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Annual Review of Vision Science

Volume 3, 2017

Inhibitory Interneurons in the Retina: Types, Circuitry, and Function*

Abstract

Visual signals in the vertebrate retina are shaped by feedback and feedforward inhibition in two synaptic layers. In one, horizontal cells establish fundamental center-surround receptive-field properties via morphologically and physiologically complex synapses with photoreceptors and bipolar cells. In the other, a panoply of amacrine cells imbue ganglion cell responses with spatiotemporally complex information about the visual world. Here, I review current ideas about horizontal cell signaling, considering the evidence for and against the leading, competing theories. I also discuss recent work that has begun to make sense of the remarkable morphological and physiological diversity of amacrine cells. These latter efforts have been aided tremendously by increasingly complete connectivity maps of inner retinal circuitry and new genetic tools that enable study of individual, sparsely expressed amacrine cell types.

Keyword(s): amacrine cell, feedback inhibition, feedforward inhibition, horizontal cell, visual processing
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2017-09-15
2024-05-09
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Literature Cited

  1. Adrian ED, Matthews R. 1928. The action of light on the eye: part III. The interaction of retinal neurones. J. Physiol. 65:273–98 [Google Scholar]
  2. Akrouh A, Kerschensteiner D. 2015. Morphology and function of three VIP-expressing amacrine cell types in the mouse retina. J. Neurophysiol. 114:2431–38 [Google Scholar]
  3. Anderson JR, Jones BW, Watt CB, Shaw MV, Yang JH. et al. 2011. Exploring the retinal connectome.. Mol. Vis. 17:355–79 [Google Scholar]
  4. Ariel M, Daw NW. 1982. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J. Physiol. 324:161–85 [Google Scholar]
  5. Baden T, Berens P, Franke K, Román Rosón M, Bethge M, Euler T. 2016. The functional diversity of retinal ganglion cells in the mouse. Nature 529:345–50 [Google Scholar]
  6. Barlow HB, Levick WR. 1965. The mechanism of directionally selective units in rabbit's retina. J. Physiol. 178:477–504 [Google Scholar]
  7. Barnes S, Bui Q. 1991. Modulation of calcium-activated chloride current via pH-induced changes of calcium-channel properties in cone photoreceptors. J. Neurosci. 11:4015–23 [Google Scholar]
  8. Baylor DA, Fuortes MG, O'Bryan PM. 1971. Receptive fields of cones in the retina of the turtle. J. Physiol. 214:265–94 [Google Scholar]
  9. Bloomfield SA, Volgyi B. 2004. Function and plasticity of homologous coupling between AII amacrine cells. Vis. Res. 44:3297–306 [Google Scholar]
  10. Bloomfield SA, Volgyi B. 2007. Response properties of a unique subtype of wide-field amacrine cell in the rabbit retina. Vis. Neurosci. 24:459–69 [Google Scholar]
  11. Boos R, Schneider H, Wassle H. 1993. Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. J. Neurosci. 13:2874–88 [Google Scholar]
  12. Borgula GA, Karwoski CJ, Steinberg RH. 1989. Light-evoked changes in extracellular pH in frog retina. Vis. Res. 29:1069–77 [Google Scholar]
  13. Boycott BB, Peichl L, Wassle H. 1978. Morphological types of horizontal cell in the retina of the domestic cat. Proc. R. Soc. Lond. B 203:229–45 [Google Scholar]
  14. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–88 [Google Scholar]
  15. Byzov AL, Cervetto L. 1977. Effects of applied currents on turtle cones in darkness and during the photoresponse. J. Physiol. 265:85–102 [Google Scholar]
  16. Byzov AL, Shura-Bura TM. 1986. Electrical feedback mechanism in the processing of signals in the outer plexiform layer of the retina. Vis. Res 26:33–44 [Google Scholar]
  17. Cadetti L, Thoreson WB. 2006. Feedback effects of horizontal cell membrane potential on cone calcium currents studied with simultaneous recordings. J. Neurophysiol. 95:1992–95 [Google Scholar]
  18. Casini G, Brecha NC. 1992. Colocalization of vasoactive intestinal polypeptide and GABA immunoreactivities in a population of wide-field amacrine cells in the rabbit retina. Vis. Neurosci. 8:373–78 [Google Scholar]
  19. Cembrowski MS, Logan SM, Tian M, Jia L, Li W. et al. 2012. The mechanisms of repetitive spike generation in an axonless retinal interneuron. Cell Rep 1:155–66 [Google Scholar]
  20. Chávez AE, Diamond JS. 2008. Diverse mechanisms underlie glycinergic feedback transmission onto rod bipolar cells in rat retina. J. Neurosci. 28:7919–28 [Google Scholar]
  21. Chávez AE, Singer JH, Diamond JS. 2006. Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443:705–8 [Google Scholar]
  22. Contini M, Raviola E. 2003. GABAergic synapses made by a retinal dopaminergic neuron. PNAS 100:1358–63 [Google Scholar]
  23. Dacey DM. 1989. Axon-bearing amacrine cells of the macaque monkey retina. J. Comp. Neurol. 284:275–93 [Google Scholar]
  24. Dacheux RF, Raviola E. 1986. The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. J. Neurosci. 6:331–45 [Google Scholar]
  25. Dale H. 1935. Pharmacology and nerve-endings (Walter Ernest Dixon Memorial Lecture). Proc. R. Soc. Med. 28:319–32 [Google Scholar]
  26. Davenport CM, Detwiler PB, Dacey DM. 2008. Effects of pH buffering on horizontal and ganglion cell light responses in primate retina: evidence for the proton hypothesis of surround formation. J. Neurosci. 28:456–64 [Google Scholar]
  27. de Vries SE, Baccus SA, Meister M. 2011. The projective field of a retinal amacrine cell. J. Neurosci. 31:8595–604 [Google Scholar]
  28. Demb JB, Singer JH. 2015. Functional circuitry of the retina. Annu. Rev. Vis. Sci. 1:263–89 [Google Scholar]
  29. DeVries SH. 2001. Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron 32:1107–17 [Google Scholar]
  30. DeVries SH, Li W, Saszik S. 2006. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50:735–48 [Google Scholar]
  31. Ding H, Smith RG, Poleg-Polsky A, Diamond JS, Briggman KL. 2016. Species-specific wiring for direction selectivity in the mammalian retina. Nature 535:105–10 [Google Scholar]
  32. Dixon DB, Takahashi KI, Copenhagen DR. 1993. L-Glutamate suppresses HVA calcium current in catfish horizontal cells by raising intracellular proton concentration. Neuron 11:267–77 [Google Scholar]
  33. Dmitriev AV, Mangel SC. 2006. Electrical feedback in the cone pedicle: a computational analysis. J. Neurophysiol. 95:1419–27 [Google Scholar]
  34. Dong CJ, Hare WA. 2003. Temporal modulation of scotopic visual signals by A17 amacrine cells in mammalian retina in vivo. J. Neurophysiol. 89:2159–66 [Google Scholar]
  35. Dowling JE. 2012. The Retina: An Approachable Part of the Brain Cambridge, MA: Belknap Press. Revis. ed.
  36. Dowling JE, Boycott BB. 1966. Organization of the primate retina: electron microscopy. Proc. R. Soc. Lond. B 166:80–111 [Google Scholar]
  37. Duebel J, Haverkamp S, Schleich W, Feng GP, Augustine GJ. et al. 2006. Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor clomeleon. Neuron 49:81–94 [Google Scholar]
  38. Eggers ED, Lukasiewicz PD. 2006. GABAA, GABAC and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. J. Physiol. 572:215–25 [Google Scholar]
  39. Eggers ED, Lukasiewicz PD. 2010. Interneuron circuits tune inhibition in retinal bipolar cells. J. Neurophysiol. 103:25–37 [Google Scholar]
  40. Euler T, Detwiler PB, Denk W. 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:845–52 [Google Scholar]
  41. Famiglietti EV. 1991. Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J. Comp. Neurol. 309:40–70 [Google Scholar]
  42. Famiglietti EV Jr., Kolb H. 1975. A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Res 84:293–300 [Google Scholar]
  43. Feller MB, Wellis DP, Stellwagen D, Werblin FS, Shatz CJ. 1996. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272:1182–87 [Google Scholar]
  44. Flores-Herr N, Protti DA, Wassle H. 2001. Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. J. Neurosci. 21:4852–63 [Google Scholar]
  45. Fried SI, Munch TA, Werblin FS. 2002. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420:411–14 [Google Scholar]
  46. Gerschenfeld HM, Piccolino M, Neyton J. 1980. Feedback modulation of cone synapses by L-horizontal cells of turtle retina. J. Exp. Biol. 89:177–92 [Google Scholar]
  47. Greferath U, Grunert U, Muller F, Wassle H. 1994. Localization of GABAA receptors in the rabbit retina. Cell Tissue Res 276:295–307 [Google Scholar]
  48. Grimes WN, Seal RP, Oesch N, Edwards RH, Diamond JS. 2011. Genetic targeting and physiological features of VGLUT3+ amacrine cells. Vis. Neurosci. 28:381–92 [Google Scholar]
  49. Grimes WN, Zhang J, Graydon CW, Kachar B, Diamond JS. 2010. Retinal parallel processors: More than 100 independent microcircuits operate within a single interneuron. Neuron 65:873–85 [Google Scholar]
  50. Grimes WN, Zhang J, Tian H, Graydon CW, Hoon M. et al. 2015. Complex inhibitory microcircuitry regulates signaling near visual threshold. J. Neurophysiol. 114:341–53 [Google Scholar]
  51. Hampson ECGM, Vaney DI, Weiler R. 1992. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. J. Neurosci. 12:4911–22 [Google Scholar]
  52. Hare WA, Owen WG. 1992. Effects of 2-amino-4-phosphonobutyric acid on cells in the distal layers of the tiger salamander's retina. J. Physiol. 445:741–57 [Google Scholar]
  53. Hare WA, Owen WG. 1996. Receptive field of the retinal bipolar cell: a pharmacological study in the tiger salamander. J. Neurophysiol. 76:2005–19 [Google Scholar]
  54. Harmar AJ, Sheward WJ, Morrison CF, Waser B, Gugger M, Reubi JC. 2004. Distribution of the VPAC2 receptor in peripheral tissues of the mouse. Endocrinology 145:1203–10 [Google Scholar]
  55. Hartline HK, Wagner HG, Ratliff F. 1956. Inhibition in the eye of Limulus. J. Gen. Physiol. 39:651–73 [Google Scholar]
  56. Hausselt SE, Euler T, Detwiler PB, Denk W. 2007. A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLOS Biol 5:e185 [Google Scholar]
  57. Haverkamp S, Wassle H. 2004. Characterization of an amacrine cell type of the mammalian retina immunoreactive for vesicular glutamate transporter 3. J. Comp. Neurol. 468:251–63 [Google Scholar]
  58. Helmstaedter M, Briggman KL, Turaga SC, Jain V, Seung HS, Denk W. 2013. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500:168–74 [Google Scholar]
  59. Herrmann R, Heflin SJ, Hammond T, Lee B, Wang J. et al. 2011. Rod vision is controlled by dopamine-dependent sensitization of rod bipolar cells by GABA. Neuron 72:101–10 [Google Scholar]
  60. Hirano AA, Brandstatter JH, Brecha NC. 2005. Cellular distribution and subcellular localization of molecular components of vesicular transmitter release in horizontal cells of rabbit retina. J. Comp. Neurol. 488:70–81 [Google Scholar]
  61. Hirano AA, Liu X, Grove JCR, Pérez de Sevilla Müller L, Barnes S, Brecha NC. 2016. Targeted deletion of vesicular GABA transporter from retinal horizontal cells eliminates feedback modulation of photoreceptor calcium channels. eNeuro 3:1–13 [Google Scholar]
  62. Hirasawa H, Betensky RA, Raviola E. 2012. Corelease of dopamine and GABA by a retinal dopaminergic neuron. J. Neurosci. 32:13281–91 [Google Scholar]
  63. Hirasawa H, Kaneko A. 2003. pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J. Gen. Physiol. 122:657–71 [Google Scholar]
  64. Hokfelt T. 1991. Neuropeptides in perspective: the last ten years. Neuron 7:867–79 [Google Scholar]
  65. Ivanova E, Hwang GS, Pan ZH. 2010. Characterization of transgenic mouse lines expressing Cre recombinase in the retina. Neuroscience 165:233–43 [Google Scholar]
  66. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R. 2001. Hemichannel-mediated inhibition in the outer retina. Science 292:1178–80 [Google Scholar]
  67. Kaneko A, Tachibana M. 1986. Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. J. Physiol. 373:443–61 [Google Scholar]
  68. Kim T, Soto F, Kerschensteiner D. 2015. An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in the mouse retina. eLife 4:e08025 [Google Scholar]
  69. Kittila CA, Massey SC. 1997. Pharmacology of directionally selective ganglion cells in the rabbit retina. J. Neurophysiol. 77:675–89 [Google Scholar]
  70. Kolb H. 1974. The connections between horizontal cells and photoreceptors in the retina of the cat: electron microscopy of Golgi preparations. J. Comp. Neurol. 155:1–14 [Google Scholar]
  71. Kolb H, Cuenca N, Dekorver L. 1991. Postembedding immunocytochemistry for GABA and glycine reveals the synaptic relationships of the dopaminergic amacrine cell of the cat retina. J. Comp. Neurol. 310:267–84 [Google Scholar]
  72. Kolb H, Famiglietti EV. 1974. Rod and cone pathways in the inner plexiform layer of cat retina. Science 186:47–49 [Google Scholar]
  73. Kosaka T, Kosaka K, Hataguchi Y, Nagatsu I, Wu JY. et al. 1987. Catecholaminergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp. Brain Res. 66:191–210 [Google Scholar]
  74. Kothmann WW, Massey SC, O'Brien J. 2009. Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. J. Neurosci. 29:14903–11 [Google Scholar]
  75. Kothmann WW, Trexler EB, Whitaker CM, Li W, Massey SC, O'Brien J. 2012. Nonsynaptic NMDA receptors mediate activity-dependent plasticity of gap junctional coupling in the AII amacrine cell network. J. Neurosci. 32:6747–59 [Google Scholar]
  76. Kuffler SW. 1953. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16:37–68 [Google Scholar]
  77. Lee S, Chen L, Chen M, Ye M, Seal RP, Zhou ZJ. 2014. An unconventional glutamatergic circuit in the retina formed by vGluT3 amacrine cells. Neuron 84:708–15 [Google Scholar]
  78. Lee S, Chen M, Zhang Y, Chen L, Zhou ZJ. 2015. Synaptic properties of vGluT3 amacrine cells in the mouse retina. Investig. Ophthalmol. Vis. Sci. 56:4377 [Google Scholar]
  79. Lee S, Kim K, Zhou ZJ. 2010. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68:1159–72 [Google Scholar]
  80. Lee S, Zhang Y, Chen M, Zhou ZJ. 2016. Segregated glycine-glutamate co-transmission from vGluT3 amacrine cells to contrast-suppressed and contrast-enhanced retinal circuits. Neuron 90:27–34 [Google Scholar]
  81. Lee S, Zhou ZJ. 2006. The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51:787–99 [Google Scholar]
  82. Levick WR. 1967. Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina. J. Physiol. 188:285–307 [Google Scholar]
  83. Lin B, Masland RH. 2008. Populations of wide-field amacrine cells in the mouse retina. J. Comp. Neurol. 508:983–83 [Google Scholar]
  84. Liu X, Hirano AA, Sun XP, Brecha NC, Barnes S. 2013. Calcium channels in rat horizontal cells regulate feedback inhibition of photoreceptors through an unconventional GABA- and pH-sensitive mechanism. J. Physiol. 591:3309–24 [Google Scholar]
  85. MacNeil MA, Masland RH. 1998. Extreme diversity among amacrine cells: implications for function. Neuron 20:971–82 [Google Scholar]
  86. Mangel SC, Dowling JE. 1985. Responsiveness and receptive-field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229:1107–09 [Google Scholar]
  87. Manookin MB, Beaudoin DL, Ernst ZR, Flagel LJ, Demb JB. 2008. Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J. Neurosci. 28:4136–50 [Google Scholar]
  88. Manookin MB, Puller C, Rieke F, Neitz J, Neitz M. 2015. Distinctive receptive field and physiological properties of a wide-field amacrine cell in the macaque monkey retina. J. Neurophysiol. 114:1606–16 [Google Scholar]
  89. Marchiafava PL. 1978. Horizontal cells influence membrane potential of bipolar cells in retina of turtle. Nature 275:141–42 [Google Scholar]
  90. Masland RH. 2012. The tasks of amacrine cells. Vis. Neurosci. 29:3–9 [Google Scholar]
  91. Meister M, Wong RO, Baylor DA, Shatz CJ. 1991. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939–43 [Google Scholar]
  92. Miller RF, Dacheux RF. 1983. Intracellular chloride in retinal neurons: measurement and meaning. Vis. Res. 23:399–411 [Google Scholar]
  93. Munch TA, da Silveira RA, Siegert S, Viney TJ, Awatramani GB, Roska B. 2009. Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat. Neurosci. 12:1308–16 [Google Scholar]
  94. Munch TA, Werblin FS. 2006. Symmetric interactions within a homogeneous starburst cell network can lead to robust asymmetries in dendrites of starburst amacrine cells. J. Neurophysiol. 96:471–77 [Google Scholar]
  95. Murphy GJ, Rieke F. 2008. Signals and noise in an inhibitory interneuron diverge to control activity in nearby retinal ganglion cells. Nat. Neurosci. 11:318–26 [Google Scholar]
  96. Nelson R, Kolb H. 1985. A17: a broad-field amacrine cell in the rod system of the cat retina. J. Neurophysiol. 54:592–614 [Google Scholar]
  97. Nguyen-Legros J, Versaux-Botteri C, Vernier P. 1999. Dopamine receptor localization in the mammalian retina. Mol. Neurobiol. 19:181–204 [Google Scholar]
  98. O'Bryan PM. 1973. Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. J. Physiol. 235:207–23 [Google Scholar]
  99. O'Malley DM, Masland RH. 1989. Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. PNAS 86:3414–18 [Google Scholar]
  100. Park SJH, Borghuis BG, Rahmani P, Zeng Q, Kim I-J, Demb JB. 2015. Function and circuitry of VIP+ interneurons in the mouse retina. J. Neurosci. 35:10685–700 [Google Scholar]
  101. Polyak SL. 1941. The Retina Chicago: Univ. Chicago Press
  102. Pourcho RG. 1982. Dopaminergic amacrine cells in the cat retina. Brain Res 252:101–9 [Google Scholar]
  103. Pourcho RG, Goebel DJ. 1985. Immunocytochemical demonstration of glycine in retina. Brain Res 348:339–42 [Google Scholar]
  104. Ramón y Cajal S. 1892. La rétine des vertébrés. La Céllule 9:119–257 [Google Scholar]
  105. Ribelayga C, Cao Y, Mangel SC. 2008. The circadian clock in the retina controls rod-cone coupling. Neuron 59:790–801 [Google Scholar]
  106. Rodieck RW. 1998. The First Steps in Seeing Sunderland, MA: Sinauer Assoc.
  107. Roska B, Nemeth E, Werblin FS. 1998. Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. J. Neurosci. 18:3451–59 [Google Scholar]
  108. Roska B, Werblin F. 2001. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410:583–87 [Google Scholar]
  109. Sandell JH, Masland RH. 1986. A system of indoleamine-accumulating neurons in the rabbit retina. J. Neurosci. 6:3331–47 [Google Scholar]
  110. Siegert S, Scherf BG, Del Punta K, Didkovsky N, Heintz N, Roska B. 2009. Genetic address book for retinal cell types. Nat. Neurosci. 12:1197–204 [Google Scholar]
  111. Sterling P. 1998. The retina. The Synaptic Organization of the Brain GM Shepherd 205–54 New York: Oxford Univ. Press [Google Scholar]
  112. Strang CE, Renna JM, Amthor FR, Keyser KT. 2010. Muscarinic acetylcholine receptor localization and activation effects on ganglion response properties. Investig. Ophthalmol. Vis. Sci. 51:2778–89 [Google Scholar]
  113. Strettoi E, Raviola E, Dacheux RF. 1992. Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. J. Comp. Neurol. 325:152–68 [Google Scholar]
  114. Sulzer D, Rayport S. 2000. Dale's principle and glutamate corelease from ventral midbrain dopamine neurons. Amino Acids 19:45–52 [Google Scholar]
  115. Thoreson WB, Babai N, Bartoletti TM. 2008. Feedback from horizontal cells to rod photoreceptors in vertebrate retina. J. Neurosci. 28:5691–95 [Google Scholar]
  116. Thoreson WB, Bryson EJ. 2004. Chloride equilibrium potential in salamander cones. BMC Neurosci 5:53 [Google Scholar]
  117. Thoreson WB, Burkhardt DA. 1990. Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Vis. Neurosci. 5:571–83 [Google Scholar]
  118. Thoreson WB, Mangel SC. 2012. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31:407–41 [Google Scholar]
  119. Tian M, Jarsky T, Murphy GJ, Rieke F, Singer JH. 2010. Voltage-gated Na channels in AII amacrine cells accelerate scotopic light responses mediated by the rod bipolar cell pathway. J. Neurosci. 30:4650–59 [Google Scholar]
  120. Tien NW, Kim T, Kerschensteiner D. 2016. Target-specific glycinergic transmission from VGluT3-expressing amacrine cells shapes suppressive contrast responses in the retina. Cell Rep 15:1369–75 [Google Scholar]
  121. Tien NW, Pearson JT, Heller CR, Demas J, Kerschensteiner D. 2015. Genetically identified suppressed-by-contrast retinal ganglion cells reliably signal self-generated visual stimuli. J. Neurosci. 35:10815–20 [Google Scholar]
  122. Tomita T. 1965. Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harb. Symp. Quant. Biol. 30:559–66 [Google Scholar]
  123. Tornqvist K, Uddman R, Sundler F, Ehinger B. 1982. Somatostatin and VIP neurons in the retina of different species. Histochemistry 76:137–52 [Google Scholar]
  124. Trenholm S, Baldridge WH. 2010. The effect of aminosulfonate buffers on the light responses and intracellular pH of goldfish retinal horizontal cells. J. Neurochem. 115:102–11 [Google Scholar]
  125. van Wyk M, Wassle H, Taylor WR. 2009. Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Vis. Neurosci. 26:297–308 [Google Scholar]
  126. Vaney DI. 1985. The morphology and topographic distribution of AII amacrine cells in the cat retina. Proc. R. Soc. Lond. B 224:475–88 [Google Scholar]
  127. Vaney DI. 1994. Patterns of neuronal coupling in the retina. Prog. Retin. Eye Res. 13:301–55 [Google Scholar]
  128. Vardi N, Smith RG. 1996. The AII amacrine network: Coupling can increase correlated activity. Vis. Res. 36:3743–57 [Google Scholar]
  129. Vardi N, Sterling P. 1994. Subcellular localization of GABAA receptor on bipolar cells in macaque and human retina. Vis. Res. 34:1235–46 [Google Scholar]
  130. Vardi N, Zhang LL, Payne JA, Sterling P. 2000. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J. Neurosci. 20:7657–63 [Google Scholar]
  131. Verweij J, Hornstein EP, Schnapf JL. 2003. Surround antagonism in macaque cone photoreceptors. J. Neurosci. 23:10249–57 [Google Scholar]
  132. Verweij J, Kamermans M, Spekreijse H. 1996. Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vis. Res. 36:3943–53 [Google Scholar]
  133. Vlasits AL, Morrie RD, Tran-Van-Minh A, Bleckert A, Gainer CF. et al. 2016. A role for synaptic input distribution in a dendritic computation of motion direction in the retina. Neuron 89:1317–30 [Google Scholar]
  134. Vu TQ, Payne JA, Copenhagen DR. 2000. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J. Neurosci. 20:1414–23 [Google Scholar]
  135. Warren TJ, Van Hook MJ, Tranchina D, Thoreson WB. 2016. Kinetics of inhibitory feedback from horizontal cells to photoreceptors: implications for an ephaptic mechanism. J. Neurosci. 36:10075–88 [Google Scholar]
  136. Wassle H, Puller C, Muller F, Haverkamp S. 2009. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J. Neurosci. 29:106–17 [Google Scholar]
  137. Wassle H, Riemann HJ. 1978. Mosaic of nerve cells in mammalian retina. Proc. R. Soc. B 200:441–61 [Google Scholar]
  138. Werblin FS. 1970. Response of retinal cells to moving spots: intracellular recording in Necturus maculosus. . J. Neurophysiol. 33:342–50 [Google Scholar]
  139. Werblin FS, Copenhagen DR. 1974. Control of retinal sensitivity. 3. Lateral interactions at the inner plexiform layer. J. Gen. Physiol. 63:88–110 [Google Scholar]
  140. Werblin FS, Dowling JE. 1969. Organization of the retina of the mudpuppy, Necturusmaculosus. II. Intracellular recording. J. Neurophysiol. 32:339–55 [Google Scholar]
  141. Wong WT, Myhr KL, Miller ED, Wong ROL. 2000. Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. J. Neurosci. 20:351–60 [Google Scholar]
  142. Xu HP, Furman M, Mineur YS, Chen H, King SL. et al. 2011. An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 70:1115–27 [Google Scholar]
  143. Yang XL. 2004. Characterization of receptors for glutamate and GABA in retinal neurons. Prog. Neurobiol. 73:127–50 [Google Scholar]
  144. Yang XL, Wu SM. 1991. Feedforward lateral inhibition in retinal bipolar cells: input-output relation of the horizontal cell-depolarizing bipolar cell synapse. PNAS 88:3310–13 [Google Scholar]
  145. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Roska B. 2011. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469:407–10 [Google Scholar]
  146. Zampighi GA, Schietroma C, Zampighi LM, Woodruff M, Wright EM, Brecha NC. 2011. Conical tomography of a ribbon synapse: structural evidence for vesicle fusion. PLOS ONE 6:e16944 [Google Scholar]
  147. Zhang J, Jung CS, Slaughter MM. 1997. Serial inhibitory synapses in retina. Vis. Neurosci. 14:553–63 [Google Scholar]
  148. Zhang Y, Kim I-J, Sanes JR, Meister M. 2012. The most numerous ganglion cell type of the mouse retina is a selective feature detector. PNAS 109:E2391–98 [Google Scholar]
  149. Zheng J-j, Lee S, Zhou ZJ. 2004. A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44:851–64 [Google Scholar]
  150. Zhou ZJ, Zhao DC. 2000. Coordinated transitions in neurotransmitter systems for the initiation and propagation of spontaneous retinal waves. J. Neurosci. 20:6570–77 [Google Scholar]
  151. Zhu Y, Xu J, Hauswirth WW, DeVries SH. 2014. Genetically targeted binary labeling of retinal neurons. J. Neurosci. 34:7845–61 [Google Scholar]
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Inhibitory Interneurons in the Retina: Types, Circuitry, and Function*
Annual Review of Vision Science 3, 1 (2017); https://doi.org/10.1146/annurev-vision-102016-061345
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