Skip to main content Accessibility help
×
Home

Synaptic organization of GABAergic amacrine cells in the salamander retina

  • JUN ZHANG (a1), HO-HWA WANG (a1) and CHEN-YU YANG (a1)

Abstract

The synaptic organization of GABA-immunoreactive (GABA-IR) amacrine cells in the inner plexiform layer (IPL) of salamander retina was studied with the use of postembedding immuno-electron microscopy. A total of 457 GABA-IR amacrine synapses, with identified postsynaptic elements, were analyzed on photomontages of electron micrographs covering 3,618 μm2 of the IPL. GABA-IR amacrine synapses were distributed throughout the IPL, with a small peak at the proximal margin of sublamina a. The majority of the output targets (81%) were GABA(−) neurons. Most of the contacts were simple synapses with one postsynaptic element identified as a process of an amacrine cell (55%), bipolar cell (19%) or ganglion cell (26%), and serial synapses were very rare. Of the 89 postsynaptic bipolar terminals, 63% participated in a reciprocal feedback synapse with the same presynaptic GABA-IR amacrine profile. There appeared to be no preference between GABA-IR amacrine contacts with rod- or cone-dominated bipolar cells (9.1% vs. 8.9%) or in the total number of amacrine synapses in sublaminas a and b (52% vs. 47%). The preponderance of amacrine cell input to bipolar cells in the OFF layer was derived from GABA-IR cells. These findings provide ultrastructural support to the existing physiological studies regarding the functional roles of the GABAergic amacrine cells in this species. Our results have added to the data base demonstrating that, in contrast to mammals, GABA-IR amacrine cells in amphibians and other nonmammals contact other amacrine cells more frequently, suggesting greater involvement of GABAergic amacrine cells in modulating lateral inhibitory pathways.

Copyright

Corresponding author

Address correspondence and reprint requests to: Chen-Yu Yang, Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, NY 11794-5230, USA. E-mail: chyang@notes.cc.sunysb.edu
Present address: Synaptic Physiology Unit, Building 36/Rm 2C09, NINDS/NIH, Bethesda, MD 20892, USA

References

Hide All

REFERENCES

Agardh, E., Bruun, A., Ehinger, B., Ekström, P., Van Veen, T., & Wu, J. (1987). Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. Journal of Comparative Neurology 258, 622630.
Belgum, J.H., Dvorak, D.R., & McReynolds, J.S. (1984). Strychnine blocks transient but not sustained inhibition in mudpuppy retinal ganglion cells. Journal of Physiology (London) 354, 273286.
Buzás, P., Jeges, S., & Gábriel, R. (1996). The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina. Visual Neuroscience 13, 10991107.
Chun, M.H. & Wässle, H. (1989). GABA-like immunoreactivity in the cat retina: Electron microscopy. Journal of Comparative Neurology 279, 5567.
Cook, P.B. & McReynolds, J.S. (1998). Modulation of sustained and transient lateral inhibitory mechanisms in the mudpuppy retina during light adaptation. Journal of Neurophysiology 79, 197204.
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287302.
Davanger, S., Ottersen, O.P., & Storm-Mathisen, J. (1991). Glutamate, GABA, and glycine in the human retina: An immunocytochemical investigation. Journal of Comparative Neurology 311, 483494.
Deng, P., Cuenca, N., Doerr, T., Pow, D.V., Miller, R., & Kolb, H. (2001). Localization of neurotransmitters and calcium binding proteins to neurons of salamander and mudpuppy retinas. Vision Research 41, 17711783.
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 21712180.
Dowling, J.E. (1968). Synaptic organization of the frog retina: An electron-microscopic analysis comparing the retinas of frogs and primates. Proceedings of the Royal Society B (London) 170, 205228.
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B (London) 166, 80111.
Dowling, J.E. & Werblin, F.S. (1969). Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. Journal of Neurophysiology 32, 315338.
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: a quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479505.
Freed, M.A. (1992). GABAergic circuits in the mammalian retina. Progress in Brain Research 90, 107131.
Gábriel, R. & Straznicky, C. (1993). Quantitative analysis of GABA-immunoreactive synapses in the inner plexiform layer of the Bufo marinus retina: Identification of direct output to ganglion cells and contacts with dopaminergic amacrine cells. Journal of Neurocytology 22, 2638.
Gao, F., Maple, B.R., & Wu, S.M. (2000). 14AA-sensitive chloride current contributes to the center light responses of bipolar cells in the tiger salamander retina. Journal of Neurophysiology 83, 34733482.
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509524.
Hubel, D.H. & Wiesel, T.N. (1960). Receptive fields of optic fibers in the spider monkey. Journal of Physiology (London) 154, 572580.
Koontz, M.A. & Hendrickson, A.E. (1990). Distribution of GABA-immunoreactive amacrine cell synapses in the inner plexiform layer of macaque monkey retina. Visual Neuroscience 5, 1728.
Lukasiewicz, P.D., Maple, B.R., & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. Journal of Neuroscience 14, 12021212.
Lukasiewicz, P.D. & Shields, C.R. (1998a). Different combinations of GABAA and GABAC receptors confer distinct temporal properties to retinal synaptic responses. Journal of Neurophysiology 79, 31573167.
Lukasiewicz, P.D. & Shields, C.R. (1998b). A diversity of GABA receptors in the retina. Seminars in Cell and Developmental Biology 9, 293299.
Lukasiewicz, P.D. & Werblin, F.S. (1990). The spatial distribution of excitatory and inhibitory inputs to ganglion cell dendrites in the tiger salamander retina. Journal of Neuroscience 10, 210221.
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 12131223.
MacDonald, R.L. & Olsen, R.W. (1994). GABAA receptor channels. Annual Review of Neuroscience 17, 569602.
Maguire, G.W., Lukasiewicz, P.D., & Werblin, F. (1989a). Amacrine cell interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience 9, 726735.
Maguire, G., Maple, B., Lukasiewicz, P.D., & Werblin, F. (1989b). Gamma-aminobutyrate type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceedings of the National Academy of Sciences of the U.S.A. 86, 1014410147.
Maple, B.R. & Wu, S.M. (1996). Synaptic inputs mediating bipolar cell responses in the tiger salamander retina. Vision Research 36, 40154023.
Marc, R.E. & Liu, W.L.S. (2000). Fundamental GABAergic amacrine cell circuitries in the retina: Nested feedback, concatenated inhibition, and axosomatic synapses. Journal of Comparative Neurology 425, 560582.
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S., & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog Rana pipiens. Journal of General Physiology 43, 129175.
Miller, R.F., Frumkes, T.E., Slaughter, M.M., & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. II. Amacrine and ganglion cells. Journal of Neurophysiology 45, 764782.
Mosinger, J.L., Studholme, K.M., & Yazulla, S. (1986). Immunocytochemical localization of GABA in the retina: A species comparison. Experimental Eye Research 42, 631644.
Muller, J.F. & Marc, R.E. (1990). GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. Journal of Comparative Neurology 291, 281304.
O'Malley, D.M., Sandell, J.H., & Masland, R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 13941408.
Osborne, N.N., Patel, S., Beaton, D.W., & Neuhoff, V. (1986). GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell and Tissue Research 243, 117123.
Pan, Z.-H. & Slaughter, M.M. (1991). Control of retinal information coding by GABAB receptors. Journal of Neuroscience 11, 18101821.
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, (3H)muscimol: A combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 2535.
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 2, 425435.
Roska, B., Nemeth, E., Orzo, L., & Werblin, F.S. (2000). Three levels of lateral inhibition: A space–time study of the retina of the tiger salamander. Journal of Neuroscience 20, 19411951.
Shen, W. & Slaughter, M.M. (2001). Multireceptor GABAergic regulation of synaptic communication in amphibian retina. Journal of Physiology (London) 530, 5567.
Vardi, N. & Auerbach, P. (1995). Specific cell types in cat retina express different forms of glutamic acid decarboxylase. Journal of Comparative Neurology 351, 374384.
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 4354.
Watt, C.B. (1991). A re-examination of enkephalin's coexistence with gamma-aminobutyric acid in amacrine cells of the larval tiger salamander retina. Brain Research 551, 351354.
Watt, C.B. (1992). A double-label study demonstrating that all serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina express GABA-like immunoreactivity. Brain Research 583, 336339.
Watt, C.B. & Florack, V.J. (1992). A double-label analysis demonstrating the non-coexistence of tyrosine hydroxylase-like and GABA-like immunoreactivities in amacrine cells of the larval tiger salamander retina. Neuroscience Letters 148, 4750.
Watt, C.B. & Florack, V.J. (1993). Double-label analyses of the coexistence of somatostatin with GABA and glycine in amacrine cells of the larval tiger salamander retina. Brain Research 617, 131137.
Watt, C.B. & Glazebrook, P.A. (1993). Synaptic organization of dopaminergic amacrine cells in the larval tiger salamander retina. Neuroscience 53, 527536.
Watt, C.B., Li, H., Fry, K.R., & Lam, D.M.K. (1985). Localization of enkephalin-like immunoreactive amacrine cells in the larval tiger salamander retina: A light and electron microscopic study. Journal of Comparative Neurology 241, 171179.
Watt, C.B., Li, T., Lam, D.M.K., & Wu, S.M. (1987). Interactions between enkephalin and gamma-aminobutyric acid in the larval tiger salamander retina. Brain Research 408, 258262.
Watt, C.B., Florack, V.J., & Walker, R.B. (1993). Quantitative analyses of the coexistence of gamma-aminobutyric acid in substance P-amacrine cells of the larval tiger salamander retina. Brain Research 603, 111116.
Watt, C.B. & Wilson, E.A. (1990). Synaptic organization of serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina. Neuroscience 35, 715723.
Wenthold, R.J., Zemple, J., Parakkal, M.A., Reeks, K.A., & Altschuler, R.A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 718.
Wong-Riley, M.T. (1974). Synaptic organization of the inner plexiform layer in the retina of the tiger salamander. Journal of Neurocytology 3, 133.
Wu, S.M. & Maple, B.R. (1998). Amino acid neurotransmitters in the retina: a functional overview. Vision Research 38, 13711384.
Wu, S.M., Gao, F., & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: Segregation of visual signals by stratification of bipolar cell axon terminals. Journal of Neuroscience 20, 44624470.
Yang, C.Y. (1996). Glutamate immunoreactivity in the tiger salamander retina differentiates between GABA-immunoreactive and glycine-immunoreactive amacrine cells. Journal of Neurocytology 25, 391403.
Yang, C.-Y., Lukasiewicz, P.D., Maguire, G., Werblin, F.S., & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 1932.
Yang, C.Y. & Yazulla, S. (1986). Neuropeptide-like immunoreactive cells in the retina of the larval tiger salamander: Attention to the symmetry of dendritic projections. Journal of Comparative Neurology 248, 105118.
Yang, C.Y. & Yazulla, S. (1988). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographic methods. Journal of Comparative Neurology 277, 96108.
Yang, C.-Y. & Yazulla, S. (1994). Glutamate-, GABA-, and GAD-immunoreactivities co-localize in bipolar cells of tiger salamander retina. Visual Neuroscience 11, 11931203.
Yang, C.Y. & Wang, H.H. (1999). Anatomical and electrophysiological evidence for GABAergic bipolar cells in tiger salamander retina. Vision Research 39, 36533661.
Yang, C.Y., Zhang, J., & Yazulla, S. (2003). Differential synaptic organization of GABAergic bipolar cells and non-GABAergic (glutamatergic) bipolar cells in the tiger salamander retina. Journal of Comparative Neurology 455, 187197.
Yang, S.-Z., Lam, D.M.K., & Watt, C.B. (1989). Localization of serotonin like-immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 287, 2837.
Yazulla, S. (1981). GABAergic synapses in the goldfish retina: An autoradiographic study of 3H-muscimol and 3H-GABA binding. Journal of Comparative Neurology 200, 8393.
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 152.
Yazulla, S. & Brecha, N. (1981). Localized binding of 3H-muscimol to synapses in the chick retina. Proceedings of the National Academy of Sciences of the U.S.A. 78, 643647.
Yazulla, S. & Yang, C.-Y. (1988). Colocalization of GABA- and glycine-immunoreactivities in a subset of retinal neurons in tiger salamander. Neuroscience Letters 95, 3741.
Zhang, J., Fu, L.W., & Yang, X.-L. (1999). Distribution of GABA-like immunoreactivity in the bullfrog retina. Chinese Journal of Neuroanatomy 15, 13.
Zhang, J., DeBlas, A.L., Miralles, C.P., & Yang, C.Y. (2003). Localization of GABA(A) receptor subunits α(1), α(3), β(1), β(2/3), γ(1), and γ(2) in the salamander retina. Journal of Comparative Neurology 459, 440453.
Zhang, J. & Wu, S.M. (2001). Immunocytochemical analysis of cholinergic amacrine cells in the tiger salamander retina. Neuroreport 12, 13711375.
Zhang, J., Yang, Z., & Wu, S.M. (2002). Quantitative analysis of GABAergic and glycinergic amacrine cells in the tiger salamander retina. Investigative Ophthalmology and Visual Science (Suppl.) 43, S766.
Zhang, J.A., Jung, C.S., & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553563.

Keywords

Synaptic organization of GABAergic amacrine cells in the salamander retina

  • JUN ZHANG (a1), HO-HWA WANG (a1) and CHEN-YU YANG (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed