The mode of retinal presynaptic inhibition switches with light intensity

Journal of Neuroscience

Volumn 32, Issue 13, 2012, Pages 4360-4371

  Ichinose, Tomomi ^a   Lukasiewicz, Peter D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; PROTEIN KINASE C;

ANIMAL TISSUE; ARTICLE; CHLORIDE CURRENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; FEMALE; IMMUNOCYTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; LIGHT INTENSITY; MALE; MOUSE; NERVE ENDING; NONHUMAN; PHOTOSTIMULATION; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA ROD;

ANIMALS; EXOCYTOSIS; FEMALE; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; LIGHT; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; PRESYNAPTIC TERMINALS; RETINAL BIPOLAR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPTIC TRANSMISSION;

EID: 84859047246     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5645-11.2012     Document Type: Article

References (59)

1. Arden GB, Hogg CR (1985) Rod-cone interactions and analysis of retinal disease. Br J Ophthalmol 69:404-415.
2. Arriza JL, Eliasof S, Kavanaugh MP, Amara SG (1997) Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci U S A 94:4155-4160.
3. Berntson A, Taylor WR (2000) Response characteristics and receptive field widths of on-bipolar cells in the mouse retina. J Physiol 524:879-889.
4. Bloomfield SA, Xin D (2000) Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. J Physiol 523:771-783.
5. Buck SL (2004) Rod-cone interactions in human vision. In: The visual neurosciences (Chalupa LM, Werner JS, eds), pp 863-878.
6. Cambridge, MA: MIT. Chávez AE, Singer JH, Diamond JS (2006) Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443:705-708.
7. Chávez AE, Grimes WN, Diamond JS (2010) Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina. J Neurosci 30:2330-2339.
8. Chen S, Diamond JS (2002) Synaptically released glutamate activates extrasynaptic NMDA receptors on cells in the ganglion cell layer of the rat retina. J Neurosci 22:2165-2173.
9. Dacheux RF, Raviola E (1986) The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. J Neurosci 6:331-345.
10. Eggers ED, Klein JS (2010) Rod and cone pathways of inhibition. Invest Ophthalmol Vis Sci 51:E-Abstract 4800.
11. Eggers ED, Lukasiewicz PD (2006a) GABAA, GABAC and glycine receptormediated inhibition differentially affects light-evoked signaling from mouse retinal rod bipolar cells. J Physiol 572:215-225.
12. Eggers ED, Lukasiewicz PD (2006b) Receptor and transmitter release properties set the time course of retinal inhibition. J Neurosci 26:9413-9425.
13. Eggers ED, Lukasiewicz PD (2010) Interneuron circuits tune inhibition in retinal bipolar cells. J Neurophysiol 103:25-37.
14. Eggers ED, McCall MA, Lukasiewicz PD (2007) Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. J Physiol 582:569-582.
15. Eliasof S, Werblin F (1993) Characterization of the glutmate transporter in retinal cones of the tiger salamander. J Neurosci 13:402-411.
16. Enroth-Cugell C, Hertz BG, Lennie P (1977) Convergence of rod and cone signals in the cat's retina. J Physiol 269:297-318.
17. Euler T, Masland RH (2000) Light-evoked responses of bipolar cells in mammalian retina. J Neurophysiol 83:1817-1829.
18. Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, Amara SG (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375:599-603.
19. Frech MJ, Backus KH (2004) Characterization of inhibitory postsynaptic currents in rod bipolar cells of the mouse retina. Vis Neurosci 21:645-652.
20. Gaffield MA, Betz WJ (2006) Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat Protoc 1:2916-2921.
21. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Wässle H (2004) Types of bipolar cells in the mouse retina. J Comp Neurol 469:70-82.
22. Gouras P, Link K (1966) Rod and cone interaction in dark-adapted monkey ganglion cells. J Physiol 184:499-510.
23. Grant GB, Dowling JE (1995) A glutamate-activated chloride current in cone-driven on bipolar cells of the white perch retina. J Neurosci 15:3852-3862.
24. Gregg RG, Kamermans M, Klooster J, Lukasiewicz PD, Peachey NS, Vessey KA, McCall MA (2007) Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. J Neurophysiol 98:3023-3033.
25. Hasegawa J, Obara T, Tanaka K, Tachibana M (2006) High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron 50:63-74.
26. Higgs MH, Lukasiewicz PD (1999) Glutamate uptake limits synaptic excitation of retinal ganglion cells. J Neurosci 19:3691-3700.
27. Hull C, Li GL, von Gersdorff H (2006) GABA transporters regulate a standing GABAC receptor-mediated current at a retinal presynaptic terminal. J Neurosci 26:6979-6984.
28. Kalbaugh TL, Zhang J, Diamond JS (2009) Coagonist release modulates NMDA receptor subtype contributions at synaptic inputs to retinal ganglion cells. J Neurosci 29:1469-1479.
29. Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M, Fukuda Y, Sasaki H, Hiroi K, Nakamura Y, Shigemoto R (1995) Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80:757-765.
30. Matsui K, Hosoi N, TachibanaM (1999) Active role of glutamate uptake in the synaptic transmission from retinal nonspiking neurons. J Neurosci 19:6755-6766.
31. Nelson R, Kolb H (1985) A17: a broad-field amacrine cell in the rod system of the cat retina. J Neurophysiol 54:592-614.
32. Otis TS, Jahr CE (1998) Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci 18:7099-7110.
33. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
34. Palmer MJ, Taschenberger H, Hull C, Tremere L, von Gersdorff H (2003) Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J Neurosci 23:4831-4841.
35. Picaud S, Larsson HP, Wellis DP, Lecar H, Werblin F (1995) Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc Natl Acad Sci U S A 92:9417-9421.
36. Pignatelli V, Strettoi E (2004) Bipolar cells of the mouse retina: a gene gun, morphological study. J Comp Neurol 476:254-266.
37. Pow DV, Barnett NL, Penfold P (2000) Are neuronal transporters relevant in retinal glutamate homeostasis? Neurochem Int 37:191-198.
38. Roska B, Werblin F (2001) Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410:583-587.
39. Rowan MJ, Ripps H, Shen W (2010) Fast glutamate uptake via EAAT2 shapes the cone-mediated light offset response in bipolar cells. J Physiol 588:3943-3956.
40. Shigeri Y, Shimamoto K, Yasuda-Kamatani Y, Seal RP, Yumoto N, Nakajima T, Amara SG (2001) Effects of threo-beta-hydroxyaspartate derivatives on excitatory amino acid transporters (EAAT4 and EAAT5). J Neurochem 79:297-302.
41. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, Nakajima T (1998) DL-threo-β-Benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53:195-201.
42. Snellman J, Nawy S (2002) Regulation of the retinal bipolar cell mGluR6 pathway by calcineurin. J Neurophysiol 88:1088-1096.
43. Snellman J, Zenisek D, Nawy S (2009) Switching between transient and sustained signalling at the rod bipolar-AII amacrine cell synapse of the mouse retina. J Physiol 587:2443-2455.
44. Steinberg RH (1969) The rod after-effect in S-potentials from the cat retina. Vision Res 9:1345-1355.
45. Szmajda BA, Devries SH (2011) Glutamate spillover between mammalian cone photoreceptors. J Neurosci 31:13431-13441.
46. Takahashi M, Sarantis M, Attwell D (1996) Postsynaptic glutamate uptake in rat cerebellar Purkinje cells. J Physiol 497:523-530.
47. Takayasu Y, Iino M, Kakegawa W, Maeno H, Watase K, Wada K, Yanagihara D, Miyazaki T, Komine O, Watanabe M, Tanaka K, Ozawa S (2005) Differential roles of glial and neuronal glutamate transporters in Purkinje cell synapses. J Neurosci 25:8788-8793.
48. Trexler EB, Li W, Massey SC (2005) Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. J Neurophysiol 93:1476-1485.
49. Veruki ML, Mørkve SH, Hartveit E (2006) Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nat Neurosci 9:1388-1396.
50. Vigh J, von Gersdorff H (2005) Prolonged reciprocal signaling via NMDA and GABA receptors at a retinal ribbon synapse. J Neurosci 25:11412-11423.
51. Vigh J, Vickers E, von Gersdorff H (2011) Light-evoked lateral GABAergic inhibition at single bipolar cell synaptic terminals is driven by distinct retinal microcircuits. J Neurosci 31:15884-15893.
52. Wadiche JI, Kavanaugh MP (1998) Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J Neurosci 18:7650-7661.
53. Wadiche JI, Amara SG, Kavanaugh MP (1995) Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-728.
54. Wadiche JI, Tzingounis AV, Jahr CE (2006) Intrinsic kinetics determine the time course of neuronal synaptic transporter currents. Proc Natl Acad Sci U S A 103:1083-1087.
55. WässleH (2004) Parallel processing in the mammalian retina. Nat Rev Neurosci 5:747-757.
56. Wässle H, Yamashita M, Greferath U, Grünert U, Müller F (1991) The rod bipolar cell of the mammalian retina. Vis Neurosci 7:99-112.
57. Wässle H, Puller C, Müller F, Haverkamp S (2009) Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29:106-117.
58. Wersinger E, Schwab Y, Sahel JA, Rendon A, Pow DV, Picaud S, Roux MJ (2006) The glutamate transporter EAAT5 works as a presynaptic receptor in mouse rod bipolar cells. J Physiol 577:221-234.
59. Xin D, Bloomfield SA (1999) Comparison of the responses of AII amacrine cells in the dark-and light-adapted rabbit retina. Vis Neurosci 16:653-665.