Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-06T07:08:53.778Z Has data issue: false hasContentIssue false
  • English
  • Français

Analysis of the distribution of glycine and GABA in amacrine cells of the developing rabbit retina: A comparison with the ontogeny of a functional GABA transport system in retinal neurons

Published online by Cambridge University Press:  02 June 2009

Denise K. Crook  and
David V. Pow
Denise K. Crook
Affiliation:
Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, The University of Queensland, Brisbane, QLD 4072, Australia
David V. Pow
Affiliation:
Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, The University of Queensland, Brisbane, QLD 4072, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

The objectives of this study were to (1) determine whether the glycinergic and GABAergic amacrine cells in the developing rabbit retina were neurochemically distinct at birth, (2) determine if the ratio of GABAergic to glycinergic amacrine cells was constant during development, (3) determine whether the capacity to take up a GABA analogue was restricted to GABAergic neurons, and (4) whether initiation of GABA transport into GABAergic neurons preceded the presence of a content of GABA in these neurons. We have used a novel strategy to immunolocalize a non-endogenous GABA analogue, γ-vinyl GABA, which is taken up into neurons by a GABA transporter. Examination of serial semithin resin-embedded sections of neonatal rabbit retinae that had been immunolabelled for glycine, GABA or γ-vinyl GABA revealed that at 1 day postnatum, 60% of amacrine cells contain glycine but not GABA and did not accumulate γ-vinyl GABA, which is similar to the percentage of glycinergic amacrine cells in the adult retina. The vast majority of the remaining amacrine cells contained GABA and many also transported γ-vinyl GABA; however, a significant number of GABA-containing cells failed to accumulate γ-vinyl GABA suggesting that possession of a content of GABA did not have to be preceded by, or be concomitant with, the presence of a GABA transport system. By 10 days postnatum, over 99% of GABA-containing amacrine cells also transported γ-vinyl GABA indicating their functional maturity. Analysis of the horizontal cells revealed no evidence for uptake of γ-vinyl GABA, but another GABA analogue, diaminobutyric acid, which is a substrate both for the neuron-associated GABA transporter and the glial GABA transporter, was accumulated into some horizontal cells at 21 days postnatum, a time point when these cells also contain endogenous GABA. We conclude that amacrine cells are committed to being GABAergic or glycinergic at, or prior to birth, and that in some amacrine cells, expression of a content of GABA may occur prior to the capacity to transport GABA. Conversely, in some ganglion cells transport of γ-vinyl GABA may precede a content of GABA.

Keywords

DevelopmentGABAGlycineRetinaTransporter
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 751 - 763
Copyright
Copyright © Cambridge University Press 1997

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

Argadh, E. & Ehinger, B. (1982). [3H] muscimol, [3H] nipecotic acid and [3H] isoguavacine as autoradiographic markers for GABA neurotransmission. Journal of Neural Transmission 57, 1–18.Google Scholar
Brecha, N.C. & Weigmann, C. (1994). Expression of GAT-1, a high-affinity gamma-aminobutyric acid plasma membrane transporter in the rat retina. Journal of Comparative Neurology 345, 602–611.CrossRefGoogle ScholarPubMed
Cherubini, E., Gaiarsa, J.L. & Ben-Ari, A. (1991). GABA: An excitatory transmitter in early postnatal life. Trends in Neuroscience 14, 515–519.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Miller, R.F. (1981 a). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. I. Receptors, horizontal, and bipolar cells. Journal of Comparative Neurology 198, 307–326.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Miller, R.F. (1981 b). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. Journal of Comparative Neurology 198, 327–334.CrossRefGoogle ScholarPubMed
Ehinger, B. (1977). Glial and neuronal uptake of GABA, glutamic acid, glutamine and glutathione in the rabbit retina. Experimental Eye Research 25, 221–234.CrossRefGoogle ScholarPubMed
Fung, S.-K., Kong, Y.-U. & Lam, D.M.-K. (1982). Prenatal development of GABAergic, glycinergic, and dopaminergic neurons in the rabbit retina. Journal of Neuroscience 2, 1623–1632.CrossRefGoogle ScholarPubMed
Gordon-Weeks, P.R., Lockerbie, R.O. & Pearce, B.R. (1984). Uptake and release of [3H]GABA by growth cones isolated from the neonatal rat brain. Neuroscience Letters 52, 205–210.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1982). Embryogenesis of the rabbit retina. Experimental Eye Research 34, 749–765.CrossRefGoogle ScholarPubMed
Ikegaki, N., Saito, N., Hashima, M. & Tanaka, C. (1994). Production of specific antibodies against GABA transporter subtypes (GAT1, GAT2, GAT3) and their application to immunocytochemistry. Molecular Brain Research 26, 47–54.CrossRefGoogle ScholarPubMed
Iverson, L.L. & Kelly, J.S. (1975). Uptake and metabolism of γ-aminobutyric acid by neurones and glial cells. Biochemical Pharmacology 24, 933–938.CrossRefGoogle Scholar
Jäger, J. & Wässle, H. (1987). Localization of glycine uptake and receptors in the cat retina. Neuroscience Letters 75, 147–151.CrossRefGoogle ScholarPubMed
Kong, Y.-C., Fung, S.-C. & Lam, D.M.-K. (1980). Postnatal development of glycinergic neurons in the rabbit retina. Journal of Comparative Neurology 193, 1127–1135.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, 89–102.Google ScholarPubMed
Lauder, J.M. (1993). Neurotransmitters as growth regulatory signals: Role of receptors and second messengers. Trends in Neuroscience 16, 233–240.CrossRefGoogle ScholarPubMed
Lipton, S.A. & Kater, S.B. (1989). Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends in Neuroscience 7, 265–270.CrossRefGoogle Scholar
Ma, W., Behar, T. & Barker, J.L. (1992). Transient expression of GABA immunoreactivity in the developing rat spinal cord. Journal of Comparative Neurology 325, 271–290.CrossRefGoogle ScholarPubMed
Madtes, P.C. Jr. & Redburn, D.A. (1982). [3H]-GABA binding in developing rabbit retina. Neurochemical Research 7, 495–503.CrossRefGoogle Scholar
Madtes, P.C. Jr. & Redburn, D.A. (1983 a). GABA as a trophic factor during development. Life Sciences 33, 979–984.CrossRefGoogle ScholarPubMed
Madtes, P.C. Jr. & Redburn, D.A. (1983 b). Synaptic interactions in the GABA system during postnatal development in retina. Brain Research Bulletin 10, 741–745.CrossRefGoogle ScholarPubMed
Marc, R.E. & Liu, W.-L.S. (1985). [3H] glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241–260.CrossRefGoogle ScholarPubMed
Masland, R.H. (1977). Maturation of function in the developing rabbit retina. Journal of Comparative Neurology 175, 275–286.CrossRefGoogle ScholarPubMed
McArdle, C.B., Dowling, J.E. & Masland, R.H. (1977). Development of outer segments and synapses in the rabbit retina. Journal of Comparative Neurology 175, 253–274.CrossRefGoogle ScholarPubMed
Messersmith, E.K. & Redburn, D.A. (1992). Gamma-aminobutyric acid immunoreactivity in multiple cells types of the developing rabbit retina. Visual Neuroscience 9, 201–211.CrossRefGoogle Scholar
Mossinger, J. & Yazulla, S. (1987). Double-label analysis of GAD- and GABA-like immunoreactivity in the rabbit retina. Vision Research 27, 23–30.CrossRefGoogle Scholar
Neal, M.J., Cunningham, J.R., Shah, M.A. & Yazulla, S. (1989). Immunocytochemical evidence that vigabatrin in rats causes GABA accumulation in glial cells of the retina. Neuroscience Letters 13, 29–32.CrossRefGoogle Scholar
Osborne, N.N., Patel, S., Beaton, D.W. & Neuhoff, V. (1986). GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell and Tissue Research 243, 117–123.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). A combined golgi and autoradio-graphie study of 3H-glycine-accumuIating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 1178–1188.CrossRefGoogle ScholarPubMed
Pow, D.V., Baldridge, W. & Crook, D.K. (1996). Activity-dependent transport of GABA analogues into specific cell types demonstrated at high resolution using a novel immunocytochemical strategy. Neuroscience 73, 1129–1143.CrossRefGoogle ScholarPubMed
Pow, D.V. & Crook, O.K. (1993). Extremely high titre polyclonal antisera against small neurotransmitter molecules: Rapid production, characterisation and use in light- and electron-microscopic immunocytochemistry. Journal of Neuroscience Methods 48, 51–63.CrossRefGoogle ScholarPubMed
Pow, D.V. & Crook, D.K. (1994). Rapid post-mortem changes in the cellular localisation of amino acid transmitters in the retina as assessed by immunocytochemistry. Brain Research 653, 199–209.CrossRefGoogle Scholar
Pow, D.V., Crook, D.K. & Wong, R.O.L. (1994). Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immunocytochemical study. Visual Neuroscience 11, 1115–1134.CrossRefGoogle ScholarPubMed
Pow, D.V. & Rogers, P.C. (1996). GABA transamination regulates neuronal glutamate content in the retina. NeuroReport 7, 2683–2686.CrossRefGoogle ScholarPubMed
Pow, D.V. & Robinson, S.R. (1994). Glutamate in some retinal neurones is derived solely from glia. Neuroscience 60, 355–366.CrossRefGoogle ScholarPubMed
Preston, J.E., al-Sarraf, H. & Segal, M.B. (1995). Permeability of the developing blood-brain barrier to 14C-mannitol using the rat in situ brain perfusion technique. Brain Research Developmental Brain Research 87, 69–76.CrossRefGoogle ScholarPubMed
Redburn, D.A. (1992). Development of GABAergic neurons in the mammalian retina. Progress in Brain Research 90, 133–147.CrossRefGoogle ScholarPubMed
Redburn, D.A. & Madtes, P. Jr. (1986). Postnatal development of 3H-GABA-accumulating cells in rabbit retina. Journal of Comparative Neurology 243, 41–57.CrossRefGoogle ScholarPubMed
Redburn, D.A. & Madtes, P. Jr. (1988). GABA—its role and development in retina. Progress in Retinal Research 6, 69–84.CrossRefGoogle Scholar
Robinson, S.R. (1991). Development of the mammalian retina. In Neuro-anatomy of the Visual Pathways and Their Development, ed. Dreher, B. & Robinson, S.R., pp. 69–128. U.K.: The MacMillan Press.Google Scholar
Rogers, P.C. & Pow, D.V. (1995). Immunocytochemical evidence for an axonal localization of GABA in the optic nerves of rabbits, rats, and cats. Visual Neuroscience 12, 1143–1149.CrossRefGoogle Scholar
Schnitzer, J. & Rusoff, A.C. (1984). Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. Journal of Neuroscience 4, 2948–2955.CrossRefGoogle ScholarPubMed
Tian, Y., Kapatos, G., Grannemann, J.G. & Bannon, M.J. (1994). Dopamine and γ-aminobutyric acid transporters: Differential regulation by agents that promote phosphorylation. Neuroscience Letters 173, 143–146.CrossRefGoogle ScholarPubMed
Versauz-Botteri, C., Pochet, R. & Nguyen-Legros, J. (1989). Immu-nohistochemical localization of GABA-containing neurons during postnatal development of the rat retina. Investigative Ophthalmology and Visual Science 30, 652–659.Google Scholar
Wässle, H., Schäfer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. Journal of Neuroscience 6, 594–604.CrossRefGoogle ScholarPubMed
Wright, L.L., Pow, D.V. & Vaney, D.I. (1996). A quantitative immunocytochemical analysis of the distribution of glycinergic and GABAergic amacrine cells in wholemount rabbit retina. Proceedings of the Australian Neuroscience Society 7, 213.Google Scholar
Yazulla, S. (1991). The mismatch problem for GABAergic amacrine cells in goldfish retina: Resolution and other issues. Neurochemical Research 16, 327–339.CrossRefGoogle ScholarPubMed
YuB.-C., W., B.B. B.-C., W., B.B., Lam, D.M.K. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376–382.CrossRefGoogle ScholarPubMed