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Transporter-mediated GABA responses in horizontal and bipolar cells of zebrafish retina

Published online by Cambridge University Press:  28 April 2008

RALPH NELSON ,
ANNA M. BENDER  and
VICTORIA P. CONNAUGHTON
RALPH NELSON*
Affiliation:
Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, Maryland
ANNA M. BENDER
Affiliation:
Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, Maryland
VICTORIA P. CONNAUGHTON
Affiliation:
Department of Biology, American University, Washington, DC
*
Address correspondence and reprint requests to: Ralph F. Nelson, Basic Neurosciences Program National Institute of Neurological Disorders and Stroke, National Institutes of Health, 5625 Fisher's Lane, Room TS-09, Rockville, MD 20892–9406. E-mail: nelsonr@ninds.nih.gov
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Abstract

GABA-mediated interactions between horizontal cells (HCs) and bipolar cells (BCs) transform signals within the image-processing circuitry of distal retina. To further understand this process, we have studied the GABA-driven membrane responses from isolated retinal neurons. Papain-dissociated retinal cells from adult zebrafish were exposed to GABAergic ligands while transmembrane potentials were monitored with a fluorescent voltage-sensitive dye (oxonol, DiBaC4(5)). In HCs hyperpolarizing, ionotropic GABA responses were almost never seen, nor were responses to baclofen or glycine. A GABA-induced depolarization followed by after hyperpolarization (dep/AHP) occurred in 38% of HCs. The median fluorescence increase (dep component) was 0.17 log units, about 22 mV. HC dep/AHP was not blocked by bicuculline or picrotoxin. Muscimol rarely evoked dep/AHP responses. In BCs picrotoxin sensitive, hyperpolarizing, ionotropic GABA and muscimol responses occurred in most cells. A picrotoxin insensitive dep/AHP response was seen in about 5% of BCs. The median fluorescence increase (dep component) was 0.18 log units, about 23 mV. Some BCs expressed both muscimol-induced hyperpolarizations and GABA-induced dep/AHP responses. For all cells, the pooled Hill fit to median dep amplitudes, in response to treatments with a GABA concentration series, gave an apparent k of 0.61 μM and an n of 1.1. The dep/AHP responses of all cells required both extracellular Na+ and Cl−, as dep/AHP was blocked reversibly by Li+ substituted for Na+ and irreversibly by isethionate substituted for Cl−. All cells with dep/AHP responses in zebrafish have the membrane physiology of neurons expressing GABA transporters. These cells likely accumulate GABA, a characteristic of GABAergic neurons. We suggest Na+ drives GABA into these cells, depolarizing the plasma membrane and triggering Na+, K+-dependent ATPase. The ATPase activity generates AHP. In addition to a GABA clearance function, these large-amplitude transporter responses may provide an outer plexiform layer GABA sensor mechanism.

Keywords

Outer plexiform layerATPaseGABA transporterBaclofenGlycineHorizontal cellBipolar cell
Type
Research Article
Information
Visual Neuroscience , Volume 25 , Issue 2 , March 2008 , pp. 155 - 165
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Baylor, D.A., Fuortes, M.G. & O'Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.CrossRefGoogle ScholarPubMed
Billups, D. & Attwell, D. (2002). Control of intracellular chloride concentration and GABA response polarity in rat retinal ON bipolar cells. Journal of Physiology 545, 183–198.Google Scholar
Blanco, R. & de la Villa, P. (1999). Ionotropic glutamate receptors in isolated horizontal cells of the rabbit retina. European Journal of Neuroscience 11, 867–873.Google Scholar
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.Google Scholar
Connaughton, V.P., Behar, T.N., Liu, W.L. & Massey, S.C. (1999). Immunocytochemical localization of excitatory and inhibitory neurotransmitters in the zebrafish retina. Visual Neuroscience 16, 483–490.CrossRefGoogle ScholarPubMed
Connaughton, V.P. & Dowling, J.E. (1998). Comparative morphology of distal neurons in larval and adult zebrafish retinas. Vision Research 38, 13–18.CrossRefGoogle ScholarPubMed
Connaughton, V.P., Dyer, K.D., Nadi, N.S. & Behar, T.N. (2001). The expression of GAD67 isoforms in zebrafish retinal tissue changes over the light/dark cycle. Journal of Neurocytology 30, 303–312.Google Scholar
Connaughton, V.P., Graham, D. & Nelson, R. (2004). Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. Journal of Comparative Neurology 477, 371–385.Google Scholar
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.Google Scholar
Connaughton, V.P., Nelson, R. & Bender, A.M. (2008). Electrophysiological evidence of GABAA and GABAC receptors on zebrafish retinal bipolar cells. Visual Neuroscience 25, 151–165.Google Scholar
Dall'Asta, V., Gatti, R., Orlandini, G., Rossi, P.A., Rotoli, B.M., Sala, R., Bussolati, O. & Gazzola, G.C. (1997). Membrane potential changes visualized in complete growth media through confocal laser scanning microscopy of bis-oxonol-loaded cells. Experimental Cell Research 231, 260–268.CrossRefGoogle ScholarPubMed
Dong, C.J., Picaud, S.A. & Werblin, F.S. (1994). GABA transporters and GABAC-like receptors on catfish cone- but not rod-driven horizontal cells. Journal of Neuroscience 14, 2648–2658.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
Duebel, J., Haverkamp, S., Schleich, W., Feng, G., Augustine, G.J., Kuner, T. & Euler, T. (2006). Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon. Neuron 49, 81–94.CrossRefGoogle ScholarPubMed
Frumkes, T.E. & Nelson, R. (1995). Functional role of GABA in cat retina: I. Effects of GABAA agonists. Visual Neuroscience 12, 641–650.CrossRefGoogle ScholarPubMed
Frumkes, T.E., Nelson, R. & Pflug, R. (1995). Functional role of GABA in cat retina: II. Effects of GABAA antagonists. Visual Neuroscience 12, 651–661.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
Grunert, U. & Wassle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509–524.CrossRefGoogle ScholarPubMed
Hirano, A.A., Brandstatter, J.H., Vila, A. & Brecha, N.C. (2007). Robust syntaxin-4 immunoreactivity in mammalian horizontal cell processes. Visual Neuroscience 24, 489–502.CrossRefGoogle ScholarPubMed
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. Journal of Comparative Neurology 191, 315–335.Google Scholar
Kamermans, M., Fahrenfort, I., Schultz, K., Janssen-Bienhold, U., Sjoerdsma, T. & Weiler, R. (2001). Hemichannel-mediated inhibition in the outer retina. Science 292, 1178–1180.Google Scholar
Kamermans, M. & Werblin, F. (1992). GABA-mediated positive auto feedback loop controls horizontal cell kinetics in tiger salamander retina. Journal of Neuroscience 12, 2451–2463.Google Scholar
Kao, Y.H., Lassova, L., Bar-Yehuda, T., Edwards, R.H., Sterling, P. & Vardi, N. (2004). Evidence that certain retinal bipolar cells use both glutamate and GABA. Journal of Comparative Neurology 478, 207–218.CrossRefGoogle ScholarPubMed
Krause, S. & Schwarz, W. (2005). Identification and selective inhibition of the channel mode of the neuronal GABA transporter 1. Molecular Pharmacology 68, 1728–1735.Google Scholar
Langheinrich, U. & Daut, J. (1997). Hyperpolarization of isolated capillaries from guinea-pig heart induced by K+ channel openers and glucose deprivation. Journal of Physiology 502, 397–408.CrossRefGoogle Scholar
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philosical Transactions of the Royal Society of London B. Biological Sciences 265, 471–489.Google Scholar
Lasansky, A. (1980). Lateral contacts and interactions of horizontal cell dendrites in the retina of the larval tiger salamander. Journal of Physiology 301, 59–68.Google Scholar
Lasansky, A. (1981). Synaptic action mediating cone responses to annular illumination in the retina of the larval tiger salamander. Journal of Physiology 310, 205–214.Google Scholar
Malchow, R.P. & Ripps, H. (1990). Effects of gamma-aminobutyric acid on skate retinal horizontal cells: Evidence for an electrogenic uptake mechanism. Processing of National Academy of Science United States of America 87, 8945–8949.Google 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). GABA-ergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–244.Google Scholar
Maric, D., Maric, I. & Barker, J.L. (2000). Dual video microscopic imaging of membrane potential and cytosolic calcium of immunoidentified embryonic rat cortical cells. Methods 21, 335–347.CrossRefGoogle ScholarPubMed
McIntire, S.L., Reimer, R.J., Schuske, K., Edwards, R.H. & Jorgensen, E.M. (1997). Identification and characterization of the vesicular GABA transporter. Nature 389, 870–876.Google Scholar
McMahon, D.G. (1994). Modulation of electrical synaptic transmission in zebrafish retinal horizontal cells. Journal of Neuroscience 14, 1722–1734.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., 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.Google Scholar
Nelson, R.F. & Connaughton, V.P. (2007). Color coding in the light responses of zebrafish horizontal cells. In Society for Neuroscience. San Diego, CA: Society for Neuroscience.Google 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). Novel GABA responses from rod-driven retinal horizontal cells. Nature 361, 162–164.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
Sandell, J.H., Martin, S.C. & Heinrich, G. (1994). The development of GABA immunoreactivity in the retina of the zebrafish (Brachydanio rerio). Journal of Comparative Neurology 345, 596–601.Google Scholar
Schwartz, E.A. (1982). Calcium-independent release of GABA from isolated horizontal cells of the toad retina. Journal of Physiology 323, 211–227.CrossRefGoogle ScholarPubMed
Schwartz, E.A. (1987). Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science 238, 350–355.CrossRefGoogle ScholarPubMed
Song, P.I., Matsui, J.I. & Dowling, J.E. (2008). Morphological types and connectivity of horizontal cells found in the adult zebrafish (Danio rerio) retina. Journal of Comparative Neurology 506, 328–338.CrossRefGoogle ScholarPubMed
Stell, W.K. & Lightfoot, D.O. (1975). Color-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–502.Google Scholar
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–305.CrossRefGoogle ScholarPubMed
Takahashi, K., Miyoshi, S. & Kaneko, A. (1994). Two components of GABA-induced currents in catfish retinal horizontal cells. Japanese Journal of Physiology 44, S141–144.Google ScholarPubMed
Takahashi, K., Miyoshi, S., Kaneko, A. & Copenhagen, D.R. (1995). Actions of nipecotic acid and SKF89976A on GABA transporter in cone-driven horizontal cells dissociated from the catfish retina. Japanese Journal of Physiology 45, 457–473.Google Scholar
Vaquero, C.F. & de la Villa, P. (1999). Localisation of the GABAC receptors at the axon terminal of the rod bipolar cells of the mouse retina. Neuroscience Research 35, 1–7.CrossRefGoogle ScholarPubMed
Vardi, N., Kaufman, D.L. & Sterling, P. (1994). Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase. Visual Neuroscience 11, 135–142.Google Scholar
Vardi, N., Zhang, L.L., Payne, J.A. & Sterling, P. (2000). Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. Journal of Neuroscience 20, 7657–7663.Google Scholar
Varela, C., Blanco, R. & De la Villa, P. (2005). Depolarizing effect of GABA in rod bipolar cells of the mouse retina. Vision Research 45, 2659–2667.Google Scholar
Verweij, J., Kamermans, M., Negishi, K. & Spekreijse, H. (1998). GABA sensitivity of spectrally classified horizontal cells in goldfish retina. Visual Neuroscience 15, 77–86.Google Scholar
Waggoner, A. (1976). Optical probes of membrane potential. Journal of Membrane Biology 27, 317–334.Google Scholar
Walton, M.K., Schaffner, A.E. & Barker, J.L. (1993). Sodium channels, GABAA receptors, and glutamate receptors develop sequentially on embryonic rat spinal cord cells. Journal of Neuroscience 13, 2068–2084.CrossRefGoogle ScholarPubMed
Wassle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 43–54.CrossRefGoogle ScholarPubMed
Yamashita, M. & Wassle, H. (1991). Reversal potential of GABA-induced currents in rod bipolar cells of the rat retina. Visual Neuroscience 6, 399–401.Google Scholar
Yang, C.-Y. & Wang, H.-H.W. (1999). Anatomical and electrophysiological evidence for GABAergic bipolar cells in tiger salamander retina. Vision Research 39, 3653–3661.Google Scholar
Yang, C.Y. (1997). L-glutamic acid decarboxylase- and gamma-aminobutyric acid-immunoreactive bipolar cells in tiger salamander retina are of ON- and OFF-response types as inferred from Lucifer Yellow injection. Journal of Comparative Neurology 385, 651–660.Google Scholar
Yang, C.Y., Brecha, N.C. & Tsao, E. (1997). Immunocytochemical localization of gamma-aminobutyric acid plasma membrane transporters in the tiger salamander retina. Journal of Comparative Neurology 389, 117–126.Google Scholar
Yang, C.Y. & Yazulla, S. (1994). Glutamate-, GABA-, and GAD-immunoreactivities co-localize in bipolar cells of tiger salamander retina. Visual Neuroscience 11, 1193–1203.Google Scholar
Yazulla, S. (1991). The mismatch problem for GABAergic amacrine cells in goldfish retina: Resolution and other issues. Neurochemistry Research 16, 327–339.Google Scholar
Yazulla, S. & Brecha, N. (1980). Binding and uptake of the GABA analogue, 3H-muscimol, in the retinas of goldfish and chicken. Investigative Ophthalmology & Visual Science 19, 1415–1426.Google Scholar
Yazulla, S. & Kleinschmidt, J. (1983). Carrier-mediated release of GABA from retinal horizontal cells. Brain Research 263, 63–75.Google Scholar
Yazulla, S. & Studholme, K.M. (2001). Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. Journal of Neurocytology 30, 551–592.Google Scholar