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Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity
Open accessAbstract
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.
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“…(CR), calbindin (CB), tyrosine hydroxylase (TH), glutamic acid decarboxylase 65 (GAD65), choline acetyltransferase (ChAT), and nitric oxide synthase (NOS) (Pourcho and Goebel, 1985; Voigt, 1986; Brecha et al., 1988; Vaney and Young, 1988; Menger et al., 1998; Haverkamp and W€assle, 2000).”
Hendrickson, A. E., Tillakaratne, N. J. K., Mehra, R. D., Esclapez, M., Erickson, A., Vician, L. J., & Tobin, A. J. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903430407 · Cited by 52
Developmental changes in metabotropic glutamate receptor-mediated calcium homeostasis
Zirpel, L., Janowiak, M. A., Taylor, D. A., & Parks, T. N. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000522)421:1 · Cited by 41
The DAPI-3 amacrine cells of the rabbit retina
Wright, L. L., Macqueen, C. L., Elston, G. N., Young, H. M., Pow, D. V., & Vaney, D. I. (1997) · Visual Neuroscience · doi:10.1017/s0952523800012141 · Cited by 51
Dendritic spread and functional coverage of starburst amacrine cells
Keeley, P. W., Whitney, I. E., Raven, M. A., & Reese, B. E. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21518 · Cited by 50
“…contacts with one another, releasing GABA from varicosities that decorate a peripheral annulus of their dendritic fields (Millar and Morgan, 1987; Brecha et al., 1988; Mariani and Hersh, 1988; Vaney and Young, 1988; Famiglietti, 1991; O’Malley et al., 1992; Greferath et al., 1993; Lee and Zhou,…”
BackgroundDudás, B., Mihály, A., & Merchenthaler, I. (2000) · The Journal of comparative neurology · doi:10.1002/1096-9861(20001127)427:4 · Cited by 57
Quinoxalines block the mechanism of directional selectivity in ganglion cells of the rabbit retina.
Cohen, E. D., & Miller, R. F. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.4.1127 · Cited by 50
Dmitrieva, N. A., Strang, C. E., & Keyser, K. T. (2006) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.6a7116.2006 · Cited by 49
Poznański, R. R. (1992) · Bulletin of Mathematical Biology · doi:10.1007/bf02460658 · Cited by 49
Kisv�rday, Z. F., Cowey, A., Stoerig, P., & Somogyi, P. (1991) · Experimental Brain Research · doi:10.1007/bf00228951 · Cited by 49
“Thus cholinergic amacrine cells contain both GABA and its synthesizing enzyme glutamate decarboxylase (Vaney and Young 1988; Brecha et al. 1988) and they also release both GABA and ACh (O'Malley and Marshland 1989).”
BackgroundChiao, C., & Masland, R. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10509.2002 · Cited by 48
“This seemed important because, among other reasons, the direction-selective neurons of the turtle retina have certain differences (notably their distribution of preferred directions) from those of the rabbit ( Bowling, 1980 ).”
BackgroundInfluentialGrzywacz, N. M., Tootle, J. S., & Amthor, F. R. (1997) · Visual Neuroscience · doi:10.1017/s0952523800008749 · Cited by 48
Evidence that certain retinal bipolar cells use both glutamate and GABA
Kao, Y., Lassová, L., Bar‐Yehuda, T., Edwards, R. H., Sterling, P., & Vardi, N. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20221 · Cited by 46
“…or a catecholaminergic modulator a fast transmitter, such as dopamine glutamate (Sulzer and Rayport, 2000), or two fast transmitters, such as acetylcholine GABA (Brecha et al., 1988; Vaney and Young, 1988; O’Malley et al., 1992), or GABA glycine (Jonas et al., 1998; O’Brien and Berger, 1999).”
BackgroundStabilization of complex input-output functions in neural clusters formed by synapse selection
Kerszberg, M., Dehaene, S., & Changeux, J. (1992) · Neural Networks · doi:10.1016/0893-6080(92)90003-2 · Cited by 46
Chapter 7 GABAergic circuits in the mammalian retina
Freed, M. A. (1992) · Progress in brain research · doi:10.1016/s0079-6123(08)63611-0 · Cited by 45
Milam, A. H., Leeuw, A. M. D., Gaur, V. P., & Saari, J. C. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902960108 · Cited by 43
Brombas, A., de Croft, S., Cooper, E. J., & Williams, S. R. (2017) · Nature Communications · doi:10.1038/ncomms15683 · Cited by 42
Glutamate in Life and Death of Retinal Amacrine Cells*
Duarte, C. B., Ferreira, I. L., Santos, P. F., Carvalho, A. L., Agostinho, P. M., & Carvalho, A. P. (1998) · General Pharmacology The Vascular System · doi:10.1016/s0306-3623(97)00360-1 · Cited by 42
Somatostatin‐immunoreactive cells in the adult cat retina
White, C. A., Chalupa, L. M., Johnson, D., & Brecha, N. C. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902930111 · Cited by 42
Münch, T. A., & Werblin, F. S. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00628.2005 · Cited by 41
“If we allow only direct and electrogenic synapses between starburst cells (using nicotinic acetylcholine receptors, and GABAA and GABAC receptors), this seems indeed to be the case.”
BackgroundInfluential
Metadata
- Authors
- Brecha, N., Johnson, D., Peichl, L., & Wässle, H.
- Affiliations
- University of California, Los Angeles (US)
- ORCID
- Peichl, L
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1988-08
- Volume
- 85
- Issue
- 16
- Pages
- 6187-6191
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC281930
- OpenAlex
- W2019521144
- Cited by
- 225
- References
- 44
- Citations by year
- 2024: 6 · 2023: 2 · 2022: 2 · 2021: 6 · 2020: 7 · 2019: 1 · 2018: 3 · 2017: 5 · 2016: 5 · 2015: 4 · 2014: 2 · 2013: 4 · 2012: 6
- FWCI
- 4.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Eye Institute (R01EY004067, EY 04067)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Ophthalmology › Retinal Development and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- cholinergic amacrine cells, displaced amacrine cells, glutamic acid decarboxylase, GABA, choline acetyltransferase, retinal ganglion cells, receptive fields, acetylcholine, GABAergic inhibition, cholinergic inhibition, rabbit retina
- MeSH terms
- Acetylcholine, Animals, Choline O-Acetyltransferase, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Horseradish Peroxidase, Indoles, Parasympathetic Nervous System, Rabbits, Retina
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