Lateral Inhibition in the Vertebrate Retina: The Case of the Missing Neurotransmitter

PLoS Biology

Volumn 13, Issue 12, 2015, Pages

  Kramer, Richard H ^a   Davenport, Christopher M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM CHANNEL N TYPE; NERVE PROTEIN;

AGONISTS; ANIMAL; BIOLOGICAL MODEL; COMPARATIVE STUDY; CYTOLOGY; HEMISPHERIC DOMINANCE; HUMAN; METABOLISM; NERVE CELL INHIBITION; PH; PHYSIOLOGY; RETINA; RETINA CONE; RETINA HORIZONTAL NERVE CELL; RETINA ROD; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM CHANNELS, N-TYPE; FUNCTIONAL LATERALITY; GAMMA-AMINOBUTYRIC ACID; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NEURAL INHIBITION; RECEPTORS, GABA; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL HORIZONTAL CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPTIC TRANSMISSION;

EID: 84953276424     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002322     Document Type: Article

References (51)

1. Campbell FW, Robson JG, Application of fourier analysis to the visibility of gratings. J Physiol. 1968;197(3):551–66. 5666169
2. Thoreson WB, Mangel SC, Lateral interactions in the outer retina. Prog Retin Eye Res. 2012;31(5):407–41. doi: 10.1016/j.preteyeres.2012.04.003 22580106
3. DeVries SH, Li W, Saszik S, Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron. 2006;50(5):735–48. 16731512
4. Hubel DH, Wiesel TN, Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol. 1962;160(1):106–154.
5. Lopez-del Hoyo N, Fazioli L, Lopez-Begines S, Fernandez-Sanchez L, Cuenca N, Llorens J, et al. Overexpression of guanylate cyclase activating protein 2 in rod photoreceptors in vivo leads to morphological changes at the synaptic ribbon. PLoS ONE. 2012;7(8):e42994. doi: 10.1371/journal.pone.0042994 22912773
6. Hartline HK, Ratliff F, Spatial summation of inhibitory influences in the eye of limulus, and the mutual interaction of receptor units. J Gen Physiol. 1958;41(5):1049–66. 13525682
7. Kuffler SW, Discharge patterns and functional organization of the mammalian retina. J Neurophysiol. 1953;16(1):37–68. 13035466
8. Baylor DA, Fuortes MGF, O'Bryan PM, Receptive fields of cones in the retina of the turtle. J Physiol. 1971;214(2):265–294. 5579638
9. Cadetti L, Thoreson WB, Feedback Effects of Horizontal Cell Membrane Potential on Cone Calcium Currents Studied With Simultaneous Recordings. J Neurophysiol. 2006;95(3):1992–5. 16371457
10. Verweij J, Kamermans M, Spekreijse H, Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Res. 1996;36(24):3943–53. 9068848
11. Wu SM, Input-output relations of the feedback synapse between horizontal cells and cones in the tiger salamander retina. J Neurophysiol. 1991;65(5):1197–206. 1651374
12. Thoreson WB, Babai N, Bartoletti TM, Feedback from Horizontal Cells to Rod Photoreceptors in Vertebrate Retina. J Neurosci. 2008;28(22):5691–5. doi: 10.1523/JNEUROSCI.0403-08.2008 18509030
13. Tomita T, Electrophysiological Study of the Mechanisms Subserving Color Coding in the Fish Retina. Cold Spring Harb Symp Quant Biol. 1965;30:559–66. 5219504
14. Copenhagen DR, Jahr CE, Release of endogenous excitatory amino acids from turtle photoreceptors. Nature. 1989;341(6242):536–9. 2477707
15. Hurd LB, Eldred WD, Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Vis Neurosci. 1989;3(01):9–20.
16. Lam DM, Lasater EM, Naka KI, gamma-Aminobutyric acid: a neurotransmitter candidate for cone horizontal cells of the catfish retina. Proc Natl Acad Sci U S A. 1978;75(12):6310–3. 32538
17. Schwartz EA, Calcium-independent release of GABA from isolated horizontal cells of the toad retina. J Physiol. 1982;323(1):211–27.
18. Kaneko A, Tachibana M, Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. J Physiol. 1986;373(1):443–61.
19. Wu SM, Dowling JE, Effects of GABA and glycine on the distal cells of the cyprinid retina. Brain Res. 1980;199(2):401–14. 7417791
20. Lee H, Brecha NC, Immunocytochemical evidence for SNARE protein-dependent transmitter release from guinea pig horizontal cells. European J Neurosci. 2010;31(8):1388–401.
21. Rea R, Li J, Dharia A, Levitan ES, Sterling P, Kramer RH, Streamlined Synaptic Vesicle Cycle in Cone Photoreceptor Terminals. Neuron. 2004;41(5):755. 15003175
22. Raviola E, Gilula NB, Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol. 1975;65(1):192–222. 1127010
23. Lasater EM, Lam DMK, The identification and some functions of GABAergic neurons in the distal catfish retina. Vision Res. 1984;24(5):497–506. 6740969
24. Schwartz EA, Transport-mediated synapses in the retina. Physiol Rev. 2002;82(4):875–91. 12270946
25. Johnson J, Chen TK, Rickman DW, Evans C, Brecha NC, Multiple γ-aminobutyric acid plasma membrane transporters GAT-1, GAT-2, GAT-3 in the rat retina. J Comp Neurol. 1996;375(2):212–24. 8915826
26. Yazulla S, Studholme KM, Light adaptation affects synaptic vesicle density but not the distribution of GABAA receptors in goldfish photoreceptor terminals. Microsc Res Tech. 1997;36(1):43–56. 9031260
27. Thoreson WB, Burkhardt DA, Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Vis Neurosci. 1990;5(06):571–83.
28. Wu SM, Feedback connections and operation of the outer plexiform layer of the retina. Curr Op Neurobiol. 1992;2(4):462–8. 1525544
29. Byzov AL, Shura-Bura TM, Electrical feedback mechanism in the processing of signals in the outer plexiform layer of the retina. Vision Res. 1986;26(1):33–44. 3012877
30. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R, Hemichannel-mediated inhibition in the outer retina. Science. 2001;292(5519):1178–80. 11349152
31. Puller C, de Sevilla Moller LPr, Janssen-Bienhold U, Haverkamp S, ZO-1 and the spatial organization of gap junctions and glutamate receptors in the outer plexiform layer of the mammalian retina. J Neurosci. 2009;29(19):6266–75. doi: 10.1523/JNEUROSCI.5867-08.2009 19439604
32. Vessey JP, Lalonde MR, Mizan HA, Welch NC, Kelly MEM, Barnes S, Carbenoxolone Inhibition of Voltage-Gated Ca Channels and Synaptic Transmission in the Retina. J Neurophysiol. 2004;92(2):1252–6. 15028741
33. Klaassen LJ, Sun Z, Steijaert MN, Bolte P, Fahrenfort I, Sjoerdsma T, et al. Synaptic transmission from horizontal cells to cones is impaired by loss of connexin hemichannels. PLoS Biol. 2011;9(7):e1001107. doi: 10.1371/journal.pbio.1001107 21811399
34. Fahrenfort I, Klooster J, Sjoerdsma T, Kamermans M, The involvement of glutamate-gated channels in negative feedback from horizontal cells to cones. Prog Brai Res. 2005;147:219–29.
35. Barnes S, Bui Q, Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors. J Neurosci. 1991 Dec;11(12):4015–23. 1660538
36. Barnes S, Merchant V, Mahmud F, Modulation of transmission gain by protons at the photoreceptor output synapse. Proc Natl Acad Sci U S A. 1993;90(21):10081–5. 7694280
37. Hirasawa H, Kaneko A, pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J Gen Physiol. 2003;122(6):657–71. 14610018
38. Davenport CM, Detwiler PB, Dacey DM, Effects of pH buffering on horizontal and ganglion cell light responses in primate retina: Evidence for the Proton Hypothesis of Surround Formation. J Neurosci. 2008;28(2):456–64. doi: 10.1523/JNEUROSCI.2735-07.2008 18184788
39. Fahrenfort I, Steijaert M, Sjoerdsma T, Vickers E, Ripps H, van Asselt J, et al. Hemichannel-mediated and pH-based feedback from horizontal cells to cones in the vertebrate retina. PLoS ONE. 2009;4(6):e6090. doi: 10.1371/journal.pone.0006090 19564917
40. Trenholm S, Baldridge WH, The effect of aminosulfonate buffers on the light responses and intracellular pH of goldfish retinal horizontal cells. J Neurochem. 2010;115(1):102–11. doi: 10.1111/j.1471-4159.2010.06906.x 20633206
41. Jacoby J, Kreitzer MA, Alford S, Qian H, Tchernookova BK, Naylor ER, et al. Extracellular pH dynamics of retinal horizontal cells examined using electrochemical and fluorometric methods. J Neurophysiol. 2012;107(3):868–79. doi: 10.1152/jn.00878.2011 22090459
42. Kreitzer MA, Collis LP, Molina AJA, Smith PJS, Malchow RP, Modulation of extracellular proton fluxes from retinal horizontal cells of the catfish by depolarization and glutamate. J Gen Physiol. 2007;130(2):169–82. 17664345
43. Wang T- M, Holzhausen LC, Kramer RH, Imaging an optogenetic pH sensor reveals that protons mediate lateral inhibition in the retina. Nat Neurosci. 2014;17(2):262–8. doi: 10.1038/nn.3627 24441679
44. Vessey JP, Stratis AK, Daniels BA, Da Silva N, Jonz MG, Lalonde MR, et al. Proton-mediated feedback inhibition of presynaptic calcium channels at the cone photoreceptor synapse. J Neurosci. 2005; 25(16):4108–17. 15843613
45. Jouhou H, Yamamoto K, Homma A, Hara M, Kaneko A, Yamada M, Depolarization of isolated horizontal cells of fish acidifies their immediate surrounding by activating V-ATPase. J Physiol. 2007;585(2):401–12.
46. Blot A, Barbour B, Ultra-rapid axon-axon ephaptic inhibition of cerebellar Purkinje cells by the pinceau. Nat Neurosci. 2014;17(2):289–95. doi: 10.1038/nn.3624 24413696
47. Furukawa T, Furshpan EJ, Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol. 1963;26(1):140–76.
48. Knopfel T, Gallero-Salas Y, Song C, Genetically encoded voltage indicators for large scale cortical imaging come of age. Curr Opin Chem Biol. 2015;27:75–83. doi: 10.1016/j.cbpa.2015.06.006 26115448
49. Liu X, Hirano AA, Sun X, Brecha NC, Barnes S, Calcium channels in rat horizontal cells regulate feedback inhibition of photoreceptors through an unconventional GABA- and pH-sensitive mechanism. J Physiol. 2013;591(13):3309–24.
50. Vroman R, Klaassen LJ, Howlett MHC, Cenedese V, Klooster J, Sjoerdsma T, et al. Extracellular ATP hydrolysis inhibits synaptic transmission by increasing pH buffering in the synaptic cleft. PLoS Biol. 2014;12(5):e1001864. doi: 10.1371/journal.pbio.1001864 24844296
51. Kemmler R, Schultz K, Dedek K, Euler T, Schubert T, Differential regulation of cone calcium signals by different horizontal cell feedback mechanisms in the mouse retina. J Neurosci. 2014;34(35):11826–43. doi: 10.1523/JNEUROSCI.0272-14.2014 25164677