1932

Abstract

The mammalian retina is an important model system for studying neural circuitry: Its role in sensation is clear, its cell types are relatively well defined, and its responses to natural stimuli—light patterns—can be studied in vitro. To solve the retina, we need to understand how the circuits presynaptic to its output neurons, ganglion cells, divide the visual scene into parallel representations to be assembled and interpreted by the brain. This requires identifying the component interneurons and understanding how their intrinsic properties and synapses generate circuit behaviors. Because the cellular composition and fundamental properties of the retina are shared across species, basic mechanisms studied in the genetically modifiable mouse retina apply to primate vision. We propose that the apparent complexity of retinal computation derives from a straightforward mechanism—a dynamic balance of synaptic excitation and inhibition regulated by use-dependent synaptic depression—applied differentially to the parallel pathways that feed ganglion cells.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-082114-035334
2015-11-24
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/vision/1/1/annurev-vision-082114-035334.html?itemId=/content/journals/10.1146/annurev-vision-082114-035334&mimeType=html&fmt=ahah

Literature Cited

  1. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD. et al. 2000. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27:513–23 [Google Scholar]
  2. Asari H, Meister M. 2012. Divergence of visual channels in the inner retina. Nat. Neurosci. 15:1581–89 [Google Scholar]
  3. Baccus SA, Meister M. 2002. Fast and slow contrast adaptation in retinal circuitry. Neuron 36:909–19 [Google Scholar]
  4. Baccus SA, Olveczky BP, Manu M, Meister M. 2008. A retinal circuit that computes object motion. J. Neurosci. 28:6807–17 [Google Scholar]
  5. Baden T, Esposti F, Nikolaev A, Lagnado L. 2011. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr. Biol. 21:1859–69 [Google Scholar]
  6. Baden T, Schubert T, Chang L, Wei T, Zaichuk M. et al. 2013. A tale of two retinal domains: near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron 80:1206–17 [Google Scholar]
  7. Baylor D. 1996. How photons start vision. PNAS 93:560–65 [Google Scholar]
  8. Beier KT, Borghuis BG, El-Danaf RN, Huberman AD, Demb JB, Cepko CL. 2013. Transsynaptic tracing with vesicular stomatitis virus reveals novel retinal circuitry. J. Neurosci. 33:135–51 [Google Scholar]
  9. Blankenship AG, Feller MB. 2010. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat. Rev. Neurosci. 11:18–29 [Google Scholar]
  10. Bleckert A, Schwartz GW, Turner MH, Rieke F, Wong RO. 2014. Visual space is represented by nonmatching topographies of distinct mouse retinal ganglion cell types. Curr. Biol. 24:310–15 [Google Scholar]
  11. Bloomfield SA, Völgyi B. 2009. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat. Rev. Neurosci. 10:495–506 [Google Scholar]
  12. Bölinger D, Gollisch T. 2012. Closed-loop measurements of iso-response stimuli reveal dynamic nonlinear stimulus integration in the retina. Neuron 73:333–46 [Google Scholar]
  13. Borghuis BG, Looger LL, Tomita S, Demb JB. 2014. Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina. J. Neurosci. 34:6128–39 [Google Scholar]
  14. Borghuis BG, Marvin JS, Looger LL, Demb JB. 2013. Two-photon imaging of nonlinear glutamate release dynamics at bipolar cell synapses in the mouse retina. J. Neurosci. 33:10972–85 [Google Scholar]
  15. Borghuis BG, Ratliff CP, Smith RG, Sterling P, Balasubramanian V. 2008. Design of a neuronal array. J. Neurosci. 28:3178–89 [Google Scholar]
  16. Boycott BB, Wässle H. 1991. Morphological classification of bipolar cells of the primate retina. Eur. J. Neurosci. 3:1069–88 [Google Scholar]
  17. Briggman KL, Euler T. 2011. Bulk electroporation and population calcium imaging in the adult mammalian retina. J. Neurophysiol. 105:2601–9 [Google Scholar]
  18. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–88 [Google Scholar]
  19. Buldyrev I, Puthussery T, Taylor WR. 2012. Synaptic pathways that shape the excitatory drive in an OFF retinal ganglion cell. J. Neurophysiol. 107:1795–807 [Google Scholar]
  20. Cafaro J, Rieke F. 2010. Noise correlations improve response fidelity and stimulus encoding. Nature 468:964–67 [Google Scholar]
  21. Cafaro J, Rieke F. 2013. Regulation of spatial selectivity by crossover inhibition. J. Neurosci. 33:6310–20 [Google Scholar]
  22. Chavez AE, Singer JH, Diamond JS. 2006. Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443:705–8 [Google Scholar]
  23. Chen S, Li W. 2012. A color-coding amacrine cell may provide a blue-Off signal in a mammalian retina. Nat. Neurosci. 15:954–56 [Google Scholar]
  24. Cleland BG, Dubin MW, Levick WR. 1971. Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J. Physiol. 217:473–96 [Google Scholar]
  25. Cohen E, Sterling P. 1992. Parallel circuits from cones to the on-beta ganglion cell. Eur. J. Neurosci. 4:506–20 [Google Scholar]
  26. Connaughton VP, Graham D, Nelson R. 2004. Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. J. Comp. Neurol. 477:371–85 [Google Scholar]
  27. Crook JD, Davenport CM, Peterson BB, Packer OS, Detwiler PB, Dacey DM. 2009. Parallel ON and OFF cone bipolar inputs establish spatially coextensive receptive field structure of blue-yellow ganglion cells in primate retina. J. Neurosci. 29:8372–87 [Google Scholar]
  28. Crook JD, Manookin MB, Packer OS, Dacey DM. 2011. Horizontal cell feedback without cone type-selective inhibition mediates “red–green” color opponency in midget ganglion cells of the primate retina. J. Neurosci. 31:1762–72 [Google Scholar]
  29. Crook JD, Packer OS, Dacey DM. 2014. A synaptic signature for ON- and OFF-center parasol ganglion cells of the primate retina. Vis. Neurosci. 31:57–84 [Google Scholar]
  30. Cui J, Pan ZH. 2008. Two types of cone bipolar cells express voltage-gated Na+ channels in the rat retina. Vis. Neurosci. 25:635–45 [Google Scholar]
  31. Dacey DM, Crook JD, Packer OS. 2014. Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina. Vis. Neurosci. 31:139–51 [Google Scholar]
  32. 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]
  33. de la Villa P, Vaquero CF, Kaneko A. 1998. Two types of calcium currents of the mouse bipolar cells recorded in the retinal slice preparation. Eur. J. Neurosci. 10:317–23 [Google Scholar]
  34. Demb JB. 2008. Functional circuitry of visual adaptation in the retina. J. Physiol. 586:4377–84 [Google Scholar]
  35. Demb JB, Singer JH. 2012. Intrinsic properties and functional circuitry of the AII amacrine cell. Vis. Neurosci. 29:51–60 [Google Scholar]
  36. Demb JB, Zaghloul K, Haarsma L, Sterling P. 2001. Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. J. Neurosci. 21:7447–54 [Google Scholar]
  37. DeVries SH. 2000. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28:847–56 [Google Scholar]
  38. DeVries SH, Li W, Saszik S. 2006. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50:735–48 [Google Scholar]
  39. Dhande OS, Stafford BK, Lim A, Huberman AD. 2015. Retinal ganglion cell and subcortical contributions to visual feature selectivity. Annu. Rev. Vis. Sci. 1291–328
  40. Do MT, Yau KW. 2010. Intrinsically photosensitive retinal ganglion cells. Physiol. Rev. 90:1547–81 [Google Scholar]
  41. Duan X, Krishnaswamy A, de la Huerta I, Sanes JR. 2014. Type II cadherins guide assembly of a direction-selective retinal circuit. Cell 158:793–807 [Google Scholar]
  42. Dumitrescu ON, Pucci FG, Wong KY, Berson DM. 2009. Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells. J. Comp. Neurol. 517:226–44 [Google Scholar]
  43. Dunn FA, Doan T, Sampath AP, Rieke F. 2006. Controlling the gain of rod-mediated signals in the mammalian retina. J. Neurosci. 26:3959–70 [Google Scholar]
  44. Dunn FA, Lankheet MJ, Rieke F. 2007. Light adaptation in cone vision involves switching between receptor and post-receptor sites. Nature 449:603–6 [Google Scholar]
  45. Dunn FA, Rieke F. 2006. The impact of photoreceptor noise on retinal gain controls. Curr. Opin. Neurobiol. 16:363–70 [Google Scholar]
  46. Dunn FA, Rieke F. 2008. Single-photon absorptions evoke synaptic depression in the retina to extend the operational range of rod vision. Neuron 57:894–904 [Google Scholar]
  47. Dunn FA, Wong RO. 2014. Wiring patterns in the mouse retina: collecting evidence across the connectome, physiology and light microscopy. J. Physiol. 592:4809–23 [Google Scholar]
  48. Eggers ED, Lukasiewicz PD. 2011. Multiple pathways of inhibition shape bipolar cell responses in the retina. Vis. Neurosci. 28:95–108 [Google Scholar]
  49. Enroth-Cugell C, Robson JG. 1966. The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol. 187:517–52 [Google Scholar]
  50. Euler T, Detwiler PB, Denk W. 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:845–52 [Google Scholar]
  51. Euler T, Haverkamp S, Schubert T, Baden T. 2014. Retinal bipolar cells: elementary building blocks of vision. Nat. Rev. Neurosci. 15:507–19 [Google Scholar]
  52. Fain GL, Matthews HR. 1990. Calcium and the mechanism of light adaptation in vertebrate photoreceptors. Trends Neurosci. 13:378–84 [Google Scholar]
  53. Farrow K, Teixeira M, Szikra T, Viney TJ, Balint K. et al. 2013. Ambient illumination toggles a neuronal circuit switch in the retina and visual perception at cone threshold. Neuron 78:325–38 [Google Scholar]
  54. Field GD, Gauthier JL, Sher A, Greschner M, Machado TA. et al. 2010. Functional connectivity in the retina at the resolution of photoreceptors. Nature 467:673–77 [Google Scholar]
  55. Freed MA, Sterling P. 1988. The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. J. Neurosci. 8:2303–20 [Google Scholar]
  56. Garvert MM, Gollisch T. 2013. Local and global contrast adaptation in retinal ganglion cells. Neuron 77:915–28 [Google Scholar]
  57. Gollisch T, Meister M. 2010. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65:150–64 [Google Scholar]
  58. Grimes WN, Hoon M, Briggman KL, Wong RO, Rieke F. 2014a. Cross-synaptic synchrony and transmission of signal and noise across the mouse retina. eLife 3:e03892 [Google Scholar]
  59. Grimes WN, Li W, Chavez AE, Diamond JS. 2009. BK channels modulate pre- and postsynaptic signaling at reciprocal synapses in retina. Nat. Neurosci. 12:585–92 [Google Scholar]
  60. Grimes WN, Schwartz GW, Rieke F. 2014b. The synaptic and circuit mechanisms underlying a change in spatial encoding in the retina. Neuron 82:460–73 [Google Scholar]
  61. 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]
  62. Guo C, Hirano AA, Stella SL Jr, Bitzer M, Brecha NC. 2010. Guinea pig horizontal cells express GABA, the GABA-synthesizing enzyme GAD 65, and the GABA vesicular transporter. J. Comp. Neurol. 518:1647–69 [Google Scholar]
  63. Haverkamp S, Wassle H, Duebel J, Kuner T, Augustine GJ. et al. 2005. The primordial, blue-cone color system of the mouse retina. J. Neurosci. 25:5438–45 [Google Scholar]
  64. 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]
  65. 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]
  66. Hochstein S, Shapley RM. 1976. Quantitative analysis of retinal ganglion cell classifications. J. Physiol. 262:237–64 [Google Scholar]
  67. Hoggarth A, McLaughlin AJ, Ronellenfitch K, Trenholm S, Vasandani R. et al. 2015. Specific wiring of distinct amacrine cells in the directionally selective retinal circuit permits independent coding of direction and size. Neuron 86:1276–91 [Google Scholar]
  68. Hoshi H, Liu WL, Massey SC, Mills SL. 2009. ON inputs to the OFF layer: bipolar cells that break the stratification rules of the retina. J. Neurosci. 29:8875–83 [Google Scholar]
  69. Hu C, Bi A, Pan ZH. 2009. Differential expression of three T-type calcium channels in retinal bipolar cells in rats. Vis. Neurosci. 26:177–87 [Google Scholar]
  70. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB. et al. 2008. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59:425–38 [Google Scholar]
  71. Ichinose T, Fyk-Kolodziej B, Cohn J. 2014. Roles of ON cone bipolar cell subtypes in temporal coding in the mouse retina. J. Neurosci. 34:8761–71 [Google Scholar]
  72. Ichinose T, Shields CR, Lukasiewicz PD. 2005. Sodium channels in transient retinal bipolar cells enhance visual responses in ganglion cells. J. Neurosci. 25:1856–65 [Google Scholar]
  73. Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH. 2009. Role of the synaptic ribbon in transmitting the cone light response. Nat. Neurosci. 12:303–10 [Google Scholar]
  74. Jacobs GH, Neitz J, Deegan JF 2nd. 1991. Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353:655–56 [Google Scholar]
  75. Jacobs GH, Williams GA. 2007. Contributions of the mouse UV photopigment to the ERG and to vision. Doc. Ophthalmol. 115:137–44 [Google Scholar]
  76. Jarsky T, Cembrowski M, Logan SM, Kath WL, Riecke H. et al. 2011. A synaptic mechanism for retinal adaptation to luminance and contrast. J. Neurosci. 31:11003–15 [Google Scholar]
  77. Jones RS, Carroll RC, Nawy S. 2012. Light-induced plasticity of synaptic AMPA receptor composition in retinal ganglion cells. Neuron 75:467–78 [Google Scholar]
  78. Kaplan E, Benardete E. 2001. The dynamics of primate retinal ganglion cells. Prog. Brain Res. 134:17–34 [Google Scholar]
  79. Kastner DB, Baccus SA. 2011. Coordinated dynamic encoding in the retina using opposing forms of plasticity. Nat. Neurosci. 14:1317–22 [Google Scholar]
  80. Kastner DB, Baccus SA. 2013. Spatial segregation of adaptation and predictive sensitization in retinal ganglion cells. Neuron 79:541–54 [Google Scholar]
  81. Ke JB, Wang YV, Borghuis BG, Cembrowski MS, Riecke H. et al. 2014. Adaptation to background light enables contrast coding at rod bipolar cell synapses. Neuron 81:388–401 [Google Scholar]
  82. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR. 2008. Molecular identification of a retinal cell type that responds to upward motion. Nature 452:478–82 [Google Scholar]
  83. Kim JS, Greene MJ, Zlateski A, Lee K, Richardson M. et al. 2014. Space–time wiring specificity supports direction selectivity in the retina. Nature 509:331–36 [Google Scholar]
  84. 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]
  85. Klug K, Herr S, Ngo IT, Sterling P, Schein S. 2003. Macaque retina contains an S-cone OFF midget pathway. J. Neurosci. 23:9881–87 [Google Scholar]
  86. Kolb H, Marshak D. 2003. The midget pathways of the primate retina. Doc. Ophthalmol. 106:67–81 [Google Scholar]
  87. Kolb H, Nelson R. 1993. OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. J. Comp. Neurol. 329:85–110 [Google Scholar]
  88. Kouyama N, Marshak DW. 1992. Bipolar cells specific for blue cones in the macaque retina. J. Neurosci. 12:1233–52 [Google Scholar]
  89. Kuffler SW. 1953. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16:37–68 [Google Scholar]
  90. Lamb TD. 2009. Evolution of vertebrate retinal photoreception. Philos. Trans. R. Soc. B 364:23 [Google Scholar]
  91. Lee BB, Martin PR, Grünert U. 2010. Retinal connectivity and primate vision. Prog. Retin. Eye Res. 29:622–39 [Google Scholar]
  92. 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]
  93. LeGates TA, Fernandez DC, Hattar S. 2014. Light as a central modulator of circadian rhythms, sleep and affect. Nat. Rev. Neurosci. 15:443–54 [Google Scholar]
  94. Li W, DeVries SH. 2006. Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nat. Neurosci. 9:669–75 [Google Scholar]
  95. Lindstrom SH, Ryan DG, Shi J, DeVries SH. 2014. Kainate receptor subunit diversity underlying response diversity in retinal off bipolar cells. J. Physiol. 592:1457–77 [Google Scholar]
  96. Manookin MB, Weick M, Stafford BK, Demb JB. 2010. NMDA receptor contributions to visual contrast coding. Neuron 67:280–93 [Google Scholar]
  97. Manu M, Baccus SA. 2011. Disinhibitory gating of reitnal output by transmission from an amacrine cell. PNAS 108:4518447–52 [Google Scholar]
  98. Marc RE, Jones BW, Watt CB, Anderson JR, Sigulinsky C, Lauritzen S. 2013. Retinal connectomics: towards complete, accurate networks. Prog. Retin. Eye Res. 37:141–62 [Google Scholar]
  99. Martemyanov KA. 2014. G protein signaling in the retina and beyond: the Cogan lecture. Investig. Ophthalmol. Vis. Sci. 55:8201–7 [Google Scholar]
  100. Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT. et al. 2013. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat. Methods 10:162–70 [Google Scholar]
  101. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:266–80 [Google Scholar]
  102. Mennerick S, Matthews G. 1996. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17:1241–49 [Google Scholar]
  103. Mills SL, Tian LM, Hoshi H, Whitaker CM, Massey SC. 2014. Three distinct blue-green color pathways in a mammalian retina. J. Neurosci. 34:1760–68 [Google Scholar]
  104. Morgans CW, Zhang J, Jeffrey BG, Nelson SM, Burke NS. et al. 2009. TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. PNAS 106:19174–78 [Google Scholar]
  105. 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]
  106. Nikolaev A, Leung KM, Odermatt B, Lagnado L. 2013. Synaptic mechanisms of adaptation and sensitization in the retina. Nat. Neurosci. 16:934–41 [Google Scholar]
  107. Nikonov SS, Kholodenko R, Lem J, Pugh EN Jr. 2006. Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J. Gen. Physiol. 127:359–74 [Google Scholar]
  108. Odermatt B, Nikolaev A, Lagnado L. 2012. Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 73:758–73 [Google Scholar]
  109. Oesch N, Euler T, Taylor WR. 2005. Direction-selective dendritic action potentials in rabbit retina. Neuron 47:739–50 [Google Scholar]
  110. Oesch NW, Diamond JS. 2011. Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat. Neurosci. 14:1555–61 [Google Scholar]
  111. Okawa H, Hoon M, Yoshimatsu T, Della Santina L, Wong RO. 2014. Illuminating the multifaceted roles of neurotransmission in shaping neuronal circuitry. Neuron 83:1303–18 [Google Scholar]
  112. Oltedal L, Hartveit E. 2010. Transient release kinetics of rod bipolar cells revealed by capacitance measurement of exocytosis from axon terminals in rat retinal slices. J. Physiol. 588:1469–87 [Google Scholar]
  113. Olveczky BP, Baccus SA, Meister M. 2003. Segregation of object and background motion in the retina. Nature 423:401–8 [Google Scholar]
  114. Ozuysal Y, Baccus SA. 2012. Linking the computational structure of variance adaptation to biophysical mechanisms. Neuron 73:1002–15 [Google Scholar]
  115. Packer OS, Verweij J, Li PH, Schnapf JL, Dacey DM. 2010. Blue-yellow opponency in primate S cone photoreceptors. J. Neurosci. 30:568–72 [Google Scholar]
  116. Pan F, Paul DL, Bloomfield SA, Volgyi B. 2010. Connexin36 is required for gap junctional coupling of most ganglion cell subtypes in the mouse retina. J. Comp. Neurol. 518:911–27 [Google Scholar]
  117. Park SJH, Kim I-J, Looger LL, Demb JB, Borghuis BG. 2014. Excitatory synaptic inputs to mouse On-Off direction-selective retinal ganglion cells lack direction tuning. J. Neurosci. 34:3976–81 [Google Scholar]
  118. Park SJH, Borghuis BG, Rahamani P, Zeng Q, Kim IJ, Demb JB. 2015. Function and circuitry of VIP+ interneurons in the mouse retina. J. Neurosci. 35:10685–700 [Google Scholar]
  119. Pearson JT, Kerschensteiner. 2015. Ambient illuminantion switches contrast preference of specific retinal processing streams. J. Neurophysiol. 114:540–50 [Google Scholar]
  120. Poleg-Polsky A, Diamond JS. 2011. Imperfect space clamp permits electrotonic interactions between inhibitory and excitatory synaptic conductances, distorting voltage clamp recordings. PLOS ONE 6:e19463 [Google Scholar]
  121. Protti DA, Flores-Herr N, von Gersdorff H. 2000. Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25:215–27 [Google Scholar]
  122. Puller C, Haverkamp S, Neitz M, Neitz J. 2014. Synaptic elements for GABAergic feed-forward signaling between HII horizontal cells and blue cone bipolar cells are enriched beneath primate S-cones. PLOS ONE 9:e88963 [Google Scholar]
  123. Puthussery T, Percival KA, Venkataramani S, Gayet-Primo J, Grunert U, Taylor WR. 2014. Kainate receptors mediate synaptic input to transient and sustained OFF visual pathways in primate retina. J. Neurosci. 34:7611–21 [Google Scholar]
  124. Reinagel P, Zador AM. 1999. Natural scene statistics at the centre of gaze. Network 10:341–50 [Google Scholar]
  125. Rivlin-Etzion M, Wei W, Feller MB. 2012. Visual stimulation reverses the directional preference of direction-selective retinal ganglion cells. Neuron 76:518–25 [Google Scholar]
  126. Roska B, Werblin F. 2001. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410:583–87 [Google Scholar]
  127. Russell TL, Werblin FS. 2010. Retinal synaptic pathways underlying the response of the rabbit local edge detector. J. Neurophysiol. 103:2757–69 [Google Scholar]
  128. Sanes JR, Masland RH. 2015. The types of retinal ganglion cells: current status and implications for neuronal classification. Annu. Rev. Neurosci. 38:221–46 [Google Scholar]
  129. Saszik S, DeVries SH. 2012. A mammalian retinal bipolar cell uses both graded changes in membrane voltage and all-or-nothing Na+ spikes to encode light. J. Neurosci. 32:297–307 [Google Scholar]
  130. Schneeweis DM, Schnapf JL. 1999. The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J. Neurosci. 19:1203–16 [Google Scholar]
  131. Schwartz G, Rieke F. 2011. Perspectives on: information and coding in mammalian sensory physiology: nonlinear spatial encoding by retinal ganglion cells: when 1 + 1 ≠ 2. J. Gen. Physiol. 138:3283–90 [Google Scholar]
  132. Schwartz GW, Okawa H, Dunn FA, Morgan JL, Kerschensteiner D. et al. 2012. The spatial structure of a nonlinear receptive field. Nat. Neurosci. 15:1572–80 [Google Scholar]
  133. Seung HS, Sümbül U. 2014. Neuronal cell types and connectivity: lessons from the retina. Neuron 83:1262–72 [Google Scholar]
  134. Shapley RM, Enroth-Cugell C. 1984. Visual adaptation and retinal gain controls. Prog. Retin. Res. 3:263–346 [Google Scholar]
  135. Sher A, DeVries SH. 2012. A non-canonical pathway for mammalian blue-green color vision. Nat. Neurosci. 15:952–53 [Google Scholar]
  136. Singer JH, Diamond JS. 2003. Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J. Neurosci. 23:10923–33 [Google Scholar]
  137. Singer JH, Diamond JS. 2006. Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J. Neurophysiol. 95:3191–98 [Google Scholar]
  138. Sivyer B, Williams SR. 2013. Direction selectivity is computed by active dendritic integration in retinal ganglion cells. Nat. Neurosci. 16:1848–56 [Google Scholar]
  139. Solomon SG, Kohn A. 2014. Moving sensory adaptation beyond suppressive effects in single neurons. Curr. Biol. 24:R1012–22 [Google Scholar]
  140. Stafford BK, Manookin MB, Singer JH, Demb JB. 2014. NMDA and AMPA receptors contribute similarly to temporal processing in mammalian retinal ganglion cells. J. Physiol. 592:4877–89 [Google Scholar]
  141. Szikra T, Trenholm S, Drinnenberg A, Juttner J, Raics Z. et al. 2014. Rods in daylight act as relay cells for cone-driven horizontal cell-mediated surround inhibition. Nat. Neurosci. 17:1728–35 [Google Scholar]
  142. Szmajda BA, Devries SH. 2011. Glutamate spillover between mammalian cone photoreceptors. J. Neurosci. 31:13431–41 [Google Scholar]
  143. Thoreson WB, Mangel SC. 2012. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31:407–41 [Google Scholar]
  144. Tikidji-Hamburyan A, Reinhard K, Seitter H, Hovhannisyan A, Procyk CA. et al. 2015. Retinal output changes qualitatively with every change in ambient illuminance. Nat. Neurosci. 18:66–74 [Google Scholar]
  145. Trenholm S, McLaughlin AJ, Schwab DJ, Turner MH, Smith RG. et al. 2014. Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations. Nat. Neurosci. 17:1759–66 [Google Scholar]
  146. Trenholm S, Schwab DJ, Balasubramanian V, Awatramani GB. 2013. Lag normalization in an electrically coupled neural network. Nat. Neurosci. 16:154–56 [Google Scholar]
  147. Vaney DI, Sivyer B, Taylor WR. 2012. Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat. Rev. Neurosci. 13:194–208 [Google Scholar]
  148. Venkataramani S, Taylor WR. 2010. Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition. J. Neurosci. 30:15664–76 [Google Scholar]
  149. Venkataramani S, Van Wyk M, Buldyrev I, Sivyer B, Vaney DI, Taylor WR. 2014. Distinct roles for inhibition in spatial and temporal tuning of local edge detectors in the rabbit retina. PLOS ONE 9:e88560 [Google Scholar]
  150. Veruki ML, Morkve SH, Hartveit E. 2006. Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nat. Neurosci. 9:1388–96 [Google Scholar]
  151. Vlasits AL, Bos R, Morrie RD, Fortuny C, Flannery JG. et al. 2014. Visual stimulation switches the polarity of excitatory input to starburst amacrine cells. Neuron 83:1172–84 [Google Scholar]
  152. von Gersdorff H, Sakaba T, Berglund K, Tachibana M. 1998. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21:1177–88 [Google Scholar]
  153. Vroman R, Klaassen LJ, Howlett MH, Cenedese V, Klooster J. et al. 2014. Extracellular ATP hydrolysis inhibits synaptic transmission by increasing pH buffering in the synaptic cleft. PLOS Biol. 12:e1001864 [Google Scholar]
  154. Wang TM, Holzhausen LC, Kramer RH. 2014. Imaging an optogenetic pH sensor reveals that protons mediate lateral inhibition in the retina. Nat. Neurosci. 17:262–68 [Google Scholar]
  155. Wang YV, Weick M, Demb JB. 2011. Spectral and temporal sensitivity of cone-mediated responses in mouse retinal ganglion cells. J. Neurosci. 31:7670–81 [Google Scholar]
  156. Wässle 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]
  157. Weick M, Demb JB. 2011. Delayed-rectifier K channels contribute to contrast adaptation in mammalian retinal ganglion cells. Neuron 71:166–79 [Google Scholar]
  158. Weiler R, Pottek M, He S, Vaney DI. 2000. Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Res. Brain Res. Rev. 32:1121–29 [Google Scholar]
  159. Werblin FS. 2010. Six different roles for crossover inhibition in the retina: correcting the nonlinearities of synaptic transmission. Vis. Neurosci. 27:1–8 [Google Scholar]
  160. Williams DR. 2011. Imaging single cells in the living retina. Vis. Res. 51:1379–96 [Google Scholar]
  161. Yin L, Smith RG, Sterling P, Brainard DH. 2006. Chromatic properties of horizontal and ganglion cell responses follow a dual gradient in cone opsin expression. J. Neurosci. 26:12351–61 [Google Scholar]
  162. Yin L, Smith RG, Sterling P, Brainard DH. 2009. Physiology and morphology of color-opponent ganglion cells in a retina expressing a dual gradient of S and M opsins. J. Neurosci. 29:2706–24 [Google Scholar]
  163. Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K. et al. 2013. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79:1078–85 [Google Scholar]
  164. Zaghloul KA, Manookin MB, Borghuis BG, Boahen K, Demb JB. 2007. Functional circuitry for peripheral suppression in mammalian Y-type retinal ganglion cells. J. Neurophysiol. 97:4327–40 [Google Scholar]
  165. Zhang AJ, Wu SM. 2009. Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic circuitry. J. Neurosci. 29:789–97 [Google Scholar]
  166. Zhang Y, Kim IJ, 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]
  167. Zhang C, McCall MA. 2012. Receptor targets of amacrine cells. Vis. Neurosci. 29:111–29 [Google Scholar]
  168. Zhou ZY, Wan QF, Thakur P, Heidelberger R. 2006. Capacitance measurements in the mouse rod bipolar cell identify a pool of releasable synaptic vesicles. J. Neurophysiol. 96:2539–48 [Google Scholar]
  169. Zhu Y, Xu J, Hauswirth WW, DeVries SH. 2014. Genetically targeted binary labeling of retinal neurons. J. Neurosci. 34:7845–61 [Google Scholar]
/content/journals/10.1146/annurev-vision-082114-035334
Loading
/content/journals/10.1146/annurev-vision-082114-035334
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error