Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity
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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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“Colocalization of SV2A and SV2C was observed in the plexes formed in the IPL by the ON- and OFF-center starburst amacrine cells, identified by labeling for ChAT and GABA (Brecha et al., 1988; Vaney and Young, 1988; O’Malley and Masland, 1989).”
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Origins of direction selectivity in the primate retina
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Receptive Field Properties of Starburst Cholinergic Amacrine Cells in the Rabbit Retina
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Cation–chloride cotransporters mediate neural computation in the retina
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Expression of neuropeptides and their receptors in the developing retina of mammals.
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Direction selectivity in the retina
Vaney, D. I. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00337-9 · Cited by 73 · see citing works
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Chapter 4 Structural organization of GABAergic circuitry in ectotherm retinas
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Stimulus-dependent recruitment of lateral inhibition underlies retinal direction selectivity
Chen, Q., Pei, Z., Koren, D., & Wei, W. (2016) · eLife · doi:10.7554/elife.21053 · Cited by 63 · see citing works
“SACs are monostratified, axonless interneurons that release GABA and acetylcholine from varicosities at the distal ends of their dendritic arbors (Brecha et al., 1988; Famiglietti, 1991; Kosaka et al., 1988; O’Malley and Masland, 1989; Vaney and Young, 1988).”
BackgroundSynaptic physiology of direction selectivity in the retina
Zhou, Z., & Lee, S. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.159020 · Cited by 67 · see citing works
“Because SACs contain and release not only ACh, but also GABA (Brecha et al. 1988; Vaney & Young, 1988; O’Malley & Masland, 1989), they have long been proposed as a likely source of the critical lateral inhibition to DSGCs (Vaney, 1990; Borg-Graham & Grzywacz, 1992).”
BackgroundDopaminergic and GABAergic retinal cell populations in mammals
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“Cholinergic amacrine cells contain and release GABA (Brecha et al., 1988; Vaney and Young, 1988; O'Malley and Masland, Figure 7.”
Tetrodotoxin‐resistant voltage‐gated sodium channels Nav1.8 and Nav1.9 are expressed in the retina
O’Brien, B. J., Caldwell, J. H., Ehring, G. R., O’Brien, K. M. B., Luo, S., & Levinson, S. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21701 · Cited by 64 · see citing works
“GABA immunostaining labeled a large proportion of the cells in the inner half of the inl, including the Nav1.”
BackgroundInfluentialNeurotransmitter receptors of starburst amacrine cells in rabbit retinal slices
Zhou, Z., & Fain, G. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05334.1995 · Cited by 61 · see citing works
“Starburst cells have also been shown to contain and release GABA (Brecha et al., 1988; Kosaka, et al., 1988; Vaney and Young, 1988; O’Malley and Masland, 1989), although a light-evoked release of GABA has not been demonstrated (O’Malley and Masland, 1989).”
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Co-stratification of GABAA receptors with the directionally selective circuitry of the rat retina
Brandstätter, J. H., Greferath, U., Euler, T., & Wässle, H. (1995) · Visual Neuroscience · doi:10.1017/s0952523800008026 · Cited by 60 · see citing works
Vaney, D. I., Collin, S. P., & Young, H. M. (1989) · Springer eBooks · doi:10.1007/978-3-642-74149-4_13 · Cited by 60 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Receptor targets of amacrine cells
Zhang, C., & McCall, M. A. (2012) · Visual Neuroscience · doi:10.1017/s0952523812000028 · Cited by 59 · see citing works
“Shortly thereafter, these cholinergic amacrine cells also were shown to express GABA or its synthetic enzyme, glutamic acid decarboxylase (Brecha et al., 1988; Kosaka et al., 1988; Vaney & Young, 1988).”
BackgroundGabriel, R., & Witkovsky, P. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00323-1 · Cited by 59 · see citing works
Chen, M., Weng, S.-J., Deng, Q., Xu, Z., & He, S. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.161240 · Cited by 58 · see citing works
“Blockade of GABAA receptors abolishes direction selectivity in DSGCs (Caldwell & Daw, 1978).”
BackgroundInfluentialSynaptic input to the on–off directionally selective ganglion cell in the rabbit retina
Dacheux, R. F., Chimento, M. F., & Amthor, F. R. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10521 · Cited by 57 · see citing works
“Conflicting evidence always opens the possibility that other unidentified GABAergic and/or glycinergic amacrine cells may be involved with the DS cell.”
BackgroundInfluentialCalretinin in neurochemically well-defined cell populations of rabbit retina
Völgyi, B., Pollák, E., Buzás, P., & Gabriel, R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00405-8 · Cited by 56 · see citing works
Transport-Mediated Synapses in the Retina
Schwartz, E. A. (2002) · Physiological Reviews · doi:10.1152/physrev.00010.2002 · Cited by 56 · see citing works
“Thus it was puzzling when immunohistochemistry revealed a high GABA concentration in their cytoplasm (18, 68, 144).”
BackgroundMassey, S. C., Linn, D. M., Kittila, C. A., & Mirza, W. (1997) · Visual Neuroscience · doi:10.1017/s0952523800011652 · Cited by 56 · see citing works
Direction-Selective Ganglion Cells in the Retina
Vaney, D. I., He, S., Taylor, W. R., & Levick, W. R. (2001) · Springer eBooks · doi:10.1007/978-3-642-56550-2_2 · Cited by 55 · see citing works
Cross-compartmental Modulation of Dendritic Signals for Retinal Direction Selectivity
Koren, D., Grove, J. C. R., & Wei, W. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.020 · Cited by 49 · see citing works
Chapter 1 Expression of GABAA receptors in the vertebrate retina
Brecha, N. C. (1992) · Progress in brain research · doi:10.1016/s0079-6123(08)63606-7 · Cited by 55 · see citing works
Akopian, A., Kumar, S., Ramakrishnan, H., Viswanáthan, S., & Bloomfield, S. A. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24074 · Cited by 52 · see citing works
“…(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 · see citing works
Architectonic analysis of the human retrosplenial cortex
Morris, R., Paxinos, G., & Petrides, M. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000522)421:1 · Cited by 43 · see citing works
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 · see citing works
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 · see citing works
“…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,…”
BackgroundCholine acetyltransferase-immunoreactive neurons in the developing rat retina
Kim, I., Lee, E.-J., Kim, M.-K., Park, D., & Chun, M. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001127)427:4 · Cited by 50 · see citing works
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 · see citing works
Dmitrieva, N. A., Strang, C. E., & Keyser, K. T. (2006) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.6a7116.2006 · Cited by 49 · see citing works
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“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 · see citing works
“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 ).”
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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 · see citing works
“…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
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Chapter 7 GABAergic circuits in the mammalian retina
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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 · see citing works
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 · see citing works
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“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
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › 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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