The DOI matches its Crossref record; 68 of the 68 references it cites were found in a registry or an index.
Role of ACh-GABA Cotransmission in Detecting Image Motion and Motion Direction
Open accessAbstract
Starburst amacrine cells (SACs) process complex visual signals in the retina using both acetylcholine (ACh) and gamma-aminobutyric acid (GABA), but the synaptic organization and function of ACh-GABA corelease remain unclear. Here, we show that SACs make cholinergic synapses onto On-Off direction-selective ganglion cells (DSGCs) from all directions but make GABAergic synapses onto DSGCs only from the null direction. ACh and GABA were released differentially in a Ca(2+) level-specific manner, suggesting the two transmitters were released from different vesicle populations. Despite the symmetric cholinergic connection, the light-evoked cholinergic input to a DSGC, detected at both light onset and offset, was motion- and direction-sensitive. This input was facilitated by two-spot apparent motion in the preferred direction but supressed in the null direction, presumably by a GABAergic mechanism. The results revealed a high level of synaptic intricacy in the starburst circuit and suggested differential, yet synergistic, roles of ACh-GABA cotransmission in motion sensitivity and direction selectivity.
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“These studies suggest that Ach and GABA are segregated into different synaptic vesicles and/or axonal boutons to endow single SACs with spatial selectivity over cotransmission of neurotransmitters.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [86]
Experimental — accuracy not yet measuredIn the citing paper
“More recently, an elegant study employing paired recordings from neighboring retinal neurons demonstrated monosynaptic transmission of both Ach and GABA from SACs to direction-sensitive retinal ganglion cells (DSGCs).86”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [86]
In the citing paper
“Ach and GABA release are differentially sensitive to calcium concentration and calcium channel antagonists, suggesting separate vesicle populations.86”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [86]
In the citing paper
“Release of GABA from SACs is restricted to the dendrites of the postsynaptic DSGCs' null direction, whereas release of Ach is not spatially restricted.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [86]
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Citations
Cites
Short-Term Synaptic Plasticity
Zucker, R. S., & Regehr, W. G. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.092501.114547 · Cited by 5,068
Corelease of Two Fast Neurotransmitters at a Central Synapse
Jonas, P., Bischofberger, J., & Sandkühler, J. (1998) · Science · doi:10.1126/science.281.5375.419 · Cited by 784
Directionally selective calcium signals in dendrites of starburst amacrine cells
Euler, T., Detwiler, P. B., & Denk, W. T. (2002) · Nature · doi:10.1038/nature00931 · Cited by 588
Kosaka, T., Tauchi, M., & Dahl, J. L. (1988) · Experimental Brain Research · doi:10.1007/bf00247609 · Cited by 417
Short-term plasticity at the calyx of held
von Gersdorff, H., & Borst, J. G. G. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn705 · Cited by 388
The shape and arrangement of the cholinergic neurons in the rabbit retina
Tauchi, M., & Masland, R. H. (1984) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1984.0085 · Cited by 385
A shared vesicular carrier allows synaptic corelease of GABA and glycine
Wojcik, S. M., Katsurabayashi, S., Guillemin, I., Friauf, E., Rosenmund, C., Brose, N., & Rhee, J.-S. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.016 · Cited by 374
Chapter 2 The mosaic of amacrine cells in the mammalian retina
Vaney, D. I. (1990) · Progress in Retinal Research · doi:10.1016/0278-4327(90)90004-2 · Cited by 372
Mechanisms and circuitry underlying directional selectivity in the retina
Fried, S. I., Münch, T. A., & Werblin, F. S. (2002) · Nature · doi:10.1038/nature01179 · Cited by 368
Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I. H., & Nakanishi, S. (2001) · Neuron · doi:10.1016/s0896-6273(01)00316-6 · Cited by 363
Synaptic corelease of ATP and GABA in cultured spinal neurons
Jo, Y., & Schlichter, R. (1999) · Nature Neuroscience · doi:10.1038/6344 · Cited by 350
Diversification of synaptic strength: presynaptic elements
Atwood, H. L., & Karunanithi, S. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn876 · Cited by 346
Dale, H. H. (1935) · PubMed · Cited by 330
Famiglietti, E. V. (1983) · Brain Research · doi:10.1016/0006-8993(83)91293-3 · Cited by 294
Pharmacology and Nerve-Endings
Dale, H. H. (1935) · Proceedings of the Royal Society of Medicine · doi:10.1177/003591573502800330 · Cited by 293
Autoradiographic identification of acetylcholine in the rabbit retina.
Masland, R. H., & Mills, J. W. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.83.1.159 · Cited by 286
Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells
Ariel, M., & Daw, N. W. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014105 · Cited by 282
Responses to acetylcholine of ganglion cells in an isolated mammalian retina
Masland, R. H., & Ames, A. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.6.1220 · Cited by 256
Mammalian motor neurons corelease glutamate and acetylcholine at central synapses
Nishimaru, H., Restrepo, C. E., Ryge, J., Yanagawa, Y., & Kiehn, O. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501331102 · Cited by 235
Brecha, N., Johnson, D., Peichl, L., & Wässle, H. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.16.6187 · Cited by 225
Burnstock, G. (2003) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2003.08.001 · Cited by 216
GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina
Vaney, D. I., & Young, H. M. (1988) · Brain Research · doi:10.1016/0006-8993(88)91366-2 · Cited by 211
Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina
Taylor, W. R., & Vaney, D. I. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07712.2002 · Cited by 201
The functions of acetylcholine in the rabbit retina
Masland, R. H., Mills, J. W., & Cassidy, C. (1984) · Proceedings of the Royal Society of London. Series B. Biological Sciences · doi:10.1098/rspb.1984.0086 · Cited by 200
‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology
Di, V. (1984) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1984.0016 · Cited by 193
The Synaptic Mechanism of Direction Selectivity in Distal Processes of Starburst Amacrine Cells
Lee, S., & Zhou, Z. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.007 · Cited by 179
Self-citationMaturation of function in the developing rabbit retina
Masland, R. H. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901750303 · Cited by 173
Identification of ON–OFF direction‐selective ganglion cells in the mouse retina
Weng, S.-J., Sun, W., & He, S. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.076695 · Cited by 172
Territorial organization of direction-selective ganglion cells in rabbit retina
Vaney, D. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06301.1994 · Cited by 171
Pharmacology of Directionally Selective Ganglion Cells in the Rabbit Retina
Kittila, C. A., & Massey, S. C. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.2.675 · Cited by 164
Cellular Mechanisms for Direction Selectivity in the Retina
Demb, J. B. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.001 · Cited by 159
Zheng, J., Lee, S., & Zhou, Z. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.015 · Cited by 155
Self-citationEffects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells
Ariel, M., & Daw, N. W. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014104 · Cited by 153
Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron
O'Malley, D. M., & Masland, R. H. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.9.3414 · Cited by 150
Yang, G., & Masland, R. H. (1992) · Science · doi:10.1126/science.1470920 · Cited by 146
A Dendrite-Autonomous Mechanism for Direction Selectivity in Retinal Starburst Amacrine Cells
Hausselt, S., Euler, T., Detwiler, P. B., & Denk, W. T. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050185 · Cited by 145
Retinal direction selectivity after targeted laser ablation of starburst amacrine cells
He, S., & Masland, R. H. (1997) · Nature · doi:10.1038/38723 · Cited by 141
Famiglietti, E. V. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903240303 · Cited by 141
Short-term synaptic plasticity: a comparison of two synapses
Blitz, D. M., Foster, K. A., & Regehr, W. G. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1475 · Cited by 140
Fried, S. I., Münch, T. A., & Werblin, F. S. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.007 · Cited by 134
Elstrott, J., Anishchenko, A., Greschner, M., Sher, A., Litke, A. M., Chichilnisky, E. J., & Feller, M. B. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.013 · Cited by 132
Receptive fields and dendritic structure of directionally selective retinal ganglion cells
Yang, G., & Masland, R. H. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05267.1994 · Cited by 128
Massey, S. C., & Neal, M. J. (1979) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1979.tb11062.x · Cited by 117
New directions in retinal research
Taylor, W. R., & Vaney, D. I. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00167-x · Cited by 107
Amthor, F. R., Keyser, K. T., & DMITRIEVA, N. A. (2002) · Visual Neuroscience · doi:10.1017/s0952523802194119 · Cited by 97
Glutamate and acetylcholine corelease at developing synapses
Li, W., Soffe, S. R., & Roberts, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404864101 · Cited by 86
Functional implications of neurotransmitter co-release: glutamate and GABA share the load
Seal, R. P., & EDWARDS, R. (2005) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2005.12.001 · Cited by 85
Action and localization of acetylcholine in the cat retina
Schmidt, M., Humphrey, M. F., & Wässle, H. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.58.5.997 · Cited by 82
Famiglietti, E. V. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-02-00562.1985 · Cited by 76
Direction selectivity in the retina
Vaney, D. I. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00337-9 · Cited by 73
Synaptic 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
Self-citationGrzywacz, N. M., Amthor, F. R., & Merwine, D. K. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.575be.x · Cited by 65
Neurotransmitter 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
Self-citationChen, M., Weng, S.-J., Deng, Q., Xu, Z., & He, S. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.161240 · Cited by 58
Synaptic 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
Chan, Y.-C., & Chiao, C. (2008) · Vision Research · doi:10.1016/j.visres.2008.08.010 · Cited by 51
Effect of ON pathway blockade on directional selectivity in the rabbit retina
Kittila, C. A., & Massey, S. C. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.2.703 · Cited by 51
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
Voltage-gated calcium and sodium currents of starburst amacrine cells in the rabbit retina
Cohen, E. D. (2001) · Visual Neuroscience · doi:10.1017/s0952523801185135 · Cited by 49
Chiao, C., & Masland, R. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10509.2002 · Cited by 48
Receptors with opposing functions are in postsynaptic microdomains under one presynaptic terminal
Tsen, G., Williams, B., Allaire, P., Zhou, Y., Ikonomov, O. C., Kondova, I. I., & Jacob, M. H. (2000) · Nature Neuroscience · doi:10.1038/72066 · Cited by 44
Complementary roles of two excitatory pathways in retinal directional selectivity
Grzywacz, N. M., Merwine, D. K., & Amthor, F. R. (1998) · Visual Neuroscience · doi:10.1017/s0952523898156109 · Cited by 37
Vardi, N., Masarachia, P. J., & Sterling, P. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902880407 · Cited by 29
Characterization of Voltage-Gated Ionic Channels in Cholinergic Amacrine Cells in the Mouse Retina
Kaneda, M., Ito, K., Morishima, Y., Shigematsu, Y., & Shimoda, Y. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01022.2006 · Cited by 27
Effects of Ca2+ channel blockers on directional selectivity of rabbit retinal ganglion cells
Jensen, R. J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.1.12 · Cited by 27
Image Processing: How the Retina Detects the Direction of Image Motion
Fried, S. I., & Masland, R. H. (2007) · Current Biology · doi:10.1016/j.cub.2006.12.013 · Cited by 25
Nicotinic acetylcholine receptor expression by directionally selective ganglion cells
Strang, C. E., Renna, J. M., Amthor, F. R., & Keyser, K. T. (2007) · Visual Neuroscience · doi:10.1017/s0952523807070435 · Cited by 20
Massey, S. C., & Neal, M. J. (1979) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1979.tb07828.x · Cited by 13
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Briggman, K. L., Helmstaedter, M., & Denk, W. (2011) · Nature · doi:10.1038/nature09818 · Cited by 883
Kay, J. N., la Huerta, I. D., Kim, I.-J., Zhang, Y., Yamagata, M., Chu, M. W., Meister, M., & Sanes, J. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0907-11.2011 · Cited by 351
Direction selectivity in the retina: symmetry and asymmetry in structure and function
Vaney, D. I., Sivyer, B., & Taylor, W. R. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3165 · Cited by 330
Neurotransmitter Corelease: Mechanism and Physiological Role
Hnasko, T. S., & Edwards, R. H. (2012) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153315 · Cited by 284
Seeing Things in Motion: Models, Circuits, and Mechanisms
Borst, A., & Euler, T. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.031 · Cited by 291
Metadata
- Authors
- Lee, S., Kim, K., & Zhou, Z. J.
- Affiliations
- University of Arkansas for Medical Sciences (US)
- Yale University (US)
- Corresponding author
- Zhou, Z. Jimmy
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 68
- Issue
- 6
- Pages
- 1159-1172
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3094727
- OpenAlex
- W1991368688
- Cited by
- 241
- References
- 68
- Citations by year
- 2026: 12 · 2025: 9 · 2024: 25 · 2023: 22 · 2022: 11 · 2021: 13 · 2020: 14 · 2019: 11 · 2018: 14 · 2017: 17 · 2016: 23 · 2015: 15 · 2014: 14 · 2013: 14 · 2012: 15
- FWCI
- 5.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Research to Prevent Blindness
- National Institutes of Health
- National Eye Institute (R01 EY10894, R01EY010894, P30EY000785, R01EY017353)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Health Sciences › Medicine › Ophthalmology › Retinal Development and Disorders
- Keywords
- acetylcholine, GABA, co-transmission, starburst amacrine cells, direction-selective ganglion cells, motion detection, direction selectivity, cholinergic synapses, GABAergic synapses, calcium-dependent neurotransmitter release, retinal circuitry
- MeSH terms
- Acetylcholine, Animals, gamma-Aminobutyric Acid, Motion Perception, Synaptic Transmission, Photic Stimulation, Rabbits, Retina, Synapses, Amacrine Cells
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