1932

Abstract

Every aspect of visual perception and behavior is built from the neural activity of retinal ganglion cells (RGCs), the output neurons of the eye. Here, we review progress toward understanding the many types of RGCs that communicate visual signals to the brain, along with the subcortical brain regions that use those signals to build and respond to representations of the outside world. We emphasize recent progress in the use of mouse genetics, viral circuit tracing, and behavioral psychophysics to define and map the various RGCs and their associated networks. We also address questions about the homology of RGC types in mice and other species including nonhuman primates and humans. Finally, we propose a framework for understanding RGC typology and for highlighting the relationship between RGC type-specific circuitry and the processing stations in the brain that support and give rise to the perception of sight.

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2015-11-24
2024-04-26
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Literature Cited

  1. Abrahamson EE, Moore RY. 2001. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 916:1–2172–91 [Google Scholar]
  2. Ackman JB, Crair MC. 2014. Role of emergent neural activity in visual map development. Curr. Opin. Neurobiol. 24:1166–75 [Google Scholar]
  3. Acuna-Goycolea C, Brenowitz SD, Regehr WG. 2008. Active dendritic conductances dynamically regulate GABA release from thalamic interneurons. Neuron 57:3420–31 [Google Scholar]
  4. Ahmadlou M, Heimel JA. 2015. Preference for concentric orientations in the mouse superior colliculus. Nat. Commun. 6:6773 [Google Scholar]
  5. Allen AE, Storchi R, Martial FP, Petersen RS, Montemurro MA. et al. 2014. Melanopsin-driven light adaptation in mouse vision. Curr. Biol. 24:212481–90 [Google Scholar]
  6. Amir S, Stewart J. 1996. Resetting of the circadian clock by a conditioned stimulus. Nature 379:6565542–45 [Google Scholar]
  7. Assali A, Gaspar P, Rebsam A. 2014. Activity dependent mechanisms of visual map formation—from retinal waves to molecular regulators. Semin. Cell Dev. Biol. 35:136–46 [Google Scholar]
  8. Azeredo da Silveira R, Roska B. 2011. Cell types, circuits, computation. Curr. Opin. Neurobiol. 21:664–71 [Google Scholar]
  9. Badea TC, Cahill H, Ecker J, Hattar S, Nathans J. 2009. Distinct roles of transcription factors Brn3a and Brn3b in controlling the development, morphology, and function of retinal ganglion cells. Neuron 61:6852–64 [Google Scholar]
  10. Barlow HB, Fitzhugh R, Kuffler SW. 1957. Change of organization in the receptive fields of the cat's retina during dark adaptation. J. Physiol. 137:3327–37 [Google Scholar]
  11. Barlow HB, Hill RM. 1963. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139:3553412–14 [Google Scholar]
  12. Baver SB, Pickard GE, Sollars PJ, Pickard GE. 2008. Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur. J. Neurosci. 27:1763–70 [Google Scholar]
  13. Berson DM. 1988. Retinal and cortical inputs to cat superior colliculus: composition, convergence and laminar specificity. Prog. Brain Res. 75:17–26 [Google Scholar]
  14. Berson DM. 2008. Retinal ganglion cell types and their central projections. The Senses: A Comprehensive Reference 1 AI Basbaum, A Kaneko, GM Shepherd, G Westheimer 491–520 San Diego: Academic [Google Scholar]
  15. Berson DM. 2013. Intrinsically photosensitive retinal ganglion cells. The New Visual Neurosciences JS Werner, LM Chalupa 183–196 Cambridge, MA: MIT Press [Google Scholar]
  16. Berson DM, Castrucci AM, Provencio I. 2010. Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J. Comp. Neurol. 518:132405–22 [Google Scholar]
  17. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:55571070–73 [Google Scholar]
  18. Bickford ME, Zhou N, Krahe TE, Govindaiah G, Guido W. 2015. Retinal and tectal “driver-like” inputs converge in the shell of the mouse dorsal lateral geniculate nucleus. J. Neurosci. 35:10523–34 [Google Scholar]
  19. Blasdel GG, Salama G. 1986. Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:6070579–85 [Google Scholar]
  20. Bleckert A, Schwartz GW, Turner MH, Rieke F, Wong ROL. 2014. Visual space is represented by nonmatching topographies of distinct mouse retinal ganglion cell types. Curr. Biol. 24:3310–15 [Google Scholar]
  21. Bloomfield SA. 1994. Orientation-sensitive amacrine and ganglion cells in the rabbit retina. J. Neurophysiol. 71:51672–91 [Google Scholar]
  22. Bonhoeffer T, Grinvald A. 1991. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353:6343429–31 [Google Scholar]
  23. Bonin V, Histed MH, Yurgenson S, Reid RC. 2011. Local diversity and fine-scale organization of receptive fields in mouse visual cortex. J. Neurosci. 31:5018506–21 [Google Scholar]
  24. Bowling DB, Michael CR. 1980. Projection patterns of single physiologically characterized optic tract fibres in cat. Nature 286:5776899–902 [Google Scholar]
  25. Boycott BB, Wässle H. 1974. The morphological types of ganglion cells of the domestic cat's retina. J. Physiol. 240:397–419 [Google Scholar]
  26. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:7337183–88 [Google Scholar]
  27. Brown TM, Gias C, Hatori M, Keding SR, Semo M. et al. 2010. Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. PLOS Biol. 8:12e1000558 [Google Scholar]
  28. Campbell FW, Gregory AH. 1960. Effect of size of pupil on visual acuity. Nature 187:1121–23 [Google Scholar]
  29. Cang J, Feldheim DA. 2013. Developmental mechanisms of topographic map formation and alignment. Annu. Rev. Neurosci. 36:51–77 [Google Scholar]
  30. Chalupa LM, Rhoades RW. 1977. Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus. J. Physiol. 270:3595–626 [Google Scholar]
  31. Chen C, Regehr WG. 2000. Developmental remodeling of the retinogeniculate synapse. Neuron 28:3955–66 [Google Scholar]
  32. Chen S-K, Badea TC, Hattar S. 2011. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 476:92–95 [Google Scholar]
  33. Cheong SK, Tailby C, Solomon SG, Martin PR. 2013. Cortical-like receptive fields in the lateral geniculate nucleus of marmoset monkeys. J. Neurosci. 33:166864–76 [Google Scholar]
  34. Cook JE. 1996. Spatial properties of retinal mosaics: an empirical evaluation of some existing measures. Vis. Neurosci. 13:115–30 [Google Scholar]
  35. Coombs J, van der List D, Wang G-Y, Chalupa LM. 2006. Morphological properties of mouse retinal ganglion cells. Neuroscience 140:1123–36 [Google Scholar]
  36. Crook JD, Peterson BB, Packer OS, Robinson FR, Troy JB, Dacey DM. 2008. Y-cell receptive field and collicular projection of parasol ganglion cells in macaque monkey retina. J. Neurosci. 28:4411277–91 [Google Scholar]
  37. Cruz-Martín A, El-Danaf RN, Osakada F, Sriram B, Dhande OS. et al. 2014. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507:7492358–61 [Google Scholar]
  38. Dacey D. 2004. Origins of perception: retinal ganglion cell diversity and the creation of parallel visual pathways. The Cognitive Neurosciences MS Gazzaniga 281–301 Cambridge, MA: MIT Press [Google Scholar]
  39. Dacey DM, Liao H-W, Peterson BB, Robinson FR, Smith VC. et al. 2005. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:7027749–54 [Google Scholar]
  40. Dacey DM, Petersen MR. 1992. Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. PNAS 89:209666–70 [Google Scholar]
  41. Dean P, Mitchell IJ, Redgrave P. 1988. Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats. Neuroscience 24:501–10 [Google Scholar]
  42. Dean P, Redgrave P, Westby GW. 1989. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12:137–47 [Google Scholar]
  43. Delogu A, Sellers K, Zagoraiou L, Bocianowska-Zbrog A, Mandal S. et al. 2012. Subcortical visual shell nuclei targeted by ipRGCs develop from a Sox14+-GABAergic progenitor and require Sox14 to regulate daily activity rhythms. Neuron 75:4648–62 [Google Scholar]
  44. Demb J, Singer J. 2015. Functional circuitry of the retina. Annu. Rev. Vis. Sci. 1263–89
  45. Dhande OS, Estevez ME, Quattrochi LE, El-Danaf RN, Nguyen PL. et al. 2013. Genetic dissection of retinal inputs to brainstem nuclei controlling image stabilization. J. Neurosci. 33:4517797–813 [Google Scholar]
  46. Dhande OS, Huberman AD. 2014a. Retinal ganglion cell maps in the brain: implications for visual processing. Curr. Opin. Neurobiol. 24:1133–42 [Google Scholar]
  47. Dhande OS, Huberman AD. 2014b. Visual circuits: mouse retina no longer a level playing field. Curr. Biol. 24:4R155–56 [Google Scholar]
  48. Distler C, Hoffmann KP. 1989a. The pupillary light reflex in normal and innate microstrabismic cats, I: behavior and receptive-field analysis in the nucleus praetectalis olivaris. Vis. Neurosci. 3:2127–38 [Google Scholar]
  49. Distler C, Hoffmann KP. 1989b. The pupillary light reflex in normal and innate microstrabismic cats, II: retinal and cortical input to the nucleus praetectalis olivaris. Vis. Neurosci. 3:2139–53 [Google Scholar]
  50. Distler C, Hoffmann K. 2011. The optokinetic reflex. The Oxford Handbook of Eye Movements SP Liversedge, ID Gilchrist, S Everling 65–83 New York: Oxford Univ. Press [Google Scholar]
  51. Dräger UC. 1975. Receptive fields of single cells and topography in mouse visual cortex. J. Comp. Neurol. 160:3269–90 [Google Scholar]
  52. Dräger UC, Hubel DH. 1975a. Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input. Nature 253:5488203–4 [Google Scholar]
  53. Dräger UC, Hubel DH. 1975b. Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. J. Neurophysiol. 38:3690–713 [Google Scholar]
  54. Dräger UC, Hubel DH. 1976. Topography of visual and somatosensory projections to mouse superior colliculus. J. Neurophysiol. 39:191–101 [Google Scholar]
  55. Duan X, Qiao M, Bei F, Kim I-J, He Z, Sanes JR. 2015. Subtype-specific regeneration of retinal ganglion cells following axotomy: effects of osteopontin and mTOR signaling. Neuron 85:1244–56 [Google Scholar]
  56. 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. 517:2226–44 [Google Scholar]
  57. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen S-K. et al. 2010. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:149–60 [Google Scholar]
  58. Edelstein K, Amir S. 1999. The role of the intergeniculate leaflet in entrainment of circadian rhythms to a skeleton photoperiod. J. Neurosci. 19:1372–80 [Google Scholar]
  59. El-Danaf RN, Huberman AD. 2015. Characteristic patterns of dendritic remodeling in early-stage glaucoma: evidence from genetically identified retinal ganglion cell types. J. Neurosci. 35:62329–43 [Google Scholar]
  60. Ellard CG, Goodale MA. 1988. A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil. Exp. Brain Res. 71:2307–19 [Google Scholar]
  61. Estevez ME, Fogerson PM, Ilardi MC, Borghuis BG, Chan E. et al. 2012. Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. J. Neurosci. 32:3913608–20 [Google Scholar]
  62. Euler T, Haverkamp S, Schubert T, Baden T. 2014. Retinal bipolar cells: elementary building blocks of vision. Nat. Rev. Neurosci. 15:8507–19 [Google Scholar]
  63. 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]
  64. Field GD, Sher A, Gauthier JL, Greschner M, Shlens J. et al. 2007. Spatial properties and functional organization of small bistratified ganglion cells in primate retina. J. Neurosci. 27:4813261–72 [Google Scholar]
  65. Field GD, Chichilnisky EJ. 2007. Information processing in the primate retina: circuitry and coding. Annu. Rev. Neurosci. 30:1–30 [Google Scholar]
  66. Feinberg EH, Meister M. 2014. Orientation columns in the mouse superior colliculus. Nature 519:7542229–32 [Google Scholar]
  67. Gale SD, Murphy GJ. 2014. Distinct representation and distribution of visual information by specific cell types in mouse superficial superior colliculus. J. Neurosci. 34:4013458–71 [Google Scholar]
  68. Gamlin PD, Clarke RJ. 1995. The pupillary light reflex pathway of the primate. J. Am. Optom. Assoc. 66:7415–18 [Google Scholar]
  69. Gamlin PD, Zhang H, Clarke RJ. 1995. Luminance neurons in the pretectal olivary nucleus mediate the pupillary light reflex in the rhesus monkey. Exp. Brain Res. 106:1169–76 [Google Scholar]
  70. Gamlin PDR. 2006. The pretectum: connections and oculomotor-related roles. Prog. Brain Res. 151:379–405 [Google Scholar]
  71. Gandhi NJ, Katnani HA. 2011. Motor functions of the superior colliculus. Annu. Rev. Neurosci. 34:205–31 [Google Scholar]
  72. Gebhardt C, Baier H, Del Bene F. 2013. Direction selectivity in the visual system of the zebrafish larva. Front. Neural Circuits 7:111 [Google Scholar]
  73. Giolli RA, Blanks RHI, Lui F. 2006. The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function. Prog. Brain Res. 151:407–440 [Google Scholar]
  74. Girman SV, Sauvé Y, Lund RD. 1999. Receptive field properties of single neurons in rat primary visual cortex. J. Neurophysiol. 82:1301–11 [Google Scholar]
  75. Grimes WN, Seal RP, Oesch N, Edwards RH, Diamond JS. 2011. Genetic targeting and physiological features of VGLUT3+ amacrine cells. Vis. Neurosci. 28:5381–92 [Google Scholar]
  76. Grubb MS, Thompson ID. 2004. Biochemical and anatomical subdivision of the dorsal lateral geniculate nucleus in normal mice and in mice lacking the β2 subunit of the nicotinic acetylcholine receptor. Vision Res. 44:283365–76 [Google Scholar]
  77. Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB. 2001. Melanopsin in cells of origin of the retinohypothalamic tract. Nat. Neurosci. 4:121165 [Google Scholar]
  78. Göz D, Studholme K, Lappi DA, Rollag MD, Provencio I, Morin LP. 2008. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLOS ONE 3:9e3153 [Google Scholar]
  79. Güler AD, Ecker JL, Lall GS, Haq S, Altimus CM. et al. 2008. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453:102–5 [Google Scholar]
  80. Hannibal J, Hindersson P, Ostergaard J, Georg B, Heegaard S. et al. 2004. Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Investig. Ophthalmol. Vis. Sci. 45:114202–9 [Google Scholar]
  81. Harrington ME. 1997. The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci. Biobehav. Rev. 21:5705–27 [Google Scholar]
  82. Harting JK, Huerta MF, Hashikawa T, van Lieshout DP. 1991. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304:2275–306 [Google Scholar]
  83. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N. et al. 2008. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLOS ONE 3:6e2451 [Google Scholar]
  84. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. 2002. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:55571065–70 [Google Scholar]
  85. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH. et al. 2003. Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:76–81 [Google Scholar]
  86. Hattar S, Kumar M, Park A, Tong P, Tung J. et al. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol. 497:3326–49 [Google Scholar]
  87. Hendry SH, Reid RC. 2000. The koniocellular pathway in primate vision. Annu. Rev. Neurosci. 23:127–53 [Google Scholar]
  88. Hofbauer A, Dräger UC. 1985. Depth segregation of retinal ganglion cells projecting to mouse superior colliculus. J. Comp. Neurol. 234:4465–74 [Google Scholar]
  89. Hong YK, Chen C. 2011. Wiring and rewiring of the retinogeniculate synapse. Curr. Opin. Neurobiol. 21:2228–37 [Google Scholar]
  90. Hu C, Hill DD, Wong KY. 2013. Intrinsic physiological properties of the five types of mouse ganglion-cell photoreceptors. J. Neurophysiol. 109:1876–89 [Google Scholar]
  91. Hubel DH, Wiesel TN. 1962. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160:106–54 [Google Scholar]
  92. Hubel DH, Wiesel TN. 1968. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195:1215–43 [Google Scholar]
  93. Huberman AD, Feller MB, Chapman B. 2008a. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 31:479–509 [Google Scholar]
  94. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB. et al. 2008b. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59:3425–38 [Google Scholar]
  95. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA. 2009. Genetic identification of an On-Off direction-selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62:3327–34 [Google Scholar]
  96. Ingle D. 1973. Two visual systems in the frog. Science 181:41041053–55 [Google Scholar]
  97. Isa T, Hall WC. 2009. Exploring the superior colliculus in vitro. J. Neurophysiol. 102:52581–93 [Google Scholar]
  98. Jaubert-Miazza L, Green E, Lo F-S, Bui K, Mills J, Guido W. 2005. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis. Neurosci. 22:5661–76 [Google Scholar]
  99. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:52901133–38 [Google Scholar]
  100. Kay JN, De la Huerta I, Kim I-J, Zhang Y, Yamagata M. et al. 2011. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J. Neurosci. 31:217753–62 [Google Scholar]
  101. Kerlin AM, Andermann ML, Berezovskii VK, Reid RC. 2010. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67:5858–71 [Google Scholar]
  102. Kim I-J, Zhang Y, Meister M, Sanes JR. 2010. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J. Neurosci. 30:41452–62 [Google Scholar]
  103. Kim I-J, Zhang Y, Yamagata M, Meister M, Sanes JR. 2008. Molecular identification of a retinal cell type that responds to upward motion. Nature 452:7186478–82 [Google Scholar]
  104. Kim JS, Greene MJ, Zlateski A, Lee K, Richardson M. et al. 2014. Space–time wiring specificity supports direction selectivity in the retina. Nature 509:7500331–36 [Google Scholar]
  105. Kirkby LA, Sack GS, Firl A, Feller MB. 2013. A role for correlated spontaneous activity in the assembly of neural circuits. Neuron 80:51129–44 [Google Scholar]
  106. Knudsen EI, du Lac S, Esterly SD. 1987. Computational maps in the brain. Annu. Rev. Neurosci. 10:41–65 [Google Scholar]
  107. Korenbrot JI. 2012. Speed, sensitivity, and stability of the light response in rod and cone photoreceptors: facts and models. Prog. Retin. Eye Res. 31:5442–66 [Google Scholar]
  108. Krahe TE, El-Danaf RN, Dilger EK, Henderson SC, Guido W. 2011. Morphologically distinct classes of relay cells exhibit regional preferences in the dorsal lateral geniculate nucleus of the mouse. J. Neurosci. 31:4817437–48 [Google Scholar]
  109. Krauzlis RJ, Lovejoy LP, Zénon A. 2013. Superior colliculus and visual spatial attention. Annu. Rev. Neurosci. 36:165–82 [Google Scholar]
  110. Krishnaswamy A, Yamagata M, Duan X, Hong YK, Sanes JR. 2015. Sidekick 2 directs formation of a retinal circuit that detects differential motion. Nature 524:466–70 [Google Scholar]
  111. Kuffler SW. 1953. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16:137–68 [Google Scholar]
  112. Langer TP, Lund RD. 1974. The upper layers of the superior colliculus of the rat: a Golgi study. J. Comp. Neurol. 158:4418–35 [Google Scholar]
  113. 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 84:4708–15 [Google Scholar]
  114. LeGates TA, Fernandez DC, Hattar S. 2014. Light as a central modulator of circadian rhythms, sleep and affect. Nat. Rev. Neurosci. 15:7443–54 [Google Scholar]
  115. Lettvin JY, Maturana HR, McCulloch WS, Pitts WH. 1959. What the frog's eye tells the frog's brain. Proc. IRE 47:111940–51 [Google Scholar]
  116. Leventhal AG, Rodieck RW, Dreher B. 1981. Retinal ganglion cell classes in the Old World monkey: morphology and central projections. Science 213:45121139–42 [Google Scholar]
  117. Levick WR. 1967. Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina. J. Physiol. 188:3285–307 [Google Scholar]
  118. Levick WR, Oyster CW, Takahashi E. 1969. Rabbit lateral geniculate nucleus: sharpener of directional information. Science 165:3894712–14 [Google Scholar]
  119. Levick WR, Thibos LN. 1982. Analysis of orientation bias in cat retina. J. Physiol. 329:243–61 [Google Scholar]
  120. Liang F, Xiong XR, Zingg B, Ji X-Y, Zhang LI, Tao HW. 2015. Sensory cortical control of a visually induced arrest behavior via corticotectal projections. Neuron 86:3755–67 [Google Scholar]
  121. Lin B, Wang SW, Masland RH. 2004. Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43:4475–85 [Google Scholar]
  122. Linden R, Perry VH. 1983. Massive retinotectal projection in rats. Brain Res. 272:1145–49 [Google Scholar]
  123. Ling S, Pratte MS, Tong F. 2015. Attention alters orientation processing in the human lateral geniculate nucleus. Nat. Neurosci. 18:496–98 [Google Scholar]
  124. Lucas RJ, Douglas RH, Foster RG. 2001. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat. Neurosci. 4:6621–26 [Google Scholar]
  125. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau K-W. 2003. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245–47 [Google Scholar]
  126. Lucas RJ, Lall GS, Allen AE, Brown TM. 2012. How rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock. Prog. Brain Res. 199:1–18 [Google Scholar]
  127. Mangini NJ, Pearlman AL. 1980. Laminar distribution of receptive field properties in the primary visual cortex of the mouse. J. Comp. Neurol. 193:1203–22 [Google Scholar]
  128. 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. 28:164136–50 [Google Scholar]
  129. Mao C-A, Li H, Zhang Z, Kiyama T, Panda S. et al. 2014. T-box transcription regulator Tbr2 is essential for the formation and maintenance of Opn4/melanopsin-expressing intrinsically photosensitive retinal ganglion cells. J. Neurosci. 34:3913083–95 [Google Scholar]
  130. Marshel JH, Kaye AP, Nauhaus I, Callaway EM. 2012. Anterior-posterior direction opponency in the superficial mouse lateral geniculate nucleus. Neuron 76:4713–20 [Google Scholar]
  131. Masseck OA, Hoffmann K-P. 2009. Comparative neurobiology of the optokinetic reflex. Ann. N. Y. Acad. Sci. 1164:430–39 [Google Scholar]
  132. May PJ. 2006. The mammalian superior colliculus: laminar structure and connections. Prog. Brain Res. 151:321–78 [Google Scholar]
  133. McLaughlin T, O’Leary DDM. 2005. Molecular gradients and development of retinotopic maps. Annu. Rev. Neurosci. 28:327–55 [Google Scholar]
  134. Métin C, Godement P, Imbert M. 1988. The primary visual cortex in the mouse: receptive field properties and functional organization. Exp. Brain Res. 69:3594–612 [Google Scholar]
  135. Mooney RD, Rhoades RW. 1990. Relationships between physiological and morphological properties of retinocollicular axons in the hamster. J. Neurosci. 10:93164–77 [Google Scholar]
  136. Morin LP. 2013. Neuroanatomy of the extended circadian rhythm system. Exp. Neurol. 243:4–20 [Google Scholar]
  137. Morin LP, Studholme KM. 2014. Retinofugal projections in the mouse. J. Comp. Neurol. 522:163733–53 [Google Scholar]
  138. Mrosovsky N. 1995. A non-photic gateway to the circadian clock of hamsters. Ciba Found. Symp. 183:154–67 discussion 167–74 [Google Scholar]
  139. Münch 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. 12:101308–16 [Google Scholar]
  140. Mysore SP, Knudsen EI. 2011. The role of a midbrain network in competitive stimulus selection. Curr. Opin. Neurobiol. 21:4653–60 [Google Scholar]
  141. Nathans J. 1987. Molecular biology of visual pigments. Annu. Rev. Neurosci. 10:163–94 [Google Scholar]
  142. Niell CM, Stryker MP. 2008. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28:307520–36 [Google Scholar]
  143. Niell CM, Stryker MP. 2010. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65:4472–79 [Google Scholar]
  144. Northmore DP, Levine ES, Schneider GE. 1988. Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp. Brain Res. 73:3595–605 [Google Scholar]
  145. Ohki K, Chung S, Ch’ng YH, Kara P, Reid RC. 2005. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433:7026597–603 [Google Scholar]
  146. Ölveczky BP, Baccus SA, Meister M. 2003. Segregation of object and background motion in the retina. Nature 423:6938401–8 [Google Scholar]
  147. Osterhout JA, Josten N, Yamada J, Pan F, Wu S. et al. 2011. Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 71:4632–39 [Google Scholar]
  148. Oyster CW, Takahashi E, Collewijn H. 1972. Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Res. 12:2183–93 [Google Scholar]
  149. Pak MW, Giolli RA, Pinto LH, Mangini NJ, Gregory KM, Vanable JW Jr. 1987. Retinopretectal and accessory optic projections of normal mice and the OKN-defective mutant mice beige, beige-J, and pearl. J. Comp. Neurol. 258:435–46 [Google Scholar]
  150. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD. et al. 2003. Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:5632525–27 [Google Scholar]
  151. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ. et al. 2002. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:56012213–16 [Google Scholar]
  152. Pang J-J, Gao F, Wu SM. 2003. Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. J. Neurosci. 23:146063–73 [Google Scholar]
  153. Passaglia CL, Troy JB, Rüttiger L, Lee BB. 2002. Orientation sensitivity of ganglion cells in primate retina. Vision Res. 42:6683–94 [Google Scholar]
  154. Petrusca D, Grivich MI, Sher A, Field GD, Gauthier JL. et al. 2007. Identification and characterization of a Y-like primate retinal ganglion cell type. J. Neurosci. 27:4111019–27 [Google Scholar]
  155. Pfeiffenberger C, Yamada J, Feldheim DA. 2006. Ephrin-As and patterned retinal activity act together in the development of topographic maps in the primary visual system. J. Neurosci. 26:5012873–84 [Google Scholar]
  156. Piscopo DM, El-Danaf RN, Huberman AD, Niell CM. 2013. Diverse visual features encoded in mouse lateral geniculate nucleus. J. Neurosci. 33:114642–56 [Google Scholar]
  157. Prichard JR, Stoffel RT, Quimby DL, Obermeyer WH, Benca RM, Behan M. 2002. Fos immunoreactivity in rat subcortical visual shell in response to illuminance changes. Neuroscience 114:3781–93 [Google Scholar]
  158. Rakic P. 1976. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261:5560467–71 [Google Scholar]
  159. Rancz EA, Franks KM, Schwarz MK, Pichler B, Schaefer AT, Margrie TW. 2011. Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics. Nat. Neurosci. 14:4527–32 [Google Scholar]
  160. Reese BE. 1984. The projection from the superior colliculus to the dorsal lateral geniculate nucleus in the rat. Brain Res. 305:1162–68 [Google Scholar]
  161. Reese BE. 1988. “Hidden lamination” in the dorsal lateral geniculate nucleus: the functional organization of this thalamic region in the rat. Brain Res. 472:2119–37 [Google Scholar]
  162. Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL. et al. 2011. Transgenic mice reveal unexpected diversity of On-Off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J. Neurosci. 31:248760–69 [Google Scholar]
  163. Rodieck RW. 1979. Visual pathways. Annu. Rev. Neurosci. 2:193–225 [Google Scholar]
  164. Rodieck RW, Binmoeller KF, Dineen J. 1985. Parasol and midget ganglion cells of the human retina. J. Comp. Neurol. 233:1115–32 [Google Scholar]
  165. Rodieck RW, Stone J. 1965. Analysis of receptive fields of cat retinal ganglion cells. J. Neurophysiol. 28:832–49 [Google Scholar]
  166. Rosenquist AC, Palmer LA. 1971. Visual receptive field properties of cells of the superior colliculus after cortical lesions in the cat. Exp. Neurol. 33:3629–52 [Google Scholar]
  167. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P. et al. 2002. Role of melanopsin in circadian responses to light. Science 298:56012211–13 [Google Scholar]
  168. Sahibzada N, Dean P, Redgrave P. 1986. Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J. Neurosci. 6:3723–33 [Google Scholar]
  169. 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]
  170. Schmidt TM, Alam NM, Chen S, Kofuji P, Li W. et al. 2014. A role for melanopsin in alpha retinal ganglion cells and contrast detection. Neuron 82:4781–88 [Google Scholar]
  171. Schmidt TM, Taniguchi K, Kofuji P. 2008. Intrinsic and extrinsic light responses in melanopsin-expressing ganglion cells during mouse development. J. Neurophysiol. 100:371–84 [Google Scholar]
  172. Scholl B, Tan AYY, Corey J, Priebe NJ. 2013. Emergence of orientation selectivity in the mammalian visual pathway. J. Neurosci. 33:2610616–24 [Google Scholar]
  173. Seabrook TA, Krahe TE, Govindaiah G, Guido W. 2013. Interneurons in the mouse visual thalamus maintain a high degree of retinal convergence throughout postnatal development. Neural Dev. 8:24 [Google Scholar]
  174. Seung HS, Sümbül U. 2014. Neuronal cell types and connectivity: lessons from the retina. Neuron 83:61262–72 [Google Scholar]
  175. Shang C, Liu Z, Chen Z, Shi Y, Wang Q. et al. 2015. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 348:62421472–77 [Google Scholar]
  176. Siegert S, Cabuy E, Scherf BG, Kohler H, Panda S. et al. 2012. Transcriptional code and disease map for adult retinal cell types. Nat. Neurosci. 15:3487–95, S1–2 [Google Scholar]
  177. Simpson JI. 1984. The accessory optic system. Annu. Rev. Neurosci. 7:13–41 [Google Scholar]
  178. Sivyer B, van Wyk M, Vaney DI, Taylor WR. 2010. Synaptic inputs and timing underlying the velocity tuning of direction-selective ganglion cells in rabbit retina. J. Physiol. 588:3243–53 [Google Scholar]
  179. Sohya K, Kameyama K, Yanagawa Y, Obata K, Tsumoto T. 2007. GABAergic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2+ imaging in transgenic mice. J. Neurosci. 27:82145–49 [Google Scholar]
  180. Sparks DL. 2002. The brainstem control of saccadic eye movements. Nat. Rev. Neurosci. 3:12952–64 [Google Scholar]
  181. Sparks DL, Nelson IS. 1987. Sensory and motor maps in the mammalian superior colliculus. Trends Neurosci. 10:8312–17 [Google Scholar]
  182. Stafford BK, Kupershtok M, Demb JB. 2010. Cell type–specific differences in NMDA receptor contributions to mouse retinal ganglion cell responses Presented at Fed. Am. Soc. Exp. Biol. Conf. Retin. Neurobiol. Vis. Process. Saxtons River, VT, Jul. 11–16
  183. Stein BE, Stanford TR, Rowland BA. 2014. Development of multisensory integration from the perspective of the individual neuron. Nat. Rev. Neurosci. 15:8520–35 [Google Scholar]
  184. Stone J. 1983. Parallel Processing in the Visual System Boston, MA: Springer
  185. Sugita Y, Miura K, Araki F, Furukawa T, Kawano K. 2013. Contributions of retinal direction-selective ganglion cells to optokinetic responses in mice. Eur. J. Neurosci. 38:62823–31 [Google Scholar]
  186. Sümbül U, Song S, McCulloch K, Becker M, Lin B. et al. 2014. A genetic and computational approach to structurally classify neuronal types. Nat. Commun. 5:3512 [Google Scholar]
  187. Sweeney NT, Tierney H, Feldheim DA. 2014. Tbr2 is required to generate a neural circuit mediating the pupillary light reflex. J. Neurosci. 34:165447–53 [Google Scholar]
  188. Szmajda BA, Grünert U, Martin PR. 2008. Retinal ganglion cell inputs to the koniocellular pathway. J. Comp. Neurol. 510:3251–68 [Google Scholar]
  189. Tamamaki N, Uhlrich DJ, Sherman SM. 1995. Morphology of physiologically identified retinal X and Y axons in the cat's thalamus and midbrain as revealed by intraaxonal injection of biocytin. J. Comp. Neurol. 354:4583–607 [Google Scholar]
  190. Thoreson WB, Mangel SC. 2012. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31:5407–41 [Google Scholar]
  191. Trejo LJ, Cicerone CM. 1984. Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Res. 300:149–62 [Google Scholar]
  192. Trenholm S, Johnson K, Li X, Smith RG, Awatramani GB. 2011. Parallel mechanisms encode direction in the retina. Neuron 71:4683–94 [Google Scholar]
  193. Triplett JW. 2014. Molecular guidance of retinotopic map development in the midbrain. Curr. Opin. Neurobiol. 24:17–12 [Google Scholar]
  194. Ts’o DY, Frostig RD, Lieke EE, Grinvald A. 1990. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249:4967417–20 [Google Scholar]
  195. Usrey WM, Alitto HJ. 2015. Visual functions of the thalamus. Annu. Rev. Vis. Sci. 1351–71
  196. van Wyk M, Taylor WR, Vaney D. 2006. Local edge detectors: a substrate for fine spatial vision at low temporal frequencies in rabbit retina. J. Neurosci. 26:5113250–63 [Google Scholar]
  197. van Wyk M, Wässle H, Taylor WR. 2009. Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Vis. Neurosci. 26:3297–308 [Google Scholar]
  198. Vaney DI, Sivyer B, Taylor WR. 2012. Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat. Rev. Neurosci. 13:3194–208 [Google Scholar]
  199. Venkataramani S, Taylor WR. 2010. Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition. J. Neurosci. 30:4615664–76 [Google Scholar]
  200. Verwey M, Amir S. 2009. Food-entrainable circadian oscillators in the brain. Eur. J. Neurosci. 30:91650–57 [Google Scholar]
  201. Völgyi B, Chheda S, Bloomfield SA. 2009. Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J. Comp. Neurol. 512:5664–87 [Google Scholar]
  202. Wang L, Rangarajan KV, Lawhn-Heath CA, Sarnaik R, Wang B-S. et al. 2009. Direction-specific disruption of subcortical visual behavior and receptive fields in mice lacking the β2 subunit of nicotinic acetylcholine receptor. J. Neurosci. 29:4112909–18 [Google Scholar]
  203. Wang L, Sarnaik R, Rangarajan K, Liu X, Cang J. 2010. Visual receptive field properties of neurons in the superficial superior colliculus of the mouse. J. Neurosci. 30:4916573–84 [Google Scholar]
  204. Watanabe M, Rodieck RW. 1989. Parasol and midget ganglion cells of the primate retina. J. Comp. Neurol. 289:3434–54 [Google Scholar]
  205. Wiesel TN. 1960. Receptive fields of ganglion cells in the cat's retina. J. Physiol. 153:583–94 [Google Scholar]
  206. Wei P, Liu N, Zhang Z, Liu X, Tang Y. et al. 2015. Processing of visually evoked innate fear by a non-canonical thalamic pathway. Nat. Commun. 6:6756 [Google Scholar]
  207. Wei W, Feller MB. 2011. Organization and development of direction-selective circuits in the retina. Trends Neurosci. 34:12638–45 [Google Scholar]
  208. Welsh DK, Takahashi JS, Kay SA. 2010. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72:551–77 [Google Scholar]
  209. Weng S, Sun W, He S. 2005. Identification of ON–OFF direction-selective ganglion cells in the mouse retina. J. Physiol. 562:915–23 [Google Scholar]
  210. Wertz A, Trenholm S, Yonehara K, Hillier D, Raics Z. et al. 2015. Single-cell–initiated monosynaptic tracing reveals layer-specific cortical network modules. Science 349:624370–74 [Google Scholar]
  211. Westby GW, Keay KA, Redgrave P, Dean P, Bannister M. 1990. Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties. Exp. Brain Res. 81:3626–38 [Google Scholar]
  212. Wickelgren BG, Sterling P. 1969. Influence of visual cortex on receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32:116–23 [Google Scholar]
  213. Witkovsky P. 2004. Dopamine and retinal function. Doc. Ophthalmol. 108:117–40 [Google Scholar]
  214. Wurtz RH, Albano JE. 1980. Visual-motor function of the primate superior colliculus. Annu. Rev. Neurosci. 3:189–226 [Google Scholar]
  215. Xiang M, Zhou H, Nathans J. 1996. Molecular biology of retinal ganglion cells. PNAS 93:2596–601 [Google Scholar]
  216. Yilmaz M, Meister M. 2013. Rapid innate defensive responses of mice to looming visual stimuli. Curr. Biol. 23:202011–15 [Google Scholar]
  217. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Botond R. 2011. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469:407–410 [Google Scholar]
  218. 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 79:61078–85 [Google Scholar]
  219. Yonehara K, Ishikane H, Sakuta H, Shintani T, Nakamura-Yonehara K. et al. 2009. Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLOS ONE 4:1e4320 [Google Scholar]
  220. Yonehara K, Shintani T, Suzuki R, Sakuta H, Takeuchi Y. et al. 2008. Expression of SPIG1 reveals development of a retinal ganglion cell subtype projecting to the medial terminal nucleus in the mouse. PLOS ONE 3:2e1533 [Google Scholar]
  221. Yoshida K, Watanabe D, Ishikane H, Tachibana M, Pastan I, Nakanishi S. 2001. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30:3771–80 [Google Scholar]
  222. Young MJ, Lund RD. 1994. The anatomical substrates subserving the pupillary light reflex in rats: origin of the consensual pupillary response. Neuroscience 62:2481–96 [Google Scholar]
  223. 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 109:36E2391–98 [Google Scholar]
  224. Zhao X, Chen H, Liu X, Cang J. 2013. Orientation-selective responses in the mouse lateral geniculate nucleus. J. Neurosci. 33:3112751–63 [Google Scholar]
  225. Zhao X, Liu M, Cang J. 2014a. Visual cortex modulates the magnitude but not the selectivity of looming-evoked responses in the superior colliculus of awake mice. Neuron 84:1202–13 [Google Scholar]
  226. Zhao X, Stafford BK, Godin AL, King WM, Wong KY. 2014b. Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells. J. Physiol. 592:1619–36 [Google Scholar]
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