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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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Hamassaki‐Britto, D. E., Brzozowska‐Prechtl, A., Karten, H. J., Lindstrom, J. M., & Keyser, K. T. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903130213 · Cited by 31
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“Whenever a SAC dendritic tip becomes sufficiently depolarized, it is assumed to release GABA (Brecha et al. 1988; O’Malley et al. 1992; Vaney and Young 1988), which binds to GABAA receptors (Brandstatter et al. 1995) and opens Cl− channels in postsynaptic SAC dendrites.”
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“In addition to the inhibitory neurotransmitter, some AC subtypes co-release an excitatory neurotransmitter—for example, glycine and glutamate (Haverkamp and Wässle, 2004; Johnson et al., 2004; Lee et al., 2014) or GABA and acetylcholine (Brecha et al., 1988; Vaney and Young, 1988).”
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InfluentialCholinergic amacrine cells of the rat retina express the δ-subunit of the GABAA-receptor
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InfluentialKIAA0369, doublecortin-like kinase, is expressed during brain development
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Distribution of 3H‐GABA uptake sites in the nematode Ascaris
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“Starburst amacrine cells also contain and release GABA ~Brecha et al., 1988; O’Malley & Masland, 1989!.”
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Gregg, R. G., McCall, M. A., & Massey, S. C. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4557-0737-9.00015-1 · Cited by 23
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Cholinergic amacrine cells in the rabbit retina accumulate muscimol
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Chapter 8 What do amacrine cells do?
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“In the retina, ACh is released by a single population of amacrine cells: the GABAergic/cholinergic starburst amacrine cell (Brecha et al. 1988; O’Malley & Masland, 1989; Lee et al. 2010).”
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“GABAergic markers have occasionally also been localised to horizontal, bipolar, interplexiform and ganglion cells in various species (Morgan 1985; Yazulla 1986; Brecha 1992; Freed 1992; Marc 1992).”
BackgroundMorphologies of Somatostatin-Immunoreactive Neurons in the Rabbit Retina
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Development of starburst cholinergic amacrine cells in the retina of Tupaia belangeri
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“(Brecha et al. 1988), later by evidence that axon terminals in visual cortex contain both acetylcholine and GABA”
Stimulus-dependent engagement of neural mechanisms for reliable motion detection in the mouse retina
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“On the other hand, neurotransmitters GABA and ACh are released from varicosities in the outer third of SAC dendritic arbors in both rabbits and rodents (Brecha et al. 1988; Famiglietti 1991; Kosaka et al. 1988; O’Malley and Masland 1989; Vaney and Young 1988).”
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Applications of DAPI Cytochemistry to Neurobiology
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“The Γ2 theme class (magenta) was classified as cholinergic amacrine cells based on containing high GABA content amongst GABAergic amacrine theme classes and a high prevalence in the GCL (Brecha et al., 1988; Jeon et al., 1998).”
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“…in sympathetic preganglionic neurons (Ito et al., 2005, 2007) and in specific central neurons, such as starburst amacrine cells in the retina (Brecha et al., 1988; Kosaka et al., 1988; Vaney & Young, 1988) and cerebral interneurons (Kosaka et al., 1988; Bayraktar et al., 1997; von Engelhardt…”
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Receptoral Mechanisms for Fast Cholinergic Transmission in Direction-Selective Retinal Circuitry
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“…with DS GCs and their utilization of the neurotransmitters ACh and GABA (Famiglietti, 1981; Ariel & Daw, 1982b; Famiglietti, 1983b; Masland et al., 1984; Tauchi &Masland, 1984; Famiglietti & Tumosa, 1987; Brecha et al., 1988; Famiglietti, 1991), as well as their DS responses (Euler et al., 2002).”
BackgroundInfluentialGABA content in the retina of pigmented and albino rats
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“1988), and that in the retina GABAergic neurons may also contain other neurotransmitters such as acetylcholine or dopamine (Brecha et al. 1988; Kosaka et al. 1988; W/issle and Chun 1988), it is possible that the same cell may express different transmitters at different times during development.”
BackgroundThe Physiology and Morphology of the Vertebrate Retina
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Photoreceptor degeneration and loss of immunoreactive GABA in the Abyssinian cat retina
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“In the mammalian retina cholinergic amacrine cells have been shown to synthesize, store and release GABA as well as acetylcholine (Brecha et al. 1988; Kosaka et al. 1988) and most of the displaced GABAergic amacrines represent ON-cholinergic cells, whose dendrites extend and stratify within…”
BackgroundOrganization and Development of Sparsely Distributed Wide-Field Amacrine Cells in the Rabbit Retina
Brecha, N. C., Casini, G., & Rickman, D. W. (1991) · Springer eBooks · doi:10.1007/978-1-4615-3390-0_8 · Cited by 12
Cone and rod cells have different target preferences in vitro as revealed by optical tweezers.
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Heterogeneity of receptor immunoreactivity at synapses of glycine-utilizing neurons
Zucker, C. L., & Ehinger, B. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0088 · Cited by 11
Characterization of adenosine A1-receptor binding sites in bovine retinal membranes
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Li, Y., Yu, S., Jia, X., Qiu, X., & He, J. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002506 · Cited by 9
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Colocalization of glycine in substance P-amacrine cells of the larval tiger salamander retina
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The Effect of Low-Dose Atropine on Alpha Ganglion Cell Signaling in the Mouse Retina
Wang, Q., Banerjee, S., So, C., Qiu, C., Sze, Y. H., Lam, T. C., To, C. H., & Pan, F. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.664491 · Cited by 9
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The Release of Acetylcholine and Gaba by Neurons of the Rabbit Retina
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“Because they also contain GABA [38,39], SACs could provide GABAergic feedback to bipolar cells and feedforward to RGCs during glutamatergic waves.”
BackgroundMathematical analysis and modeling of motion direction selectivity in the retina
Escobar, M.-J., Pezo, D., & Orio, P. (2013) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2013.08.003 · Cited by 8
“At these outputs, SACs are particularly characterized by being the only neurons in the retina to release two types of neurotransmitters, that is, an excitatory (Ach) and an inhibitory (GABA) type (Vaney and Young, 1988; Brecha et al., 1988).”
BackgroundMost calretinin-containing amacrine cells in the rabbit retina co-localize glycine
Gabriel, R., Völgyi, B., & Pollák, E. (1999) · Visual Neuroscience · doi:10.1017/s095252389916601x · Cited by 8
“To take this observation one step further, we tried to determine whether these GABA10calretinin1 neurons corresponded to any of the formerly identified GABA-positive amacrine cell subtypes (Osborne & Beaton, 1986; Brecha et al., 1988; Vaney & Young, 1988 a,b; Casini & Brecha, 1992) (Table 3).”
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Nitric oxide inhibits the release of acetylcholine in the isolated retina
Okada, M., Osumi, Y., Okuma, Y., & Ueno, H. (2001) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s004170100274 · Cited by 7
“co-localizes with ACh in cholinergic amacrine cells [2, 9, 22], and inhibits the release of ACh [12].”
Background
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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