Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Aug;85(16):6187–6191. doi: 10.1073/pnas.85.16.6187

Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity.

N Brecha 1, D Johnson 1, L Peichl 1, H Wässle 1
PMCID: PMC281930  PMID: 3413087

Abstract

The transmitters acetylcholine and gamma-aminobutyrate (GABA) play critical roles in the formation of receptive-field properties of retinal ganglion cells. In rabbit retina, cholinergic amacrine and displaced amacrine cells were identified by immunohistochemical staining for the enzyme choline acetyltransferase and by their avid accumulation of the fluorescent dye 4',6-diamidino-2-phenylindole. Several GABA-immunoreactive and glutamate decarboxylase-immunoreactive cell types, including a prominent population of small, round amacrine and displaced amacrine cells, were also identified. Double-label experiments demonstrated that all amacrine and displaced amacrine cells that prominently accumulate 4',6-diamidino-2-phenylindole contain GABA and glutamate decarboxylase immunoreactivity. However, not all GABA-immunoreactive cells accumulate this dye. Quantitative analysis of the ganglion cell layer of whole mount preparations of the retina showed that choline acetyltransferase-immunoreactive cells and the majority of GABA-immunoreactive cells have a small, round shape and similar cell density profiles that parallel that of displaced amacrine cells. These studies establish that cholinergic cells are a major subpopulation of GABA-immunoreactive amacrine and displaced amacrine cells. The role these cells have in the formation of ganglion cell receptive-field properties may be parsimoniously explained by an excitatory postsynaptic action mediated by acetylcholine and an inhibitory presynaptic action mediated by GABA.

Full text

PDF
6187

Images in this article

6188Image
on p.6188
6189Image
on p.6189
6189Image
on p.6189

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agardh E., Bruun A., Ehinger B., Ekström P., van Veen T., Wu J. Y. Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. J Comp Neurol. 1987 Apr 22;258(4):622–630. doi: 10.1002/cne.902580411. [DOI] [PubMed] [Google Scholar]
  2. Agardh E., Ehinger B. Retinal GABA neuron labelling with [3H]isoguvacine in different species. Exp Eye Res. 1983 Feb;36(2):215–229. doi: 10.1016/0014-4835(83)90007-6. [DOI] [PubMed] [Google Scholar]
  3. Ariel M., Daw N. W. Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. J Physiol. 1982 Mar;324:135–160. doi: 10.1113/jphysiol.1982.sp014104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ariel M., Daw N. W. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J Physiol. 1982 Mar;324:161–185. doi: 10.1113/jphysiol.1982.sp014105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baughman R. W., Bader C. R. Biochemical characterization and cellular localization of the cholinergic system in the chicken retina. Brain Res. 1977 Dec 23;138(3):469–485. doi: 10.1016/0006-8993(77)90684-9. [DOI] [PubMed] [Google Scholar]
  6. Brandon C. Cholinergic neurons in the rabbit retina: immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Res. 1987 Jan 20;401(2):385–391. doi: 10.1016/0006-8993(87)91426-0. [DOI] [PubMed] [Google Scholar]
  7. Brandon C., Lam D. M., Wu J. Y. The gamma-aminobutyric acid system in rabbit retina: localization by immunocytochemistry and autoradiography. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3557–3561. doi: 10.1073/pnas.76.7.3557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brandon C. Retinal GABA neurons: localization in vertebrate species using an antiserum to rabbit brain glutamate decarboxylase. Brain Res. 1985 Oct 7;344(2):286–295. doi: 10.1016/0006-8993(85)90806-6. [DOI] [PubMed] [Google Scholar]
  9. Brecha N., Johnson D., Bolz J., Sharma S., Parnavelas J. G., Lieberman A. R. Substance P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit. Nature. 1987 May 14;327(6118):155–158. doi: 10.1038/327155a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Caldwell J. H., Daw N. W., Wyatt H. J. Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J Physiol. 1978 Mar;276:277–298. doi: 10.1113/jphysiol.1978.sp012233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chesselet M. F. Presynaptic regulation of neurotransmitter release in the brain: facts and hypothesis. Neuroscience. 1984 Jun;12(2):347–375. doi: 10.1016/0306-4522(84)90058-7. [DOI] [PubMed] [Google Scholar]
  12. Cunningham J. R., Neal M. J. Effect of gamma-aminobutyric acid agonists, glycine, taurine and neuropeptides on acetylcholine release from the rabbit retina. J Physiol. 1983 Mar;336:563–577. doi: 10.1113/jphysiol.1983.sp014598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ehinger B., Falck B. Autoradiography of some suspected neurotransmitter substances: GABA glycine, glutamic acid, histamine, dopamine, and L-dopa. Brain Res. 1971 Oct 8;33(1):157–172. doi: 10.1016/0006-8993(71)90314-3. [DOI] [PubMed] [Google Scholar]
  14. Famiglietti E. V., Jr 'Starburst' amacrine cells and cholinergic neurons: mirror-symmetric on and off amacrine cells of rabbit retina. Brain Res. 1983 Feb 14;261(1):138–144. doi: 10.1016/0006-8993(83)91293-3. [DOI] [PubMed] [Google Scholar]
  15. Hayden S. A., Mills J. W., Masland R. M. Acetylcholine synthesis by displaced amacrine cells. Science. 1980 Oct;210(4468):435–437. doi: 10.1126/science.7433984. [DOI] [PubMed] [Google Scholar]
  16. Houser C. R., Crawford G. D., Barber R. P., Salvaterra P. M., Vaughn J. E. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res. 1983 Apr 25;266(1):97–119. doi: 10.1016/0006-8993(83)91312-4. [DOI] [PubMed] [Google Scholar]
  17. Hughes A., Vaney D. I. Coronate cells: displaced amacrines of the rabbit retina? J Comp Neurol. 1980 Jan 1;189(1):169–189. doi: 10.1002/cne.901890110. [DOI] [PubMed] [Google Scholar]
  18. Hutchins J. B. Acetylcholine as a neurotransmitter in the vertebrate retina. Exp Eye Res. 1987 Jul;45(1):1–38. doi: 10.1016/s0014-4835(87)80075-1. [DOI] [PubMed] [Google Scholar]
  19. Hökfelt T., Johansson O., Ljungdahl A., Lundberg J. M., Schultzberg M. Peptidergic neurones. Nature. 1980 Apr 10;284(5756):515–521. doi: 10.1038/284515a0. [DOI] [PubMed] [Google Scholar]
  20. Johnson C. D., Epstein M. L. Monoclonal antibodies and polyvalent antiserum to chicken choline acetyltransferase. J Neurochem. 1986 Mar;46(3):968–976. doi: 10.1111/j.1471-4159.1986.tb13064.x. [DOI] [PubMed] [Google Scholar]
  21. Kosaka T., Kosaka K., Hataguchi Y., Nagatsu I., Wu J. Y., Ottersen O. P., Storm-Mathisen J., Hama K. Catecholaminergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res. 1987;66(1):191–210. doi: 10.1007/BF00236215. [DOI] [PubMed] [Google Scholar]
  22. Masland R. H., Ames A., 3rd Responses to acetylcholine of ganglion cells in an isolated mammalian retina. J Neurophysiol. 1976 Nov;39(6):1220–1235. doi: 10.1152/jn.1976.39.6.1220. [DOI] [PubMed] [Google Scholar]
  23. Masland R. H., Livingstone C. J. Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. J Neurophysiol. 1976 Nov;39(6):1210–1219. doi: 10.1152/jn.1976.39.6.1210. [DOI] [PubMed] [Google Scholar]
  24. Masland R. H., Mills J. W. Autoradiographic identification of acetylcholine in the rabbit retina. J Cell Biol. 1979 Oct;83(1):159–178. doi: 10.1083/jcb.83.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Masland R. H., Mills J. W., Cassidy C. The functions of acetylcholine in the rabbit retina. Proc R Soc Lond B Biol Sci. 1984 Nov 22;223(1230):121–139. doi: 10.1098/rspb.1984.0086. [DOI] [PubMed] [Google Scholar]
  26. Masland R. H., Mills J. W., Hayden S. A. Acetylcholine-synthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proc R Soc Lond B Biol Sci. 1984 Nov 22;223(1230):79–100. doi: 10.1098/rspb.1984.0084. [DOI] [PubMed] [Google Scholar]
  27. Massey S. C., Neal M. J. The light evoked release of acetylcholine from the rabbit retina iN vivo and its inhibition by gamma-aminobutyric acid. J Neurochem. 1979 Apr;32(4):1327–1329. doi: 10.1111/j.1471-4159.1979.tb11062.x. [DOI] [PubMed] [Google Scholar]
  28. Massey S. C., Redburn D. A. A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. J Neurosci. 1982 Nov;2(11):1633–1643. doi: 10.1523/JNEUROSCI.02-11-01633.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Massey S. C., Redburn D. A. Light evoked release of acetylcholine in response to a single flash: cholinergic amacrine cells receive ON and OFF input. Brain Res. 1985 Mar 4;328(2):374–377. doi: 10.1016/0006-8993(85)91052-2. [DOI] [PubMed] [Google Scholar]
  30. Matute C., Streit P. Monoclonal antibodies demonstrating GABA-like immunoreactivity. Histochemistry. 1986;86(2):147–157. doi: 10.1007/BF00493380. [DOI] [PubMed] [Google Scholar]
  31. Mosinger J. L., Yazulla S. Colocalization of GAD-like immunoreactivity and 3H-GABA uptake in amacrine cells of rabbit retina. J Comp Neurol. 1985 Oct 22;240(4):396–406. doi: 10.1002/cne.902400407. [DOI] [PubMed] [Google Scholar]
  32. Mosinger J. L., Yazulla S., Studholme K. M. GABA-like immunoreactivity in the vertebrate retina: a species comparison. Exp Eye Res. 1986 Jun;42(6):631–644. doi: 10.1016/0014-4835(86)90052-7. [DOI] [PubMed] [Google Scholar]
  33. Oertel W. H., Schmechel D. E., Tappaz M. L., Kopin I. J. Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience. 1981;6(12):2689–2700. doi: 10.1016/0306-4522(81)90113-5. [DOI] [PubMed] [Google Scholar]
  34. Schmidt M., Wässle H., Humphrey M. Number and distribution of putative cholinergic neurons in the cat retina. Neurosci Lett. 1985 Sep 6;59(3):235–240. doi: 10.1016/0304-3940(85)90137-5. [DOI] [PubMed] [Google Scholar]
  35. Storm-Mathisen J., Leknes A. K., Bore A. T., Vaaland J. L., Edminson P., Haug F. M., Ottersen O. P. First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature. 1983 Feb 10;301(5900):517–520. doi: 10.1038/301517a0. [DOI] [PubMed] [Google Scholar]
  36. Tauchi M., Masland R. H. The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc R Soc Lond B Biol Sci. 1984 Nov 22;223(1230):101–119. doi: 10.1098/rspb.1984.0085. [DOI] [PubMed] [Google Scholar]
  37. Vaney D. I. 'Coronate' amacrine cells in the rabbit retina have the 'starburst' dendritic morphology. Proc R Soc Lond B Biol Sci. 1984 Feb 22;220(1221):501–508. doi: 10.1098/rspb.1984.0016. [DOI] [PubMed] [Google Scholar]
  38. Vaney D. I. A quantitative comparison between the ganglion cell populations and axonal outflows of the visual streak and periphery of the rabbit retina. J Comp Neurol. 1980 Jan 15;189(2):215–233. doi: 10.1002/cne.901890202. [DOI] [PubMed] [Google Scholar]
  39. Vaney D. I., Peichi L., Boycott B. B. Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. J Comp Neurol. 1981 Jul 1;199(3):373–391. doi: 10.1002/cne.901990305. [DOI] [PubMed] [Google Scholar]
  40. Vaney D. I., Peichl L., Wässle H., Illing R. B. Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Res. 1981 May 18;212(2):447–453. doi: 10.1016/0006-8993(81)90476-5. [DOI] [PubMed] [Google Scholar]
  41. Voigt T. Cholinergic amacrine cells in the rat retina. J Comp Neurol. 1986 Jun 1;248(1):19–35. doi: 10.1002/cne.902480103. [DOI] [PubMed] [Google Scholar]
  42. Wässle H., Chun M. H., Müller F. Amacrine cells in the ganglion cell layer of the cat retina. J Comp Neurol. 1987 Nov 15;265(3):391–408. doi: 10.1002/cne.902650308. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES