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Electrophysiological evidence of GABAA and GABAC receptors on zebrafish retinal bipolar cells

Published online by Cambridge University Press:  28 April 2008

VICTORIA P. CONNAUGHTON ,
RALPH NELSON  and
ANNA M. BENDER
VICTORIA P. CONNAUGHTON*
Affiliation:
Department of Biology, American University, Washington, DC
RALPH NELSON
Affiliation:
Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
ANNA M. BENDER
Affiliation:
Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
*
Address correspondence and reprint requests to: V.P. Connaughton, Department of Biology, American University, 4400 Massachusetts Ave, NW, Washington, DC 20016. E-mail: vconn@american.edu
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Abstract

To refine inhibitory circuitry models for ON and OFF pathways in zebrafish retina, GABAergic properties of zebrafish bipolar cells were studied with two techniques: whole cell patch responses to GABA puffs in retinal slice, and voltage probe responses in isolated cells. Retinal slices documented predominantly axon terminal responses; isolated cells revealed mainly soma-dendritic responses. In the slice, GABA elicited a conductance increase, GABA responses were more robust at axon terminals than dendrites, and Erev varied with [Cl−]in. Axon terminals of ON- and OFF-type cells were similarly sensitive to GABA (30–40 pA peak current); axotomized cells were unresponsive. Bicuculline-sensitive, picrotoxin-sensitive, and picrotoxin-insensitive components were identified. Muscimol was as effective as GABA; baclofen was ineffective. Isolated bipolar cells were either intact or axotomized. Even in cells without an axon, GABA or muscimol (but not baclofen) hyperpolarized dendritic and somatic regions, suggesting significant distal expression. Median fluorescence change for GABA was −0.22 log units (∼ −16 mV); median half-amplitude dose was 0.4 μM. Reduced [Cl−]out blocked GABA responses. GABA hyperpolarized isolated ON-bipolar cells; OFF-cells were either unresponsive or depolarized. Hyperpolarizing GABA responses in isolated cells were bicuculline and TPMPA insensitive, but blocked or partially blocked by picrotoxin or zinc. In summary, axon terminals contain bicuculline-sensitive GABAA receptors and both picrotoxin-sensitive and insensitive GABAC receptors. Dendritic processes express zinc- and picrotoxin-sensitive GABAC receptors.

Keywords

RetinaBipolar cellsGABAZebrafishInhibition
Type
Research Article
Information
Visual Neuroscience , Volume 25 , Issue 2 , March 2008 , pp. 139 - 153
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Blanco, R., Vaquero, C.F. & de la Villa, P. (1996). The effects of GABA and glycine on horizontal cells of the rabbit retina. Vision Research 36, 3987–3995.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. (1977). Responses and receptive-field organization of cones in perch retinas. Journal of Neurophysiology 40, 53–62.CrossRefGoogle ScholarPubMed
Connaughton, V.P. (2003). Zebrafish retinal slice preparation. Methods in Cell Science 25, 49–58.CrossRefGoogle ScholarPubMed
Connaughton, V.P., Behar, T.N., Liu, W.-L.S. & Massey, S. (1999). Immunocytochemical localization of excitatory and inhibitory neurotransmitters in the zebrafish retina. Visual Neuroscience 16, 483–490.CrossRefGoogle ScholarPubMed
Connaughton, V.P., Bender, A.M. & Nelson, R. (2000). GABA-evoked responses of zebrafish retinal bipolar cells. Investigative Ophthalmology and Visual Science 41, S621.Google Scholar
Connaughton, V.P. & Dowling, J.E. (1998). Comparative morphology of distal neurons in developing and adult zebrafish retinas. Vision Research 38, 13–18.CrossRefGoogle ScholarPubMed
Connaughton, V.P., Graham, D. & Nelson, R. (2004). Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina using the DiOlistic technique. Journal of Comparative Neurology 477, 371–385.CrossRefGoogle Scholar
Connaughton, V.P. & Maguire, G. (1998). Differential expression of voltage-gated K+ and Ca+2 currents in bipolar cells in the zebrafish retinal slice. European Journal of Neuroscience 10, 1350–1362.CrossRefGoogle ScholarPubMed
Connaughton, V.P. & Nelson, R. (2000). Axonal stratification patterns and glutamate-gated conductance mechanisms in zebrafish retinal bipolar cells. Journal of Physiology 524, 135–146.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate, and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287–302.CrossRefGoogle ScholarPubMed
Cui, J., Ma, Y.-P., Lipton, S.A. & Pan, Z.-H. (2003). Glycine receptors and glycinergic synaptic input at the axon terminals of mammalian retinal rod bipolar cells. Journal of Physiology 553, 895–909.CrossRefGoogle ScholarPubMed
Dong, C.-J. & Hare, W.A. (2002). GABAC feedback pathway modulates the amplitude and kinetics of ERG b-wave in a mammalian retina in vivo. Vision Research 42, 1081–1087.CrossRefGoogle Scholar
Dowling, J.E. & Werblin, F.S. (1969). Organizatin of the retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. Journal of Neurophysiology 32, 315–338.CrossRefGoogle Scholar
Du, J.-L. & Yang, X.-L. (2000). Subcellular localization and complements of GABAA and GABAC receptors on bullfrog retinal bipolar cells. Journal of Neurophysiology 84, 666–676.CrossRefGoogle ScholarPubMed
Du, J.-L. & Yang, X.-L. (2002a). Bullfrog retinal bipolar cells may express heterogeneous glycine receptors at dendrites and axon terminals. Neuroscience Letters 322, 177–181.CrossRefGoogle ScholarPubMed
Du, J.-L. & Yang, X.-L. (2002b). Glycinergic synaptic transmission to bullfrog retinal bipolar cells is input-specific. Neuroscience 113, 779–784.CrossRefGoogle ScholarPubMed
Eggers, E.D. & Lukasiewicz, P. (2006). GABAA, GABAC, and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. Journal of Physiology 572, 215–225.CrossRefGoogle ScholarPubMed
Euler, T. & Wässle, H. (1998). Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. Journal of Neurophysiology 79, 1384–1395.CrossRefGoogle Scholar
Feigenspan, A. & Bormann, J. (1994). Differential pharmacology of GABAA and GABAC receptors on rat retinal bipolar cells. European Journal of Pharmacology 288, 97–104.CrossRefGoogle ScholarPubMed
Feigenspan, A., Wässle, H. & Bormann, J. (1993). Pharmacology of GABA receptor Cl-channels in rat retinal bipolar cells. Nature 361, 159–161.CrossRefGoogle ScholarPubMed
Fisher, S.K. & Boycott, B.B. (1974). Synaptic connexions made by horizontal cells within the outer plexiform layer of the retina of the cat and the rabbit. Proceeding of the Royal Society of London B 186, 317–331.Google Scholar
Frech, M.J. & Backus, K.H. (2004). Characterization of inhibitory postsynaptic currents in rod bipolar cells of the mouse retina. Visual Neuroscience 21, 645–652.CrossRefGoogle ScholarPubMed
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.CrossRefGoogle ScholarPubMed
Freed, M.A., Smith, R.G. & Sterling, P. (2003). Timing of quantal release from the retinal bipolar terminal is regulated by a feedback circuit. Neuron 38, 89–101.CrossRefGoogle ScholarPubMed
Gao, F., Maple, B.R. & Wu, S.M. (2000). I4AA-sensitive chloride current contributes to the center light responses of bipolar cells in the tiger salamander retina. Journal of Neurophysiology 83, 3473–3482.CrossRefGoogle Scholar
Greferath, U., Muller, F., Wässle, H., Shivers, B. & Seeburg, P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.CrossRefGoogle ScholarPubMed
Han, M.-H., Li, Y. & Yang, X.-L. (1997). Desensitizing GABAC receptors on carp retinal bipolar cells. Neuroreport 8, 1331–1335.CrossRefGoogle ScholarPubMed
Han, M.-H. & Yang, X.-L. (1999). Zn+2 differentially modulates kinetics of GABAC vs. GABAA receptors in carp retinal bipolar cells. Neuroreport 10, 2593–2597.CrossRefGoogle Scholar
Hanitzsch, R., Kuppers, L. & Flade, A. (2004). The effect of GABA and the GABA-uptake-blocker NO-711 on the b-wave of the ERG and the responses of horizontal cells to light. Graefe's Archive of Clinical Experimental Ophthalmology 242, 784–791.CrossRefGoogle ScholarPubMed
Heidelberger, R. & Matthews, G. (1991). Inhibition of calcium influx and calcium current by gamma-aminobutyric acid in single synaptic terminals. Proceeding of the National Academy of Science 88, 7135–7139.CrossRefGoogle ScholarPubMed
Hull, C., Li, G.-L. & von Gersdorff, H. (2006). GABA transporters regulate a standing GABAC receptor-mediated current at a retinal presynaptic terminal. Journal of Neuroscience 26, 6979–6984.CrossRefGoogle Scholar
Hull, C. & von Gersdorff, H. (2004). Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal. Neuron 44, 469–482.CrossRefGoogle Scholar
Ivanova, E., Muller, E. & Wässle, H. (2006). Characterization of the glycinergic input to bipolar cells of the mouse retina. European Journal of Neuroscience 23, 350–364.CrossRefGoogle ScholarPubMed
Kaneda, M., Andrasfalvy, B. & Kaneko, A. (2000). Modulation of Zn+2 of GABA responses in bipolar cells of the mouse retina. Visual Neuroscience 17, 273–281.CrossRefGoogle Scholar
Kaneko, A., Suzuki, S., Pinto, H. & Tachibana, M. (1991). Membrane currents and pharmacology of retinal bipolar cells: A comparative study on goldfish and mouse. Comparative Biochemistry and Physiology C 98, 115–127.CrossRefGoogle ScholarPubMed
Kapousta-Bruneau, N.V. (2000). Opposite effects of GABAA and GABAC receptor antagonists on the b-wave of the ERG recorded from the isolated rat retina. Vision Research 40, 1653–1665.CrossRefGoogle ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Kenyon, J.L. (2002). Primer on Junctional Potentials for the Patchologist, 3rd edition. Las Vegas: University of Nevada School of Medicine.Google Scholar
Klooster, J., Cardozo, B.N., Yazulla, S. & Kamermans, M. (2004). Postsynaptic localization of gamma-aminobutyric acid transporters and receptors in the outer plexiform layer of the goldfish retina: An ultrastructural study. Journal of Comparative of Neurology 474, 58–74.CrossRefGoogle ScholarPubMed
Kolb, H. & Jones, J. (1984). Synaptic organization of the outer plexiform layer of the turtle retina: An electron microscope study of serial sections. Journal of Neurocytology 13, 567–591.CrossRefGoogle ScholarPubMed
Kolb, H. & West, R.W. (1977). Synaptic connections of the interplexiform cell in the retina of the cat. Journal of Neurocytology 6, 155–170.CrossRefGoogle ScholarPubMed
Kondo, H. & Toyoda, J.-I. (1983). GABA and glycine effects on the bipolar cells of the carp retina. Vision Research 23, 1259–1264.CrossRefGoogle ScholarPubMed
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philosophical Transactions of the Royal Society London B-Biological Sciences 265, 471–489.Google ScholarPubMed
Linberg, K.A. & Fisher, S.K. (1988). Ultrastructural evidence that horizontal cell axon terminals are presynaptic in the human retina. Journal of Comparative Neurology 268, 281–297.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D., Eggers, E.D., Sagdullaev, B.T. & McCall, M.A. (2004). GABAC receptor-mediated inhibition in the retina. Vision Research 44, 3289–3296.CrossRefGoogle ScholarPubMed
Lukasiewicz, P., 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.CrossRefGoogle ScholarPubMed
Lukasiewicz, P. & Shields, C.R. (1998). Different combinations of GABAA and GABAC receptors confer distinct temporal properties to retinal synaptic responses. Journal of Neurophysiology 79, 3157–3167.CrossRefGoogle ScholarPubMed
Lukasiewicz, P. & Wong, R.O.L. (1997). GABAC receptors on ferret retinal bipolar cells: A diversity of subtypes in mammals? Visual Neuroscience 14, 989–994.CrossRefGoogle ScholarPubMed
Mack, A.F., Behrens, U.D. & Wagner, H.-J. (2000). Inhibitory control of synaptic activity in goldfish Mb bipolar cell terminals visualized by FM1-43. Visual Neuroscience 17, 823–829.CrossRefGoogle ScholarPubMed
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F.S. (1989). Gamma-aminobutyric type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceeding of the National Academy of Science 86, 10144–10147.CrossRefGoogle Scholar
Maple, B.R. & Wu, S.M. (1998). Glycinergic synaptic inputs to bipolar cells in the tiger salamander retina. Journal of Physiology 506, 731–744.CrossRefGoogle Scholar
Marc, R.E. & Cameron, D. (2001). A molecular phenotype atlas of the zebrafish retina. Journal of Neurocytology 30, 593–654.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–224.CrossRefGoogle ScholarPubMed
Matthews, G., Ayoub, G.S. & Heidelberger, R. (1994). Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology. Journal of Neuroscience 14, 1079–1090.CrossRefGoogle ScholarPubMed
McGillem, G.S., Rotolo, T.C. & Dacheux, R.F. (2000). GABA responses of rod bipolar cells in rabbit retinal slices. Visual Neuroscience 17, 381–389.CrossRefGoogle ScholarPubMed
Nelson, R., Bender, A.M. & Connaughton, V.P. (2003). Stimulation of sodium pump restores membrane potential to neurons excited by glutamate in zebrafish distal retina. Journal of Physiology 549, 787–800.CrossRefGoogle ScholarPubMed
Nelson, R., Bender, A.M. & Connaughton, V.P. (2006). Transporter-like GABA excitation of horizontal and bipolar cells in zebrafish distal retina. Investigative Ophthalmology and Visual Science. E-abstract 390.Google Scholar
Nelson, R., Bender, A.M. & Connaughton, V.P. (2008). Transported-mediated BAGA responses in horizontal and bipolar cells of the zebrafish retina. Visual Neuroscience 25, 139–149.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.CrossRefGoogle ScholarPubMed
Nelson, R., Schaffner, A.E., Li, Y.-X. & Walton, M.K. (1999). Distribution of GABAC-like responses among acutely dissociated rat retinal neurons. Visual Neuroscience 16, 179–190.CrossRefGoogle ScholarPubMed
Pan, Y., Khalili, P., Ripps, H. & Qian, H. (2005). Pharmacology of GABAC receptors: Responses to agonists and antagonists distinguish A- and B-subtypes of homomeric rho receptors expressed in Xenopus oocytes. Neuroscience Letters 376, 60–65.CrossRefGoogle ScholarPubMed
Pan, Z.-H. (2001). Voltage-activated Ca+2 channels and ionotropic GABA receptors localized at axon terminals of mammalian retinal bipolar cells. Visual Neuroscience 18, 279–288.CrossRefGoogle Scholar
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, 25–35.CrossRefGoogle ScholarPubMed
Qian, H. & Dowling, J.E. (1993). GABA responses on retinal bipolar cells. Biology Bulletin 185, 312.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Qian, H. & Dowling, J.E. (1995). GABAA and GABAC receptors on hybrid bass retinal bipolar cells. Journal of Neurophysiology 74, 1920–1928.CrossRefGoogle ScholarPubMed
Qian, H., Dowling, J.E. & Ripps, H. (1998). Molecular and pharmacological properties of GABA-rho subunits from white perch retina. Journal of Neurobiology 37, 305–320.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Qian, H., Li, L., Chappell, R.L. & Ripps, H. (1997). GABA receptors of bipolar cells from the skate retina: Actions of zinc on GABA-mediated membrane currents. Journal of Neurophysiology 78, 2402–2412.CrossRefGoogle ScholarPubMed
Qian, H., Malchow, R.P., Chappell, R.L. & Ripps, H. (1996). Zinc enhances ionic currents induced in skate Muller (glial) cells by the inhibitory neurotransmitter GABA. Proceeding of the Royal Society of London B 263, 791–796.Google ScholarPubMed
Qian, H. & Pan, Y. (2002). Co-assembly of GABA rho subunits with GABAA receptor gamma-2 subunit cloned from white perch retina. Molecular Brain Research 103, 62–70.CrossRefGoogle ScholarPubMed
Qian, H. & Ripps, H. (1999). Response kinetics and pharmacological properties of hetermoeric receptors formed by coassembly of GABA rho- and gamma2-subunits. Proceeding of the Royal Society of London B 266, 2419–2425.CrossRefGoogle Scholar
Qian, H., Ripps, H., Schuette, E. & Chappell, R.L. (2001). Responses of small- and large-field bipolar cells to GABA and glycine. Brain Research 893, 273–277.CrossRefGoogle ScholarPubMed
Shen, Y., Chen, L., Ping, Y. & Yang, X.-L. (2005). Glycine modulates the center response of ON type rod-dominant bipolar cells in carp retina. Brain Research Bulletin 67, 492–497.CrossRefGoogle Scholar
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca+2 entry elicits transient postsynaptic currents at a retinal ribbon synapse. Journal of Neuroscience 23, 10923–10933.CrossRefGoogle Scholar
Tachibana, M. & Kaneko, A. (1987). Gamma-aminobutyric acid exerts a local inhibition action on the axon terminal of bipolar cells: Evidence for negative feedback from amacrine cells. Proceeding of the National Academy of Science 84, 3501–3505.CrossRefGoogle Scholar
Tachibana, M. & Kaneko, A. (1998). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–305.CrossRefGoogle Scholar
Vaquero, C.F. & de la Villa, P. (1999). Localisation of the GABAC receptors at the axon terminal of rod bipolar cells of the mouse retina. Neuroscience Research 35, 1–7.CrossRefGoogle ScholarPubMed
Wang, T.-L., Hackam, A., Guggino, W.B. & Cutting, G.R. (1995). A single histidine residue is essential for zinc inhibition of GABA rho1 receptors. Journal of Neuroscience 15, 7684–7691.CrossRefGoogle Scholar
Woodward, R.M., Polenzani, L. & Miledi, R. (1993). Characterization of bicuculline/baclofen-insensitive (rho-like) gamma-aminobutyric acid receptors expressed in Xenopus oocytes. II. Pharmacology of gamma-aminobutyric acid-A and gamma-aminobutyric acid-B receptor agonists and antagonists. Molecular Pharmacology 43, 609–625.Google Scholar
Wu, D. & Zhu, P.H. (2000). Inhibition of calcium signaling in terminal and soma of carp retinal bipolar cells by GABA. Acta Pharmacology Sinica 21, 709–714.Google ScholarPubMed
Wu, S.M. (1986). Effects of gamma-aminobutyric acid on cones and bipolar cells of the tiger salamander retina. Brain Research 365, 70–77.CrossRefGoogle ScholarPubMed
Wu, S.M. & Maple, B. (1998). Amino acid neurotransmitters in the retina: A functional overview. Vision Research 38, 1371–1384.CrossRefGoogle ScholarPubMed
Yazulla, S. & Studholme, K.M. (2001). Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. Journal of Neurocytology 30, 551–592.CrossRefGoogle ScholarPubMed
Yazulla, S., Studholme, K.M. & Wu, J.Y. (1987). GABAergic input to the synaptic terminals of Mb1 bipolar cells in the goldfish retina. Brain Research 411, 400–405.CrossRefGoogle Scholar
Zhang, D., Pan, Z.-H., Awobuluyi, M. & Lipton, S.A. (2001). Structure and function of GABAC receptors: A comparison of native versus recombinant receptors. Trends in Pharmacology Science 22, 121–132.CrossRefGoogle ScholarPubMed
Zhang, D., Pan, Z.-H., Zhang, X., Brideau, A.D. & Lipton, S.A. (1995). Cloning of a gamma-aminobutyric acid type C receptor subunit in rat retina with methionine residue critical for picrotoxinin channel block. Proceeding of the National Academy of Science 92, 11756–11760.CrossRefGoogle ScholarPubMed
Zhang, D.-O. & Yang, X.-L. (1997). OFF pathway is preferentially suppressed by the activation of GABAA receptors in carp retina. Brain Research 759, 160–162.CrossRefGoogle ScholarPubMed
Zhang, J., De Blas, A.L., Miralles, C.P. & Yang, C.-Y. (2003). Localization of GABAA receptor subunits alpha1, alpha3, beta1, beta2/3, gamma1, and gamma2 in the salamander retina. Journal of Comparative Neurology 459, 440–453.CrossRefGoogle Scholar
Zhang, J. & Slaughter, M.M. (1995). Preferential suppression of the ON pathway by GABAC receptors in the amphibian retina. Journal of Neurophysiology 74, 1583–1592.CrossRefGoogle ScholarPubMed
Zhou, C. & Dacheux, R.F. (2005). Glycine- and GABA-activated inhibitory currents on axon terminals of rabbit cone bipolar cells. Visual Neuroscience 22, 759–767.CrossRefGoogle ScholarPubMed