors. Neuron 12, 155–165.CrossRefGoogle ScholarPubMed
Blute, T.A., Mayer, B. & Eldred, W.D. (1997). Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina. Visual Neuroscience 14, 717–729.Google Scholar
Bruhn, S.L. & Cepko, C.L. (1996). Development of the pattern of photoreceptors in the chick retina. The Journal of Neuroscience 16, 1430–1439.Google Scholar
Catsicas, S., Catsicas, M. & Clarke, P.G. (1987). Long-distance intraretinal connections in birds. Nature 326(6109):186–187.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.Google Scholar
Cuthbertson, S., Zagvazdin, Y.S., Kimble, T.D., Lamoreaux, W.J., Jackson, B.S., Fitzgerald, M.E. & Reiner, A. (1999). Preganglionic endings from nucleus of Edinger-Westphal in pigeon ciliary ganglion contain neuronal nitric oxide synthase. Visual Neuroscience 16, 819–834.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. J Comp Neurol 284(2):275–293.Google Scholar
Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. & Snyder, S.H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proceedings of the National Academy of Sciences of the United States of America 88, 7797–7801.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. The Journal of Physiology 414, 351–375.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1992). Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. The Journal of Physiology 445, 201–230.CrossRefGoogle ScholarPubMed
Drenhaus, U., Morino, P. & Veh, R.W. (2003). On the development of the stratification of the inner plexiform layer in the chick retina. The Journal of Comparative Neurology 460, 1–12.Google Scholar
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.CrossRefGoogle ScholarPubMed
Ehrlich, D., Keyser, K.T. & Karten, H.J. (1987). Distribution of substance P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallus gallus). The Journal of Comparative Neurology 266, 220–233.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Blute, T.A. (2005). Imaging of nitric oxide in the retina. Vision Research 45, 3469–3486.Google Scholar
Fischer, A.J., Dierks, B.D. & Reh, T.A. (2002). Exogenous growth factors induce the production of ganglion cells at the retinal margin. Development 129, 2283–2291.Google Scholar
Fischer, A.J., Omar, G., Walton, N.A., Verrill, T.A. & Unson, C.G. (2005). Glucagon-expressing neurons within the retina regulate the proliferation of neural progenitors in the circumferential marginal zone of the avian eye. The Journal of Neuroscience 25, 10157–10166.CrossRefGoogle ScholarPubMed
Fischer, A.J., Ritchey, E.R., Scott, M.A. & Wynne, A. (2008). Bullwhip neurons in the retina regulate the size and shape of the eye. Developmental Biology 317, 196–212.CrossRefGoogle ScholarPubMed
Fischer, A.J., Scott, M.A., Zelinka, C. & Sherwood, P. (2010). A novel type of glial cell in the retina is stimulated by insulin-like growth factor 1 and may exacerbate damage to neurons and Muller glia. Glia 58, 633–649.Google Scholar
Fischer, A.J., Skorupa, D., Schonberg, D.L. & Walton, N.A. (2006). Characterization of glucagon-expressing neurons in the chicken retina. The Journal of Comparative Neurology 496, 479–494.CrossRefGoogle ScholarPubMed
Fischer, A.J., Stanke, J.J., Ghai, K., Scott, M. & Omar, G. (2007). Development of bullwhip neurons in the embryonic chicken retina. The Journal of Comparative Neurology 503, 538–549.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
Gan, L., Wang, S.W., Huang, Z. & Klein, W.H. (1999) POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Developmental Biology 210, 469–480.CrossRefGoogle Scholar
Gan, L., Xiang, M., Zhou, L., Wagner, D.S., Klein, W.H. & Nathans, J. (1996). POU domain factor Brn-3b is required for the development of a large set of retinal ganglion cells. Proceedings of the National Academy of Sciences of the United States of America 93, 3920–3925.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
Haberecht, M.F., Schmidt, H.H., Mills, S.L., Massey, S.C., Nakane, M. & Redburn-Johnson, D.A. (1998). Localization of nitric oxide synthase, NADPH diaphorase and soluble guanylyl cyclase in adult rabbit retina. Visual Neuroscience 15, 881–890.CrossRefGoogle ScholarPubMed
Haverkamp, S., Kolb, H. & Cuenca, N. (2000). Morphological and neurochemical diversity of neuronal nitric oxide synthase-positive amacrine cells in the turtle retina. Cell & Tissue Research 302, 11–19.Google Scholar
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organisation. In Handbook of Sensory Physiology, ed. Crescitelli, F., pp. 613–756. Berlin, Germany: Springer.Google Scholar
Huxlin, K.R. (1995). NADPH-diaphorase expression in neurons and glia of the normal adult rat retina. Brain Research 692, 195–206.Google Scholar
Karten, J.H., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in the pigeon (Columbia livia). Proceedings of the National Academy of Sciences of the United States of America 74, 1753–1756.Google Scholar
Kihara, A.H., Paschon, V., Cardoso, C.M., Higa, G.S., Castro, L.M., Hamassaki, D.E. & Britto, L.R. (2009). Connexin36, an essential element in the rod pathway, is highly expressed in the essentially rodless retina of Gallus gallus. The Journal of Comparative Neurology 512, 651–663.Google Scholar
Koistinaho, J., Swanson, R.A., De Vente, J. & Sagar, S.M. (1993). NADPH-diaphorase (nitric oxide synthase)-reactive amacrine cells of rabbit retina: Putative target cells and stimulation by light. Neuroscience 57, 587–597.Google Scholar
Kurenni, D.E., Thurlow, G.A., Turner, R.W., Moroz, L.L., Sharkey, K.A. & Barnes, S. (1995). Nitric oxide synthase in tiger salamander retina. The Journal of Comparative Neurology 361, 525–536.CrossRefGoogle ScholarPubMed
Lindstrom, S.H., Nacsa, N., Blankenship, T., Fitzgerald, P.G., Weller, C., Vaney, D.I. & Wilson, M. (2009). Distribution and structure of efferent synapses in the chicken retina. Visual Neuroscience 26, 215–226.Google Scholar
Liu, W., Khare, S.L., Liang, X., Peters, M.A., Liu, X., Cepko, C.L. & Xiang, M. (2000). All Brn3 genes can promote retinal ganglion cell differentiation in the chick. Development 127, 3237–3247.Google Scholar
Matsumoto, T., Nakane, M., Pollock, J.S., Kuk, J.E. & Forstermann, U. (1993). A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neuroscience Letters 155, 61–64.CrossRefGoogle ScholarPubMed
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150, 359–361.Google Scholar
Mayer, B., John, M. & Bohme, E. (1990). Purification of a Ca2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor-role of tetrahydrobiopterin. FEBS Letters 277, 215–219.Google Scholar
Millar, T., Ishimoto, I., Johnson, C.D., Epstein, M.L., Chubb, I.W. & Morgan, I.G. (1985). Cholinergic and acetylcholinesterase-containing neurons of the chicken retina. Neuroscience Letters 61, 311–316.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737.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
Naito, J. & Chen, Y. (2004). Morphologic analysis and classification of ganglion cells of the chick retina by intracellular injection of Lucifer Yellow and retrograde labeling with DiI. The Journal of Comparative Neurology 469, 360–376.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
Palanza, L., Jhaveri, S., Donati, S., Nuzzi, R. & Vercelli, A. (2005). Quantitative spatial analysis of the distribution of NADPH-diaphorase-positive neurons in the developing and mature rat retina. Brain Research Bulletin 65, 349–360.CrossRefGoogle ScholarPubMed
Perez, M.T., Larsson, B., Alm, P., Andersson, K.E. & Ehinger, B. (1995). Localisation of neuronal nitric oxide synthase-immunoreactivity in rat and rabbit retinas. Experimental Brain Research 104, 207–217.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
Pottek, M., Schultz, K. & Weiler, R. (1997). Effects of nitric oxide on the horizontal cell network and dopamine release in the carp retina. Vision Research 37, 1091–1102.CrossRefGoogle ScholarPubMed
Ramón y Cajal, S. (1893). La retine des vertebres. La Cellule 9, 17–257.Google Scholar
Ramón y Cajal, S. (1972). The Structure of the Retina. Springfield, IL: C. C. Thomas. xxxix.Google 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
Rompani, S.B. & Cepko, C.L. (2010). A common progenitor for retinal astrocytes and oligodendrocytes. The Journal of Neuroscience 30, 4970–4980.Google Scholar
Sagar, S.M. (1986). NADPH diaphorase histochemistry in the rabbit retina. Brain Research 373, 153–158.Google Scholar
Sagar, S.M. (1987). Somatostatin-like immunoreactive material in the rabbit retina: Immunohistochemical staining using monoclonal antibodies. The Journal of Comparative Neurology 266, 291–299.Google Scholar
Sandell, J.H. (1985). NADPH diaphorase cells in the mammalian inner retina. The Journal of Comparative Neurology 238, 466–472.Google Scholar
Sandell, J.H. & Masland, RH. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. J Histochem Cytochem 36(5):555–559.Google Scholar
Sato, T. (1990). NADPH-diaphorase positive amacrine cells in the retinae of the frog (Rana esculenta) and pigeon (Columbia livia). Archives of Histology & Cytology 53, 63–69.Google Scholar
Savchenko, A., Barnes, S. & Kramer, R.H. (1997). Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694–698.Google Scholar
Spira, A.W., Shimizu, Y. & Rorstad, O.P. (1984). Localization, chromatographic characterization, and development of somatostatin-like immunoreactivity in the guinea pig retina. The Journal of Neuroscience 4, 3069–3079.CrossRefGoogle ScholarPubMed
Straznicky, C. & Chehade, M. (1987). The formation of the area centralis of the retinal ganglion cell layer in the chick. Development 100, 411–420.Google Scholar
Thomas, E. & Pearse, A.G. (1961). The fine localization of dehydrogenases in the nervous system. Zeitschrift für Zellforschung und Mikroskopische Anatomie. Abteilung Histochemie 2, 266–282.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.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. & 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.Google Scholar
Versaux-Botteri, C., Martin-Martinelli, E., Nguyen-Legros, J., Geffard, M., Vigny, A. & Denoroy, L. (1986). Regional specialization of the rat retina: Catecholamine-containing amacrine cell characterization and distribution. The Journal of Comparative Neurology 243, 422–433.Google Scholar
Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. The Journal of Comparative Neurology 440, 109–125.Google Scholar
Wassle, H., Chun, M.H. & Muller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. The Journal of Comparative Neurology 265, 391–408.Google Scholar
Weiler, R. & Kewitz, B. (1993). The marker for nitric oxide synthase, NADPH-diaphorase, co-localizes with GABA in horizontal cells and cells of the inner retina in the carp retina. Neuroscience Letters 158, 151–154.Google Scholar
Weller, C., Lindstrom, S.H., De Grip, W.J. & Wilson, M. (2009). The area centralis in the chicken retina contains efferent target amacrine cells. Visual Neuroscience 26, 249–254.Google Scholar
Wetzel, R.K. & Eldred, W.D. (1997). Specialized neuropeptide Y- and glucagon-like immunoreactive amacrine cells in the peripheral retina of the turtle. Visual Neuroscience 14, 867–877.Google Scholar
White, C.A., Chalupa, L.M., Johnson, D. & Brecha, N.C. (1990). Somatostatin-immunoreactive cells in the adult cat retina. The Journal of Comparative Neurology 293, 134–150.Google Scholar
Williamson, D.E. & Eldred, W.D. (1989). Amacrine and ganglion cells with corticotropin-releasing-factor-like immunoreactivity in the turtle retina. The Journal of Comparative Neurology 280, 424–435.Google Scholar
Wright, L.L. & Vaney, D.I. (2004). The type 1 polyaxonal amacrine cells of the rabbit retina: A tracer-coupling study. Visual Neuroscience 21, 145–155.Google Scholar
Xiang, M., Zhou, L., Macke, J.P., Yoshioka, T., Hendry, S.H., Eddy, R.L., Shows, T.B. & Nathans, J. (1995). The Brn-3 family of POU-domain factors: Primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. The Journal of Neuroscience 15(Pt 1), 4762–4785.Google Scholar
Yamamoto, R., Bredt, D.S., Snyder, S.H. & Stone, R.A. (1993). The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 54, 189–200.CrossRefGoogle ScholarPubMed
Yang, G., Millar, T.J. & Morgan, I.G. (1989). Co-lamination of cholinergic amacrine cell and displaced ganglion cell dendrites in the chicken retina. Neuroscience Letters 103, 151–156.Google Scholar
Yew, D.T., Wong, H.W., Li, W.P., Lai, H.W. & Yu, W.H. (1999). Nitric oxide synthase neurons in different areas of normal aged and Alzheimer’s brains. Neuroscience 89, 675–686.Google Scholar
Yu, D. & Eldred, W.D. (2005). Nitric oxide stimulates gamma-aminobutyric acid release and inhibits glycine release in retina. The Journal of Comparative Neurology 483, 278–291.Google Scholar
Zhang, D. & Eldred, W.D. (1992). Colocalization of enkephalin-, glucagon-, and corticotropin-releasing factor-like immunoreactivity in GABAergic amacrine cells in turtle retina. Brain Research 596, 46–57.Google Scholar