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Serial inhibitory synapses in retina

Published online by Cambridge University Press:  02 June 2009

Jian Zhang ,
Chang-Sub Jung  and
Malcolm M. Slaughter
Jian Zhang
Affiliation:
Departments of Physiology, Biophysical Sciences, and Ophthalmology, School of Medicine, State University of New York, Buffalo
Chang-Sub Jung
Affiliation:
Departments of Physiology, Biophysical Sciences, and Ophthalmology, School of Medicine, State University of New York, Buffalo
Malcolm M. Slaughter
Affiliation:
Departments of Physiology, Biophysical Sciences, and Ophthalmology, School of Medicine, State University of New York, Buffalo
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Abstract

Whole-cell voltage clamp in the retinal slice and intracellular current clamp in the intact retina were used to study inhibitory interactions in the inner plexiform layer. Picrotoxin or strychnine reduced inhibitory, light-evoked currents in a majority of ganglion cells. However, in nearly a third of the ganglion cells, each of these antagonists enhanced the inhibitory synaptic current. All inhibitory current was blocked by the addition of the other antagonist. This indicates a cross-inhibition between GABAergic and glycinergic feedforward pathways. Blocking of GABAARs with SR95531 shortened the time course of both excitatory and inhibitory synaptic currents in ganglion cells. Application of picrotoxin, which blocked both GABAARs and GABACRs, produced the opposite effect. Recordings in the intact retina indicated that the light responses of ON bipolar cells, sustained ON, and transient ON-OFF third-order neurons were all made more transient by SR95531 and made more sustained by picrotoxin. The data suggest that a GABAC feedback pathway to bipolar cells makes light responses more phasic and that this feedback is inhibited through a GABAAR pathway. Consequently, the balance between GABAAR and GABACR inhibition regulates the time course of inputs to ganglion cells.

Keywords

RetinaGABAGlycineGanglion cellsInhibition
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 3 , May 1997 , pp. 553 - 563
Copyright
Copyright © Cambridge University Press 1997

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References

REFERENCES

Amin, J. & Weiss, D.S. (1994). Homomeric ρ1 GABA channels: Activation properties and domains. Receptors and Channels 2, 227–236.Google Scholar
Bai, S.-H. & Slaughter, M.M. (1989). Effects of baclofen on transient neurons in the mudpuppy retina: Electrogenic and network actions. Journal of Neurophysiology 61, 382–390.Google Scholar
Belgum, J.H., Dvorak, D.R. & Mcreynolds, J.S. (1982). Sustained synaptic input to ganglion cells of mudpuppy retina. Journal of Physiology 326, 91–108.Google Scholar
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 354, 273–286.Google Scholar
Chun, M.H. & Wässle, H. (1989). GABA-like immunoreactivity in the cat retina: Electron microscopy. Journal of Comparative Neurology 279, 55–67.Google Scholar
Cutting, G.R., Lu, L., O'Hara, B., Kasch, L.M., Donovan, D., Schimada, S., Antonarakis, D.E., Guggino, W.B., Uhl, G.R. & Kazaxian, H.H. (1991). Cloning of the GABAρ1 cDNA: A novel GABA subunit highly expressed in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2673–2677.CrossRefGoogle Scholar
Frumkes, T.E., Miller, R.F., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. III. Amacrine-mediated inhibitory influences on ganglion cell receptive-field organization: A model. Journal of Neurophysiology 45, 783–804.Google Scholar
Frumkes, T.E. & Nelson, R. (1995). Functional role of GABA in cat retina: I. Effects of GABAA agonists. Visual Neuroscience 12, 641–650.Google Scholar
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the Macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509–524.Google Scholar
Han, Y. & Slaughter, M.M. (1996). Strychnine sensitivity of glycine responses in isolated ganglion cells from amphibian retina. Investigative Ophthalmology and Visual Science 37, S139.Google Scholar
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, 17–28.Google Scholar
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, 1202–1212.Google Scholar
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, 1213–1223.Google Scholar
Marc, R.E. (1992). Structural organization of GABAergic circuitry in ectotherm retinas. Progress in Brain Research 90, 61–92.CrossRefGoogle Scholar
Massey, S.C. & Redburn, D.A. (1982). A tonic γ-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 1633–1643.CrossRefGoogle ScholarPubMed
Mienville, J.M. & Vicini, S. (1987). A pyridazinyl derivative of gamma-aminobutyric acid (GABA), SR95531, is a potent antagonist of C1-channel opening regulated by GABAA receptors. Neuropharmacology 26, 779–783.Google Scholar
Miller, R.F. & Dacheux, R.F. (1976). Synaptic organization and ionic basis of ON and OFF channels in the mudpuppy retina. 1. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolars, and amacrine cells. Journal of General Physiology 67, 639–659.Google Scholar
Miller, R.F., Frumkes, T.E., Slaughter, 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, 783–804.Google Scholar
Neal, M.J. & Cunningham, J.R. (1995). Baclofen enhancement of acetylcholine release from amacrine cells in the rabbit retina by reduction of glycinergic inhibition. Journal of Physiology 482, 363–372.Google Scholar
Neher, E. (1992). Correction for liquid junction potentials in patch clamp experiments. Methods in Enzymology 207, 123–131.Google Scholar
Nygaard, R.W. & Frumkes, T.E. (1982). LEDs: Convenient, inexpensive sources for visual experimentation. Vision Research 22, 435–440.Google Scholar
PAN, Z.-H. & Lipton, S.A. (1995). Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. Journal of Neuroscience 15, 2668–2679.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 2, 425–435.Google Scholar
Qian, H. & Dowling, J.E. (1994). Pharmacology of novel GABA receptors found on rod horizontal cells of the white perch retina. Journal of Neuroscience 14, 4299–4307.Google Scholar
Sherry, D.M. & Yazulla, S. (1993). GABA and glycine in retina amacrine cells: Combined Golgi impregnation and immunocytochemistry. Philosophical Transactions of the Royal Society B (London) 342, 295–320.Google Scholar
Slaughter, M.M. & Bai, S.-H. (1989). Differential effects of baclofen on sustained and transient cells in the mudpuppy retina. Journal of Neurophysiology 61, 374–381.Google Scholar
Wellis, D.P. & Werblin, F.S. (1995). Dopamine modulates GABAC receptors mediating inhibition of calcium entry into and transmitter release from bipolar cell terminals in tiger salamander retina. Journal of Neuroscience 15, 4748–4761.Google Scholar
Werblin, F.S. (1978). Transmission along and between rods in the tiger salamander retina. Journal of Physiology 280, 449–470.Google Scholar
Werblin, F., Maguire, G., Lukasiewicz, P., Eliasof, S. & Wu, S.M. (1988). Neural interactions mediating the detection of motion in the retina of the tiger salamander. Visual Neuroscience 1, 317–329.Google Scholar
Woodward, R.M., Polenzani, L. & Miledi, R. (1993). Characterization of bicuculline/baclofen-insensitive (ρ-like) γ-aminobutyric acid receptors expressed in Xenopus oocytes: II. Pharmacology of γ-aminobutyric acidA and γ-aminobutyric acidB receptor agonists and antagonists. Molecular Pharmacology 43, 609–625.Google Scholar
Wu, S.-M. (1987). Synaptic connections between neurons in living slices of the larval salamander retina. Journal of Neuroscience Methods 20, 139–149.Google Scholar
Wu, S.M. (1992). Functional organization of GABAergic circuitry in ectotherm retinas. Progress in Brain Research 90, 93–106.Google Scholar
Yang, C.Y. & Yazulla, S. (1988). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunohistochemical and autoradiographic methods. Journal of Comparative Neurology 277, 96–108.Google Scholar
Zhang, J. & Slaughter, M.M. (1995 a). Preferential suppression of the ON pathway by GABAC receptors in the amphibian retina. Journal of Neurophysiology 74, 1583–1592.Google Scholar
Zhang, J. & Slaughter, M.M. (1995 b). Serial GABAergic synapses regulate the temporal properties of bipolar cell transmitter release. Investigative Ophthalmology and Visual Science 37, S418.Google Scholar