Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-18T13:54:52.341Z Has data issue: false hasContentIssue false

Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis, I: Gamma-aminobutyric acid

Published online by Cambridge University Press:  02 June 2009

David M. Sherry
Affiliation:
Departments of Neuroscience and Ophthalmology, University of Florida, Gainesville
Robert J. Ulshafer
Affiliation:
Departments of Neuroscience and Ophthalmology, University of Florida, Gainesville

Abstract

The inhibitory amino-acid neurotransmitter, gamma-aminobutyric acid (GABA), was localized in the pure cone retina of the lizard Anolis carolinensis by autoradiographic and immunocytochemical techniques. Uptake of [3H]-GABA labeled horizontal cells, amacrine cells, numerous cells in the ganglion cell layer, both plexiform layers, and the nerve fiber layer. Label in the inner plexiform layer showed distinct lamination.

The pattern of GABA immunoreactivity was similar to the pattern of [3H]-GABA uptake, although some differences, particularly in labeling of amacrine and ganglion cells, were observed. Immunocytochemistry revealed endogenous stores of GABA in a set of horizontal cells, amacrine cells, and cells in the ganglion cell layer. Both plexiform layers were labeled by the GABA antisera. Labeling in the inner plexiform layer (IPL) was highly stratified and GABA-immunoreactive strata were present in both sublaminae a and b. Six subtypes of conventionally placed GABA-immunoreactive amacrine cells and one displaced amacrine cell subtype were identified. Three of the six conventional amacrine cell subtypes were of pyriform morphology and three subtypes were of multipolar morphology. GABA-immunoreactive interstitial cells also were observed.

Under certain conditions the GABA antiserum labeled the cones. Etching the resin eliminated cone labeling, suggesting that GABA in the cones is present in a labile pool, unlike GABA in horizontal or amacrine cells, or the observed labeling was not due to endogenous GABA. Cones did not demonstrate [3H]-GABA uptake.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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

Agardh, E., Bruun, A., Ehinger, B. & Storm-Mathisen, J. (1986). GABA immunoreactivity in the retina. Investigative Ophthalmology and Visual Science 27, 674678.Google ScholarPubMed
Ammermuller, J. & Weiler, R. (1989). Correlation between electro-physiological response and morphological classes of turtle retinal amacrine cells. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 117132. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Ayoub, G.S., Korenbrot, J.I. & Copenhagen, D.R. (1989). Release of endogenous glutamate from isolated cone photoreceptors of the lizard. Neuroscience Research (Suppl.) 10, 4756.Google ScholarPubMed
Ball, A.K. (1987). Immunocytochemical and autoradiographic localization of GABAergic neurons in the goldfish retina. Journal of Comparative Neurology 255, 317325.CrossRefGoogle ScholarPubMed
Ball, A. & Brandon, C. (1986). Localization of 3H-GABA, muscimol, and glycine in goldfish retinas stained for glutamate decarboxylase. Journal of Neuroscience 6, 16211627.CrossRefGoogle ScholarPubMed
Bok, D. & Young, R.W. (1972). The renewal of diffusely distributed protein in the outer segments of rods and cones. Vision Research 12, 161169.CrossRefGoogle ScholarPubMed
Brandon, C. (1985). Retinal GABA neurons: Localization in vertebrate species using an antiserum to rabbit brain glutamate decarboxylase. Brain Research 344, 286295.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1893). La retine des vertebres. In The Vertebrate Retina: Principles of Structure and Function, trans. Rodieck, R.W. & Maguire, D., pp. 775904. San Francisco: W.H. Freeman and Company.Google Scholar
Chun, M.-H., Wassle, H. & Brecha, N. (1988). Colocalization of [3H]-muscimol uptake and choline acetyltransferase immunoreactivity in amacrine cells of the cat retina. Neuroscience Letters 94, 259263.CrossRefGoogle ScholarPubMed
Crescitelli, F. (1972). The visual cells and visual pigments of the vertebrate eye. In Handbook of Sensory Physiology, Vol. VII/1, ed. Dartnall, H.J.A., pp. 245363. New York: Springer-Verlag.Google Scholar
Danscher, G. & Norgaard, J.O.R. (1983). Light microscopic visualization of colloidal gold on resin-embedded tissue. Journal of Histochemistry and Cytochemistry 31, 13941398.CrossRefGoogle ScholarPubMed
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 83218325.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Yaqub, A. (1989). The diverse localization of aspartate-like immunoreactivity in the turtle retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 321.Google Scholar
Engbretson, G.A., Anderson, K.J. & Wu, J.Y. (1987). GAD and GABA immunoreactive cones in the retina of a lizard. Investigative Ophthalmology and Visual Science (Suppl.) 28, 279.Google Scholar
Engbretson, G.A., Anderson, K.J. & Wu, J.Y. (1989). GABA as a potential transmitter in lizard photoreceptors: Immunocytochemical and biochemical evidence. Journal of Comparative Neurology 278, 461471.CrossRefGoogle Scholar
Engbretson, G.A. & Battelle, B.A. (1987). Serotonin and dopamine in the retina of a lizard. Journal of Comparative Neurology 257, 140147.CrossRefGoogle ScholarPubMed
Fowlkes, D.H., Karwoski, C.J. & Proenza, L.M. (1984). Endogenous circadian rhythm in electroretinogram of free-moving lizards. Investigative Ophthalmology and Visual Science 25, 121124.Google ScholarPubMed
GuilletteL.J., Jr. L.J., Jr. (1982). A physiological (Ringer's) solution for Anoline lizards. Herpetology Reviews 13, 3738.Google Scholar
Hodgekinson, P.E. & Still, A.W. (1980). Color and brightness preferences in the lizard Anolis carolinensis. Perception 9, 6168.CrossRefGoogle Scholar
HurdL.B., II. L.B., II. & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 920.CrossRefGoogle ScholarPubMed
Lake, N. & Verdone-Smith, C. (1989). Immunocytochemical localization of taurine in the mammalian retina. Current Eye Research 8, 163173.CrossRefGoogle ScholarPubMed
Lam, D.M.K., Fung, S.C. & Kong, Y.C. (1980). Postnatal development of GABAergic neurons in the rabbit retina. Journal of Comparative Neurology 193, 89102.Google ScholarPubMed
Lam, D.M.K., Li, H.-B., Su, Y.Y.T. & Watt, C.B. (1985). The signature hypothesis: Colocalizations of neuroactive substances as anatomical probes for circuitry analyses. Vision Research 25, 13531364.CrossRefGoogle ScholarPubMed
Leeper, H. (1978a). Horizontal cells of the turtle retina: Light microscopy of Golgi preparations. Journal of Comparative Neurology 182, 777794.CrossRefGoogle ScholarPubMed
Leeper, H. (1978b). Horizontal cells of the turtle retina: Analysis of interactions between photoreceptor cells and horizontal cells by light microscopy. Journal of Comparative Neurology 182, 795810.CrossRefGoogle Scholar
Marc, R.E. (1986). Neurochemical stratification in the IPL of the vertebrate retina. Vision Research 26, 223238.CrossRefGoogle Scholar
Marc, R.E., Liu, W.-L.S., Kalloniatis, M., Raiguel, S.F. & Van Haesendonck, E. (1990). Patterns of glutamate immunoreactivity in the goldfish retina. Journal of Neuroscience 10, 40064034.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221246.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1987). Neuronal and synaptic organization of the outer plexiform layer of the pigeon retina. American Journal of Anatomy 179, 2539.CrossRefGoogle ScholarPubMed
Marshall, J. & Voaden, M.J. (1974). An autoradiographic study of the cells accumulating 3H-gamma-aminobutyric acid in the isolated retinas of pigeons and chickens. Investigative Ophthalmology 13, 602607.Google Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399425.CrossRefGoogle Scholar
Mosinger, J.L., Yazulla, S. & Studholme, K.M. (1986). GABA-like immunoreactivity in the vertebrate retina: A species comparison. Experimental Eye Research 42, 631644.CrossRefGoogle ScholarPubMed
Muller, J.F. & Marc, R.E. (1990). GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. Journal of Comparative Neurology 291, 281304.CrossRefGoogle ScholarPubMed
Nishimura, Y., Schwartz, M.L. & Rakic, P. (1986). GABA and GAD immunoreactivity of photoreceptor terminals in primate retina. Nature 320, 753756.CrossRefGoogle ScholarPubMed
Ottersen, O.P. (1987). Postembedding light- and electron-microscopic immunocytochemistry of amino acids: Description of a new model system allowing identical conditions for specificity testing and tissue processing. Experimental Brain Research 69, 167174.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the.GABA agonist, 3H-muscimol: A combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 2535.CrossRefGoogle ScholarPubMed
Roth, J. (1983). The colloidal gold marker system for light and electron microscopic cytochemistry. In Techniques in Immunocytochemistry, Vol. 2, ed. Bullock, G.R. & Petrusz, P., pp. 217284. London, England: Academic Press.Google Scholar
Seguela, P., Geffard, M., Buijs, R.M. & Le Moal, M. (1984). Antibodies against gamma-aminobutyric acid: Specificity studies and immunocytochemical results. Proceedings of the National Academy of Sciences of the U.S.A. 81, 38883892.CrossRefGoogle ScholarPubMed
Sherry, D.M. & Ulshafer, R.J. (1986). Uptake and release of 3H-GABA in the “all-cone” Anolis retina. Investigative Ophthalmology and Visual Science (Suppl). 27, 232.Google Scholar
Sherry, D.M. & Ulshafer, R.J. (1988). Immunocytochemical localization of putative neurotransmitters in the “all-cone” Anolis retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 195.Google Scholar
Sherry, D.M. & Ulshafer, R.J. (1992). Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis, II: Glutamate and aspartate. Visual Neuroscience (in press).CrossRefGoogle Scholar
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473502.CrossRefGoogle ScholarPubMed
Stell, W.K., Lightfoot, D.O., Wheeler, T.G. & Leeper, H.F. (1975). Goldfish retina: Functional polarization of cone horizontal cell dendrites and synapses. Science 190, 989990.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1987). Functional and morphological correlates of amacrine cells in carp retina. Neuroscience 20, 935950.CrossRefGoogle ScholarPubMed
Underwood, G. (1951). Reptilian retinas. Nature 167, 183185.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369373.CrossRefGoogle ScholarPubMed
Wenthold, R.J., Zemple, J.M., Parakkal, M.H., Reeks, K.A. & Altschuler, R.A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 718.CrossRefGoogle ScholarPubMed
Yang, C.Y. & Yazulla, S. (1988). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocyto-chemical and autoradiographical methods. Journal of Comparative Neurology 277, 96108.CrossRefGoogle Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 152.CrossRefGoogle Scholar
Yazulla, S. & Studholme, K.M. (1990). Multiple subtypes of glycine-immunoreactive neurons in the goldfish retina: Single- and double- label studies. Visual Neuroscience 4, 299309.CrossRefGoogle ScholarPubMed
Yazulla, S., Studholme, K.M. & Wu, J.-Y. (1986). Comparative distribution of [3H]-GABA uptake and GAD immunoreactivity in goldfish retinal amacrine cells: A double label analysis. Journal of Comparative Neurology 244, 149162.CrossRefGoogle ScholarPubMed
Young, R.W. (1977). The daily rhythm of shedding and degradation of cone outer segments in the lizard retina. Journal of Ultraslructural Research 61, 172185.CrossRefGoogle ScholarPubMed
Yu, B.C.-Y., Watt, C.B., Lam, D.M.K. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376382.CrossRefGoogle ScholarPubMed