Rod Vision Is Controlled by Dopamine-Dependent Sensitization of Rod Bipolar Cells by GABA

Neuron

Volumn 72, Issue 1, 2011, Pages 101-110

  Herrmann, Rolf ^a   Heflin, Stephanie J ^c   Hammond, Timothy ^a   Lee, Bowa ^a   Wang, Jing ^d   Gainetdinov, Raul R ^b,e   Caron, Marc G ^b   Eggers, Erika D ^f   Frishman, Laura J ^d   McCall, Maureen A ^c   Arshavsky, Vadim Y ^a  

^a DUKE UNIVERSITY EYE CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

^d UNIVERSITY OF HOUSTON   (United States)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^f UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID C RECEPTOR; CHLORIDE; DOPAMINE; DOPAMINE 1 RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; CHLORIDE CURRENT; CHLORIDE TRANSPORT; CONTROLLED STUDY; DARK ADAPTATION; GABAERGIC SYSTEM; HYPERPOLARIZATION; MEMBRANE STEADY POTENTIAL; MOUSE; NIGHT VISION; NONHUMAN; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; RETINA HORIZONTAL NERVE CELL;

ADAPTATION, OCULAR; ANIMALS; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; MICE; NEURAL INHIBITION; NIGHT VISION; PHOTIC STIMULATION; RECEPTORS, DOPAMINE D1; RECEPTORS, GABA; RETINAL BIPOLAR CELLS; SYNAPTIC TRANSMISSION;

EID: 80053590699     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.07.030     Document Type: Article

References (51)

1. Amin J., Weiss D.S. Homomeric rho 1 GABA channels: activation properties and domains. Receptors Channels 1994, 2:227-236.
2. Babai N., Thoreson W.B. Horizontal cell feedback regulates calcium currents and intracellular calcium levels in rod photoreceptors of salamander and mouse retina. J. Physiol. 2009, 587:2353-2364.
3. Carlsson A., Waters N., Holm-Waters S., Tedroff J., Nilsson M., Carlsson M.L. Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu. Rev. Pharmacol. Toxicol. 2001, 41:237-260.
4. Chávez A.E., Grimes W.N., Diamond J.S. Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina. J. Neurosci. 2010, 30:2330-2339.
5. Deniz S., Wersinger E., Schwab Y., Mura C., Erdelyi F., Szabó G., Rendon A., Sahel J.A., Picaud S., Roux M.J. Mammalian retinal horizontal cells are unconventional GABAergic neurons. J. Neurochem. 2011, 116:350-362.
6. Dunn F.A., Doan T., Sampath A.P., Rieke F. Controlling the gain of rod-mediated signals in the Mammalian retina. J. Neurosci. 2006, 26:3959-3970.
7. Eggers E.D., Lukasiewicz P.D. GABA(A), GABA(C) and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. J. Physiol. 2006, 572:215-225.
8. Eggers E.D., McCall M.A., Lukasiewicz P.D. Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. J. Physiol. 2007, 582:569-582.
9. Enz R., Brandstätter J.H., Hartveit E., Wässle H., Bormann J. Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. Eur. J. Neurosci. 1995, 7:1495-1501.
10. Euler T., Masland R.H. Light-evoked responses of bipolar cells in a mammalian retina. J. Neurophysiol. 2000, 83:1817-1829.
11. Euler T., Wässle H. Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. J. Neurophysiol. 1998, 79:1384-1395.
12. Glykys J., Mody I. Activation of GABAA receptors: views from outside the synaptic cleft. Neuron 2007, 56:763-770.
13. Greengard P. The neurobiology of slow synaptic transmission. Science 2001, 294:1024-1030.
14. Guo C., Hirano A.A., Stella S.L., Bitzer M., Brecha N.C. Guinea pig horizontal cells express GABA, the GABA-synthesizing enzyme GAD 65, and the GABA vesicular transporter. J. Comp. Neurol. 2010, 518:1647-1669.
15. Hankins M., Ikeda H. Early abnormalities of retinal dopamine pathways in rats with hereditary retinal dystrophy. Doc. Ophthalmol. 1994, 86:325-334.
16. Herrmann R., Lobanova E.S., Hammond T., Kessler C., Burns M.E., Frishman L.J., Arshavsky V.Y. Phosducin regulates transmission at the photoreceptor-to-ON-bipolar cell synapse. J. Neurosci. 2010, 30:3239-3253.
17. Hull C., Li G.L., von Gersdorff H. GABA transporters regulate a standing GABAC receptor-mediated current at a retinal presynaptic terminal. J. Neurosci. 2006, 26:6979-6984.
18. Jones S.M., Palmer M.J. Activation of the tonic GABAC receptor current in retinal bipolar cell terminals by nonvesicular GABA release. J. Neurophysiol. 2009, 102:691-699.
19. Kamermans M., Spekreijse H. The feedback pathway from horizontal cells to cones. A mini review with a look ahead. Vision Res. 1999, 39:2449-2468.
20. Knapp A.G., Schmidt K.F., Dowling J.E. Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells. Proc. Natl. Acad. Sci. USA 1990, 87:767-771.
21. Li L., Dowling J.E. Effects of dopamine depletion on visual sensitivity of zebrafish. J. Neurosci. 2000, 20:1893-1903.
22. Li B., McKernan K., Shen W. Spatial and temporal distribution patterns of Na-K-2Cl cotransporter in adult and developing mouse retinas. Vis. Neurosci. 2008, 25:109-123.
23. Lukasiewicz P.D., Shields C.R. A diversity of GABA receptors in the retina. Semin. Cell Dev. Biol. 1998, 9:293-299.
24. Mangel S.C., Dowling J.E. Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 1985, 229:1107-1109.
25. McCall M.A., Lukasiewicz P.D., Gregg R.G., Peachey N.S. Elimination of the rho1 subunit abolishes GABA(C) receptor expression and alters visual processing in the mouse retina. J. Neurosci. 2002, 22:4163-4174.
26. Mills S.L., Xia X.B., Hoshi H., Firth S.I., Rice M.E., Frishman L.J., Marshak D.W. Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network. Vis. Neurosci. 2007, 24:593-608.
27. Naarendorp F., Sieving P.A. The scotopic threshold response of the cat ERG is suppressed selectively by GABA and glycine. Vision Res. 1991, 31:1-15.
28. Nir I., Haque R., Iuvone P.M. Diurnal metabolism of dopamine in the mouse retina. Brain Res. 2000, 870:118-125.
29. Robson J.G., Frishman L.J. Dissecting the dark-adapted electroretinogram. Doc. Ophthalmol. 1998, 95:187-215.
30. Robson J.G., Maeda H., Saszik S.M., Frishman L.J. In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Res. 2004, 44:3253-3268.
31. Rodieck R.W. The First Steps in Seeing 1998, Sinauer Associates, Sunderland, MA.
32. Roska B., Nemeth E., Orzo L., Werblin F.S. Three levels of lateral inhibition: A space-time study of the retina of the tiger salamander. J. Neurosci. 2000, 20:1941-1951.
33. Satoh H., Kaneda M., Kaneko A. Intracellular chloride concentration is higher in rod bipolar cells than in cone bipolar cells of the mouse retina. Neurosci. Lett. 2001, 310:161-164.
34. Schwartz E.A. Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science 1987, 238:350-355.
35. Shapley R.M., Enroth-Cugell C. Visual adaptation and retinal gain controls. Prog. Retinal Res. 1984, 3:263-346.
36. Shields C.R., Tran M.N., Wong R.O., Lukasiewicz P.D. Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. J. Neurosci. 2000, 20:2673-2682.
37. Suzuki S., Tachibana M., Kaneko A. Effects of glycine and GABA on isolated bipolar cells of the mouse retina. J. Physiol. 1990, 421:645-662.
38. Tachibana M., Kaneko A. gamma-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proc. Natl. Acad. Sci. USA 1987, 84:3501-3505.
39. Tessier-Lavigne M., Attwell D., Mobbs P., Wilson M. Membrane currents in retinal bipolar cells of the axolotl. J. Gen. Physiol. 1988, 91:49-72.
40. Thibos L.N., Werblin F.S. The response properties of the steady antagonistic surround in the mudpuppy retina. J. Physiol. 1978, 278:79-99.
41. Vardi N., Kaufman D.L., Sterling P. Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase. Vis. Neurosci. 1994, 11:135-142.
42. Vardi N., Zhang L.L., Payne J.A., Sterling P. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J. Neurosci. 2000, 20:7657-7663.
43. Veruki M.L., Wässle H. Immunohistochemical localization of dopamine D1 receptors in rat retina. Eur. J. Neurosci. 1996, 8:2286-2297.
44. Vu T.Q., Payne J.A., Copenhagen D.R. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J. Neurosci. 2000, 20:1414-1423.
45. Wässle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 2004, 5:747-757.
46. Wässle H., Chun M.H. GABA-like immunoreactivity in the cat retina: light microscopy. J. Comp. Neurol. 1989, 279:43-54.
47. Weiler R., Pottek M., He S., Vaney D.I. Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Res. Brain Res. Rev. 2000, 32:121-129.
48. Witkovsky P. Dopamine and retinal function. Doc. Ophthalmol. 2004, 108:17-40.
49. Yang X.L., Wu S.M. Feedforward lateral inhibition in retinal bipolar cells: input-output relation of the horizontal cell-depolarizing bipolar cell synapse. Proc. Natl. Acad. Sci. USA 1991, 88:3310-3313.
50. Yang X.L., Tornqvist K., Dowling J.E. Modulation of cone horizontal cell activity in the teleost fish retina. II. Role of interplexiform cells and dopamine in regulating light responsiveness. J. Neurosci. 1988, 8:2269-2278.
51. Zhang L.L., Delpire E., Vardi N. NKCC1 does not accumulate chloride in developing retinal neurons. J. Neurophysiol. 2007, 98:266-277.