1932

Abstract

We know a good deal about the operation of the retina when either rod or cone photoreceptors provide the dominant input (i.e., under very dim or very bright conditions). However, we know much less about how the retina operates when rods and cones are coactive (i.e., under intermediate lighting conditions, such as dusk). Such mesopic conditions span 20–30% of the light levels over which vision operates and encompass many situations in which vision is essential (e.g., driving at night). These lighting conditions are challenging because rod and cone signals differ substantially: Rod responses are nearing saturation, while cone responses are weak and noisy. A rich history of perceptual studies guides our investigation of how the retina operates under mesopic conditions and in doing so provides a powerful opportunity to link general issues about parallel processing in neural circuits with computation and perception. We review some of the successes and challenges in understanding the retinal basis of perceptual rod-cone interactions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-091517-034055
2018-09-15
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/vision/4/1/annurev-vision-091517-034055.html?itemId=/content/journals/10.1146/annurev-vision-091517-034055&mimeType=html&fmt=ahah

Literature Cited

  1. Ala-Laurila P, Rieke F 2014. Coincidence detection of single-photon responses in the inner retina at the sensitivity limit of vision. Curr. Biol. 24:2888–98
    [Google Scholar]
  2. Arden GB, Hogg CR 1985. Rod-cone interactions and analysis of retinal disease. Br. J. Ophthalmol. 69:404–15
    [Google Scholar]
  3. Barlow HB, Levick WR, Yoon M 1971. Responses to single quanta of light in retinal ganglion cells of the cat. Vis. Res. 3:Suppl.87–101
    [Google Scholar]
  4. Baylor DA, Lamb TD, Yau KW 1979. Responses of retinal rods to single photons. J. Physiol. 288:613–34
    [Google Scholar]
  5. Baylor DA, Nunn BJ, Schnapf JL 1984. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. . Physiol 357:575–607
    [Google Scholar]
  6. Baylor DA, Nunn BJ, Schnapf JL 1987. Spectral sensitivity of cones of the monkey Macaca fascicularis. J. . Physiol 390:145–60
    [Google Scholar]
  7. Behrens C, Schubert T, Haverkamp S, Euler T, Berens P 2016. Connectivity map of bipolar cells and photoreceptors in the mouse retina. eLife 5:e20041
    [Google Scholar]
  8. Benimoff NI, Schneider S, Hood DC 1982. Interactions between rod and cone channels above threshold: a test of various models. Vis. Res. 22:1133–40
    [Google Scholar]
  9. Blick DW, MacLeod DI 1978. Rod threshold: influence of neighboring cones. Vis. Res. 18:1611–16
    [Google Scholar]
  10. Bloomfield SA, Dacheux RF 2001. Rod vision: pathways and processing in the mammalian retina. Prog. Retin. Eye Res. 20:351–84
    [Google Scholar]
  11. Boycott BB, Hopkins JM, Sperling HG 1987. Cone connections of the horizontal cells of the rhesus monkey's retina. Proc. R. Soc. B 229:345–79
    [Google Scholar]
  12. Buck SL 1985. Cone-rod interaction over time and space. Vis. Res. 25:907–16
    [Google Scholar]
  13. Buck SL 2004. Rod-cone interactions in human vision. The Visual Neurosciences LM Chalupa, JS Werner 863–78 Cambridge, MA: MIT Press
    [Google Scholar]
  14. Buck SL 2014. The interaction of rod and cone signals: pathways and psychophysics. The New Visual Neurosciences JS Werner, LM Chalupa 485–97 Cambridge, MA: MIT Press
    [Google Scholar]
  15. Buck SL, Pulos E 1987. Rod-cone interaction in monocular but not binocular pathways. Vis. Res. 27:479–82
    [Google Scholar]
  16. Burns ME, Baylor DA 2001. Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu. Rev. Neurosci. 24:779–805
    [Google Scholar]
  17. Cao D, Lee BB, Sun H 2010. Combination of rod and cone inputs in parasol ganglion cells of the magnocellular pathway. J. Vis. 10:114
    [Google Scholar]
  18. Cao D, Pokorny J, Smith VC 2005. Matching rod percepts with cone stimuli. Vis. Res. 45:2119–28
    [Google Scholar]
  19. Chichilnisky EJ 2001. A simple white noise analysis of neuronal light responses. Netw. Comput. Neural Syst. 12:199–213
    [Google Scholar]
  20. Cowan CS, Abd-El-Barr M, van der Heijden M, Lo EM, Paul D et al. 2016. Connexin 36 and rod bipolar cell independent rod pathways drive retinal ganglion cells and optokinetic reflexes. Vis. Res. 119:99–109
    [Google Scholar]
  21. Dacey DM, Diller LC, Verweij J, Williams DR 2000. Physiology of L- and M-cone inputs to H1 horizontal cells in the primate retina. J. Opt. Soc. Am. A 17:589–96
    [Google Scholar]
  22. Dacey DM, Packer OS 2003. Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr. Opin. Neurobiol. 13:421–27
    [Google Scholar]
  23. Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL 2002. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36:703–12
    [Google Scholar]
  24. Demb JB, Pugh EN 2002. Connexin36 forms synapses essential for night vision. Neuron 36:551–53
    [Google Scholar]
  25. Demb JB, Singer JH 2015. Functional circuitry of the retina. Annu. Rev. Vis. Sci. 1:263–89
    [Google Scholar]
  26. Donner K 1992. Noise and the absolute thresholds of cone and rod vision. Vis. Res. 32:853–66
    [Google Scholar]
  27. Drum B 1982. Summation of rod and cone responses at absolute threshold. Vis. Res. 22:823–26
    [Google Scholar]
  28. Dunn FA, Rieke F 2006. The impact of photoreceptor noise on retinal gain controls. Curr. Opin. Neurobiol. 16:363–70
    [Google Scholar]
  29. 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]
  30. 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]
  31. Enroth-Cugell C, Hertz BG, Lennie P 1977. Convergence of rod and cone signals in the cat's retina. J. Physiol. 269:297–318
    [Google Scholar]
  32. 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]
  33. Eysteinsson T, Frumkes TE 1989. Physiological and pharmacological analysis of suppressive rod-cone interaction in Necturus retina [corrected]. J. Neurophysiol. 61:866–77
    [Google Scholar]
  34. Field GD, Chichilnisky EJ 2007. Information processing in the primate retina: circuitry and coding. Annu. Rev. Neurosci. 30:1–30
    [Google Scholar]
  35. Field GD, Greschner M, Gauthier JL, Rangel C, Shlens J et al. 2009. High-sensitivity rod photoreceptor input to the blue-yellow color opponent pathway in macaque retina. Nat. Neurosci. 12:1159–64
    [Google Scholar]
  36. Field GD, Rieke F 2002. Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron 35:733–47
    [Google Scholar]
  37. Field GD, Sampath AP, Rieke F 2005. Retinal processing near absolute threshold: from behavior to mechanism. Annu. Rev. Physiol. 67:491–514
    [Google Scholar]
  38. Frumkes TE, Sekuler MD, Barris MC, Reiss EH, Chalupa LM 1973. Rod-cone interaction in human scotopic vision. I. Temporal analysis. Vis. Res. 13:1269–82
    [Google Scholar]
  39. Frumkes TE, Temme LA 1977. Rod-cone interaction in human scotopic vision–II. Cones influence rod increment thresholds. Vis. Res. 17:673–79
    [Google Scholar]
  40. Gouras P, Link K 1966. Rod and cone interaction in dark-adapted monkey ganglion cells. J. Physiol. 184:499–510
    [Google Scholar]
  41. Grimes WN, Graves LR, Summers MT, Rieke F 2015. A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates. eLife 4:e08033
    [Google Scholar]
  42. Grimes WN, Hoon M, Briggmann KL, Wong RO, Rieke F 2014.a Cross-synaptic synchrony and transmission of signal and noise across the mouse retina. eLife 3:e03892
    [Google Scholar]
  43. Grimes WN, Schwartz GW, Rieke F 2014.b The synaptic and circuit mechanisms underlying a change in spatial encoding in the retina. Neuron 82:460–73
    [Google Scholar]
  44. Hack I, Peichl L, Brandstatter JH 1999. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. PNAS 96:14130–35
    [Google Scholar]
  45. 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]
  46. Joesch M, Meister M 2016. A neuronal circuit for colour vision based on rod-cone opponency. Nature 532:236–39
    [Google Scholar]
  47. 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]
  48. Kilavik BE, Kremers J 2006. Interactions between rod and L-cone signals in deuteranopes: gains and phases. Vis. Neurosci. 23:201–7
    [Google Scholar]
  49. Kingdom FA 2011. Lightness, brightness and transparency: a quarter century of new ideas, captivating demonstrations and unrelenting controversy. Vis. Res. 51:652–73
    [Google Scholar]
  50. Kolb H 1977. The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations. J. Neurocytol. 6:131–53
    [Google Scholar]
  51. Kolb H, Famiglietti EV 1974. Rod and cone pathways in the inner plexiform layer of cat retina. Science 186:47–49
    [Google Scholar]
  52. Latch M, Lennie P 1977. Rod-cone interaction in light adaptation. J. Physiol. 269:517–34
    [Google Scholar]
  53. Lyubarsky AL, Falsini B, Pennesi ME, Valentini P, Pugh EN 1999. UV- and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments. J. Neurosci. 19:442–55
    [Google Scholar]
  54. MacLeod DI 1972. Rods cancel cones in flicker. Nature 235:173–74
    [Google Scholar]
  55. Mangel SC 1991. Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. J. Physiol. 442:211–34
    [Google Scholar]
  56. Mariani AP 1984. Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature 308:184–86
    [Google Scholar]
  57. Masland RH 2012. The neuronal organization of the retina. Neuron 76:266–80
    [Google Scholar]
  58. Mastronarde DN 1983. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J. Neurophysiol. 49:325–49
    [Google Scholar]
  59. Murphy GJ, Rieke F 2006. Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52:511–24
    [Google Scholar]
  60. Nelson R 1977. Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J. Comp. Neurol. 172:109–35
    [Google Scholar]
  61. Nelson R, Kolb H 1984. Amacrine cells in scotopic vision. Ophthalmic Res 16:21–26
    [Google Scholar]
  62. 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]
  63. Pang JJ, Gao F, Lem J, Bramblett DE, Paul DL, Wu SM 2010. Direct rod input to cone BCs and direct cone input to rod BCs challenge the traditional view of mammalian BC circuitry. PNAS 107:395–400
    [Google Scholar]
  64. Petzold A, Plant GT 2006. Clinical disorders affecting mesopic vision. Ophthalmic Physiol. Opt. 26:326–41
    [Google Scholar]
  65. Purkinje JE 1825. Neue Beiträge zur Kenntniss des Sehens in subjectiver Hinsicht Berlin: Reimer
  66. Raphael S, MacLeod DI 2011. Mesopic luminance assessed with minimum motion photometry. J. Vis. 11:914
    [Google Scholar]
  67. Rieke F 2008. Seeing in the dark: retinal processing and absolute visual threshold. The Senses: A Comprehensive Reference R Masland, T Albright 393–412 San Diego, CA: Academic
    [Google Scholar]
  68. Rushton WA 1972. Pigments and signals in colour vision. J. Physiol. 220:1P–31P
    [Google Scholar]
  69. Sampath AP, Rieke F 2004. Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41:431–43
    [Google Scholar]
  70. Schneeweis DM, Schnapf JL 1995. Photovoltage of rods and cones in the macaque retina. Science 268:1053–56
    [Google Scholar]
  71. Schneeweis DM, Schnapf JL 1999. The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J. Neurosci. 19:1203–16
    [Google Scholar]
  72. Sharpe LT, Stockman A 1999. Rod pathways: the importance of seeing nothing. Trends Neurosci 22:497–504
    [Google Scholar]
  73. Sharpe LT, Stockman A, MacLeod DI 1989. Rod flicker perception: scotopic duality, phase lags and destructive interference. Vis. Res. 29:1539–59
    [Google Scholar]
  74. Singer JH, Diamond JS 2003. Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J. Neurosci. 23:10923–33
    [Google Scholar]
  75. Solomon SG, Lennie P 2007. The machinery of colour vision. Nat. Rev. Neurosci. 8:276–86
    [Google Scholar]
  76. Soucy E, Wang Y, Nirenberg S, Nathans J, Meister M 1998. A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21:481–93
    [Google Scholar]
  77. Stiles WS 1939. The directional sensitivity of the retina and the spectral sensitivities of rods and cones. Proc. R. Soc. B 127:64–105
    [Google Scholar]
  78. Stiles WS, Burch JM 1959. N.P.L. colour-matching investigation: final report (1958). Opt. Acta 6:1–26
    [Google Scholar]
  79. Stockman A, Sharpe LT 2006. Into the twilight zone: the complexities of mesopic vision and luminous efficiency. Ophthalmic Physiol. Opt. 26:225–39
    [Google Scholar]
  80. Sun H, Pokorny J, Smith VC 2001. Rod-cone interactions assessed in inferred magnocellular and parvocellular postreceptoral pathways. J. Vis. 1:15
    [Google Scholar]
  81. Temme LA, Frumkes TE 1977. Rod-cone interaction in human scotopic vision–III: Rods influence cone increment thresholds. Vis. Res. 17:681–85
    [Google Scholar]
  82. Trexler EB, Li W, Massey SC 2005. Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. J. Neurophysiol. 93:1476–85
    [Google Scholar]
  83. Tsukamoto Y, Morigiwa K, Ueda M, Sterling P 2001. Microcircuits for night vision in mouse retina. J. Neurosci. 21:8616–23
    [Google Scholar]
  84. Tsukamoto Y, Omi N 2014. Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas. Front. Neuroanat. 8:105
    [Google Scholar]
  85. Tsukamoto Y, Omi N 2016. ON bipolar cells in macaque retina: type-specific synaptic connectivity with special reference to OFF counterparts. Front. Neuroanat. 10:104
    [Google Scholar]
  86. van den Berg TJ, Spekreijse H 1977. Interaction between rod and cone signals studied with temporal sine wave stimulation. J. Opt. Soc. Am. 67:1210–17
    [Google Scholar]
  87. Wandell BA 1995. Foundations of Vision Sunderland, MA: Sinauer
  88. Westheimer G 1970. Rod-cone independence for sensitizing interaction in the human retina. J. Physiol. 206:109–16
    [Google Scholar]
  89. Wu SM 2010. Synaptic organization of the vertebrate retina: general principles and species-specific variations: the Friedenwald lecture. Investig. Ophthalmol. Vis. Sci. 51:1264–74
    [Google Scholar]
/content/journals/10.1146/annurev-vision-091517-034055
Loading
/content/journals/10.1146/annurev-vision-091517-034055
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