1932

Abstract

The retina is a tremendously complex image processor, containing numerous cell types that form microcircuits encoding different aspects of the visual scene. Each microcircuit exhibits a distinct pattern of synaptic connectivity. The developmental mechanisms responsible for this patterning are just beginning to be revealed. Furthermore, signals processed by different retinal circuits are relayed to specific, often distinct, brain regions. Thus, much work has focused on understanding the mechanisms that wire retinal axonal projections to their appropriate central targets. Here, we highlight recently discovered cellular and molecular mechanisms that together shape stereotypic wiring patterns along the visual pathway, from within the retina to the brain. Although some mechanisms are common across circuits, others play unconventional and circuit-specific roles. Indeed, the highly organized connectivity of the visual system has greatly facilitated the discovery of novel mechanisms that establish precise synaptic connections within the nervous system.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-072116-031607
2017-07-25
2024-04-22
Loading full text...

Full text loading...

/deliver/fulltext/neuro/40/1/annurev-neuro-072116-031607.html?itemId=/content/journals/10.1146/annurev-neuro-072116-031607&mimeType=html&fmt=ahah

Literature Cited

  1. Anderson JR, Jones BW, Watt CB, Shaw MV, Yang JH. et al. 2011. Exploring the retinal connectome. Mol. Vis. 17:355–79 [Google Scholar]
  2. Avellaneda-Chevrier VK, Wang X, Hooper ML, Chauhan BC. 2015. The retino-retinal projection: tracing retinal ganglion cells projecting to the contralateral retina. Neurosci. Lett. 591:105–9 [Google Scholar]
  3. Baier H. 2013. Synaptic laminae in the visual system: molecular mechanisms forming layers of perception. Annu. Rev. Cell Dev. Biol. 29:385–416 [Google Scholar]
  4. Barlow HB, Levick WR. 1965. The mechanism of directionally selective units in rabbit's retina. J. Physiol. 178:477–504 [Google Scholar]
  5. Barton B, Brewer AA. 2015. fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements. PNAS 112:5201–6 [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. Bolte P, Herrling R, Dorgau B, Schultz K, Feigenspan A. et al. 2016. Expression and localization of connexins in the outer retina of the mouse. J. Mol. Neurosci. 58:178–92 [Google Scholar]
  10. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–88 [Google Scholar]
  11. 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:e1000558 [Google Scholar]
  12. Cang J, Feldheim DA. 2013. Developmental mechanisms of topographic map formation and alignment. Annu. Rev. Neurosci. 36:51–77 [Google Scholar]
  13. Cao Y, Sarria I, Fehlhaber KE, Kamasawa N, Orlandi C. et al. 2015. Mechanism for selective synaptic wiring of rod photoreceptors into the retinal circuitry and its role in vision. Neuron 87:1248–60 [Google Scholar]
  14. Chalupa LM. 1998. Introduction: development and organization of the retina: cellular, molecular and functional perspectives. Semin. Cell Dev. Biol. 9:239–40 [Google Scholar]
  15. Chatzopoulou E, Miguez A, Savvaki M, Levasseur G, Muzerelle A. et al. 2008. Structural requirement of TAG-1 for retinal ganglion cell axons and myelin in the mouse optic nerve. J. Neurosci. 28:7624–36 [Google Scholar]
  16. 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]
  17. 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]
  18. Cruz-Martin 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 507:358–61 [Google Scholar]
  19. de la Torre JR, Hopker VH, Ming GL, Poo MM, Tessier-Lavigne M. et al. 1997. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron 19:1211–24 [Google Scholar]
  20. Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, Sretavan DW. 1997. Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19:575–89 [Google Scholar]
  21. Demb JB, Singer JH. 2015. Functional circuitry of the retina. Annu. Rev. Vis. Sci. 1:263–89 [Google Scholar]
  22. 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. 33:17797–813 [Google Scholar]
  23. Dhande OS, Stafford BK, Lim JHA, Huberman AD. 2015. Contributions of retinal ganglion cells to subcortical visual processing and behaviors. Annu. Rev. Vis. Sci. 1:291–328 [Google Scholar]
  24. 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]
  25. 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]
  26. Dunn FA, Della Santina L, Parker ED, Wong RO. 2013. Sensory experience shapes the development of the visual system's first synapse. Neuron 80:1159–66 [Google Scholar]
  27. Dunn FA, Wong RO. 2012. Diverse strategies engaged in establishing stereotypic wiring patterns among neurons sharing a common input at the visual system's first synapse. J. Neurosci. 32:10306–17 [Google Scholar]
  28. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK. et al. 2010. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:49–60 [Google Scholar]
  29. Eggers ED, Lukasiewicz PD. 2011. Multiple pathways of inhibition shape bipolar cell responses in the retina. Vis. Neurosci. 28:95–108 [Google Scholar]
  30. Eggers ED, McCall MA, Lukasiewicz PD. 2007. Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. J. Physiol. 582:569–82 [Google Scholar]
  31. Erskine L, Herrera E. 2007. The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. Dev. Biol. 308:1–14 [Google Scholar]
  32. Erskine L, Reijntjes S, Pratt T, Denti L, Schwarz Q. et al. 2011. VEGF signaling through neuropilin 1 guides commissural axon crossing at the optic chiasm. Neuron 70:951–65 [Google Scholar]
  33. Euler T, Detwiler PB, Denk W. 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:845–52 [Google Scholar]
  34. 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]
  35. 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]
  36. Feller MB. 2009. Retinal waves are likely to instruct the formation of eye-specific retinogeniculate projections. Neural Dev 4:24 [Google Scholar]
  37. Fernandez DC, Chang YT, Hattar S, Chen SK. 2016. Architecture of retinal projections to the central circadian pacemaker. PNAS 113:6047–52 [Google Scholar]
  38. Fletcher EL, Koulen P, Wässle H. 1998. GABAA and GABAC receptors on mammalian rod bipolar cells. J. Comp. Neurol. 396:351–65 [Google Scholar]
  39. Fried SI, Munch TA, Werblin FS. 2002. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420:411–14 [Google Scholar]
  40. Fried SI, Munch TA, Werblin FS. 2005. Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46:117–27 [Google Scholar]
  41. Fuerst PG, Bruce F, Tian M, Wei W, Elstrott J. et al. 2009. DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64:484–97 [Google Scholar]
  42. Greferath U, Grünert U, Fritschy JM, Stephenson A, Möhler H, Wässle H. 1995. GABAA receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J. Comp. Neurol. 353:553–71 [Google Scholar]
  43. Grimes WN, Zhang J, Tian H, Graydon CW, Hoon M. et al. 2015. Complex inhibitory microcircuitry regulates retinal signaling near visual threshold. J. Neurophysiol. 114:341–53 [Google Scholar]
  44. Guido W. 2008. Refinement of the retinogeniculate pathway. J. Physiol. 586:4357–62 [Google Scholar]
  45. Günhan E, Choudary PV, Landerholm TE, Chalupa LM. 2002. Depletion of cholinergic amacrine cells by a novel immunotoxin does not perturb the formation of segregated On and Off cone bipolar cell projections. J. Neurosci. 22:2265–73 [Google Scholar]
  46. Günhan-Agar E, Kahn D, Chalupa LM. 2000. Segregation of On and Off bipolar cell axonal arbors in the absence of retinal ganglion cells. J. Neurosci. 20:306–14 [Google Scholar]
  47. Hammer S, Monavarfeshani A, Lemon T, Su J, Fox MA. 2015. Multiple retinal axons converge onto relay cells in the adult mouse thalamus. Cell Rep 12:1575–83 [Google Scholar]
  48. Hartveit E, Veruki ML. 2012. Electrical synapses between AII amacrine cells in the retina: function and modulation. Brain Res 1487:160–72 [Google Scholar]
  49. 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. 497:326–49 [Google Scholar]
  50. Hattori D, Chen Y, Matthews BJ, Salwinski L, Sabatti C. et al. 2009. Robust discrimination between self and non-self neurites requires thousands of Dscam1 isoforms. Nature 461:644–48 [Google Scholar]
  51. Hoon M, Okawa H, Della Santina L, Wong RO. 2014. Functional architecture of the retina: development and disease. Prog. Retin. Eye Res. 42:44–84 [Google Scholar]
  52. Hoon M, Sinha R, Okawa H, Suzuki SC, Hirano AA. et al. 2015. Neurotransmission plays contrasting roles in the maturation of inhibitory synapses on axons and dendrites of retinal bipolar cells. PNAS 112:12840–45 [Google Scholar]
  53. Huberman AD, Clandinin TR, Baier H. 2010. Molecular and cellular mechanisms of lamina-specific axon targeting. Cold Spring Harb. Perspect. Biol. 2:a001743 [Google Scholar]
  54. 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]
  55. 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 62:327–34 [Google Scholar]
  56. Inayat S, Barchini J, Chen H, Feng L, Liu X, Cang J. 2015. Neurons in the most superficial lamina of the mouse superior colliculus are highly selective for stimulus direction. J. Neurosci. 35:7992–8003 [Google Scholar]
  57. Ivanova E, Müller U, Wässle H. 2006. Characterization of the glycinergic input to bipolar cells of the mouse retina. Eur. J. Neurosci. 23:350–64 [Google Scholar]
  58. Joesch M, Meister M. 2016. A neuronal circuit for colour vision based on rod-cone opponency. Nature 532:236–39 [Google Scholar]
  59. Kanagawa M, Omori Y, Sato S, Kobayashi K, Miyagoe-Suzuki Y. et al. 2010. Post-translational maturation of dystroglycan is necessary for pikachurin binding and ribbon synaptic localization. J. Biol. Chem. 285:31208–16 [Google Scholar]
  60. Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M. et al. 2011. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J. Neurosci. 31:7753–62 [Google Scholar]
  61. Keeley PW, Luna G, Fariss RN, Skyles KA, Madsen NR. et al. 2013. Development and plasticity of outer retinal circuitry following genetic removal of horizontal cells. J. Neurosci. 33:17847–62 [Google Scholar]
  62. Keeley PW, Reese BE. 2010. Role of afferents in the differentiation of bipolar cells in the mouse retina. J. Neurosci. 30:1677–85 [Google Scholar]
  63. Kerschensteiner D, Morgan JL, Parker ED, Lewis RM, Wong RO. 2009. Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature 460:1016–20 [Google Scholar]
  64. Kim IJ, 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. 30:1452–62 [Google Scholar]
  65. 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]
  66. 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]
  67. 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]
  68. Kolb H. 1979. The inner plexiform layer in the retina of the cat: electron microscopic observations. J. Neurocytol. 8:295–329 [Google Scholar]
  69. Kolb H, Famiglietti EV. 1974. Rod and cone pathways in the inner plexiform layer of cat retina. Science 186:47–49 [Google Scholar]
  70. Kostadinov D, Sanes JR. 2015. Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function. eLife 4:e08964 [Google Scholar]
  71. 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]
  72. Kuwajima T, Yoshida Y, Takegahara N, Petros TJ, Kumanogoh A. et al. 2012. Optic chiasm presentation of Semaphorin6D in the context of Plexin-A1 and Nr-CAM promotes retinal axon midline crossing. Neuron 74:676–90 [Google Scholar]
  73. Lee SC, Meyer A, Schubert T, Huser L, Dedek K, Haverkamp S. 2015. Morphology and connectivity of the small bistratified A8 amacrine cell in the mouse retina. J. Comp. Neurol. 523:1529–47 [Google Scholar]
  74. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. 2012. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488:517–21 [Google Scholar]
  75. Livingstone MS. 1998. Mechanisms of direction selectivity in macaque V1. Neuron 20:509–26 [Google Scholar]
  76. Majumdar S, Heinze L, Haverkamp S, Ivanova E, Wässle H. 2007. Glycine receptors of A-type ganglion cells of the mouse retina. Vis. Neurosci. 24:471–87 [Google Scholar]
  77. Marc RE, Anderson JR, Jones BW, Sigulinsky CL, Lauritzen JS. 2014. The AII amacrine cell connectome: a dense network hub. Front. Neural Circuits 8:104 [Google Scholar]
  78. Matsuoka RL, Chivatakarn O, Badea TC, Samuels IS, Cahill H. et al. 2011a. Class 5 transmembrane semaphorins control selective mammalian retinal lamination and function. Neuron 71:460–73 [Google Scholar]
  79. Matsuoka RL, Jiang Z, Samuels IS, Nguyen-Ba-Charvet KT, Sun LO. et al. 2012. Guidance-cue control of horizontal cell morphology, lamination, and synapse formation in the mammalian outer retina. J. Neurosci. 32:6859–68 [Google Scholar]
  80. Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A, Badea TC, Chedotal A, Kolodkin AL. 2011b. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470:259–63 [Google Scholar]
  81. Moleirinho S, Tilston-Lunel A, Angus L, Gunn-Moore F, Reynolds PA. 2013. The expanding family of FERM proteins. Biochem. J. 452:183–93 [Google Scholar]
  82. Morgan JL, Berger DR, Wetzel AW, Lichtman JW. 2016. The fuzzy logic of network connectivity in mouse visual thalamus. Cell 165:192–206 [Google Scholar]
  83. Morgan JL, Dhingra A, Vardi N, Wong RO. 2006. Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells. Nat. Neurosci. 9:85–92 [Google Scholar]
  84. Morgan JL, Soto F, Wong RO, Kerschensteiner D. 2011. Development of cell type-specific connectivity patterns of converging excitatory axons in the retina. Neuron 71:1014–21 [Google Scholar]
  85. Morin LP, Studholme KM. 2014. Retinofugal projections in the mouse. J. Comp. Neurol. 522:3733–53 [Google Scholar]
  86. Morrie RD, Feller MB. 2015. An asymmetric increase in inhibitory synapse number underlies the development of a direction selective circuit in the retina. J. Neurosci. 35:9281–86 [Google Scholar]
  87. Müller M, Holländer H. 1988. A small population of retinal ganglion cells projecting to the retina of the other eye: an experimental study in the rat and the rabbit. Exp. Brain Res. 71:611–17 [Google Scholar]
  88. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R. et al. 1993. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for l-2-amino-4-phosphonobutyrate. J. Biol. Chem. 268:11868–73 [Google Scholar]
  89. Okawa H, Della Santina L, Schwartz GW, Rieke F, Wong RO. 2014. Interplay of cell-autonomous and nonautonomous mechanisms tailors synaptic connectivity of converging axons in vivo. Neuron 82:125–37 [Google Scholar]
  90. Omori Y, Araki F, Chaya T, Kajimura N, Irie S. et al. 2012. Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells. J. Neurosci. 32:6126–37 [Google Scholar]
  91. Osterhout JA, El-Danaf RN, Nguyen PL, Huberman AD. 2014. Birthdate and outgrowth timing predict cellular mechanisms of axon target matching in the developing visual pathway. Cell Rep 8:1006–17 [Google Scholar]
  92. Osterhout JA, Josten N, Yamada J, Pan F, Wu SW. et al. 2011. Cadherin-6 mediates axon-target matching in a non-image-forming visual circuit. Neuron 71:632–39 [Google Scholar]
  93. Osterhout JA, Stafford BK, Nguyen PL, Yoshihara Y, Huberman AD. 2015. Contactin-4 mediates axon-target specificity and functional development of the accessory optic system. Neuron 86:985–99 [Google Scholar]
  94. Pang JJ, Gao F, Paul DL, Wu SM. 2012. Rod, M-cone and M/S-cone inputs to hyperpolarizing bipolar cells in the mouse retina. J. Physiol. 590:845–54 [Google Scholar]
  95. Park SJ, Kim IJ, 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]
  96. Perlman I, Kolb H, Nelson R. 2012. S-potentials and horizontal cells Webvision, Moran Eye Cent., Jan. http://webvision.med.utah.edu/book/part-v-phototransduction-in-rods-and-cones/horizontal-cells/
  97. Petros TJ, Rebsam A, Mason CA. 2008. Retinal axon growth at the optic chiasm: to cross or not to cross. Annu. Rev. Neurosci. 31:295–315 [Google Scholar]
  98. Plump AS, Erskine L, Sabatier C, Brose K, Epstein CJ. et al. 2002. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33:219–32 [Google Scholar]
  99. Randlett O, MacDonald RB, Yoshimatsu T, Almeida AD, Suzuki SC. et al. 2013. Cellular requirements for building a retinal neuropil. Cell Rep 3:282–90 [Google Scholar]
  100. Raven MA, Oh EC, Swaroop A, Reese BE. 2007. Afferent control of horizontal cell morphology revealed by genetic respecification of rods and cones. J. Neurosci. 27:3540–47 [Google Scholar]
  101. Ribic A, Liu X, Crair MC, Biederer T. 2014. Structural organization and function of mouse photoreceptor ribbon synapses involve the immunoglobulin protein synaptic cell adhesion molecule 1. J. Comp. Neurol. 522:900–20 [Google Scholar]
  102. Rice DS, Nusinowitz S, Azimi AM, Martinez A, Soriano E, Curran T. 2001. The reelin pathway modulates the structure and function of retinal synaptic circuitry. Neuron 31:929–41 [Google Scholar]
  103. 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. 31:8760–69 [Google Scholar]
  104. Robles E, Laurell E, Baier H. 2014. The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity. Curr. Biol. 24:2085–96 [Google Scholar]
  105. 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]
  106. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M. et al. 2008. Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat. Neurosci. 11:923–31 [Google Scholar]
  107. Schreiner D, Weiner JA. 2010. Combinatorial homophilic interaction between γ-protocadherin multimers greatly expands the molecular diversity of cell adhesion. PNAS 107:14893–98 [Google Scholar]
  108. Schubert T, Hoon M, Euler T, Lukasiewicz PD, Wong RO. 2013. Developmental regulation and activity-dependent maintenance of GABAergic presynaptic inhibition onto rod bipolar cell axonal terminals. Neuron 78:124–37 [Google Scholar]
  109. 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]
  110. Shanks JA, Ito S, Schaevitz L, Yamada J, Chen B. et al. 2016. Corticothalamic axons are essential for retinal ganglion cell axon targeting to the mouse dorsal lateral geniculate nucleus. J. Neurosci. 36:5252–63 [Google Scholar]
  111. Shen N, Qu Y, Yu Y, So KF, Goffinet AM. et al. 2016. Frizzled3 shapes the development of retinal rod bipolar cells. Investig. Ophthalmol. Vis. Sci. 57:2788–96 [Google Scholar]
  112. Simpson JI. 1984. The accessory optic system. Annu. Rev. Neurosci. 7:13–41 [Google Scholar]
  113. Soto F, Ma X, Cecil JL, Vo BQ, Culican SM, Kerschensteiner D. 2012. Spontaneous activity promotes synapse formation in a cell-type-dependent manner in the developing retina. J. Neurosci. 32:5426–39 [Google Scholar]
  114. Soto F, Watkins KL, Johnson RE, Schottler F, Kerschensteiner D. 2013. NGL-2 regulates pathway-specific neurite growth and lamination, synapse formation, and signal transmission in the retina. J. Neurosci. 33:11949–59 [Google Scholar]
  115. Stincic T, Smith RG, Taylor WR. 2016. Time course of EPSCs in ON-type starburst amacrine cells is independent of dendritic location. J. Physiol. 594:5685–94 [Google Scholar]
  116. Strettoi E, Mears AJ, Swaroop A. 2004. Recruitment of the rod pathway by cones in the absence of rods. J. Neurosci. 24:7576–82 [Google Scholar]
  117. Su J, Haner CV, Imbery TE, Brooks JM, Morhardt DR. et al. 2011. Reelin is required for class-specific retinogeniculate targeting. J. Neurosci. 31:575–86 [Google Scholar]
  118. Sun LO, Brady CM, Cahill H, Al-Khindi T, Sakuta H. et al. 2015. Functional assembly of accessory optic system circuitry critical for compensatory eye movements. Neuron 86:971–84 [Google Scholar]
  119. Sun LO, Jiang Z, Rivlin-Etzion M, Hand R, Brady CM. et al. 2013. On and Off retinal circuit assembly by divergent molecular mechanisms. Science 342:1241974 [Google Scholar]
  120. Sweeney NT, James KN, Sales EC, Feldheim DA. 2015. Ephrin-As are required for the topographic mapping but not laminar choice of physiologically distinct RGC types. Dev. Neurobiol. 75:584–93 [Google Scholar]
  121. Szikra T, Trenholm S, Drinnenberg A, Jüttner 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]
  122. Tarpey P, Thomas S, Sarvananthan N, Mallya U, Lisgo S. et al. 2006. Mutations in FRMD7, a newly identified member of the FERM family, cause X-linked idiopathic congenital nystagmus. Nat. Genet. 38:1242–44 [Google Scholar]
  123. Taylor WR, Smith RG. 2012. The role of starburst amacrine cells in visual signal processing. Vis. Neurosci. 29:73–81 [Google Scholar]
  124. Thoreson WB, Mangel SC. 2012. Lateral interactions in the outer retina. Prog. Retin. Eye Res. 31:407–41 [Google Scholar]
  125. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H. et al. 2005. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 168:825–36 [Google Scholar]
  126. Trotter JH, Klein M, Jinwal UK, Abisambra JF, Dickey CA. et al. 2011. ApoER2 function in the establishment and maintenance of retinal synaptic connectivity. J. Neurosci. 31:14413–23 [Google Scholar]
  127. Tsukamoto Y, Morigiwa K, Ishii M, Takao M, Iwatsuki K. et al. 2007. A novel connection between rods and ON cone bipolar cells revealed by ectopic metabotropic glutamate receptor 7 (mGluR7) in mGluR6-deficient mouse retinas. J. Neurosci. 27:6261–67 [Google Scholar]
  128. Tsukamoto Y, Omi N. 2013. Functional allocation of synaptic contacts in microcircuits from rods via rod bipolar to AII amacrine cells in the mouse retina. J. Comp. Neurol. 521:3541–55 [Google Scholar]
  129. Tsukamoto Y, Omi N. 2014a. Some OFF bipolar cell types make contact with both rods and cones in macaque and mouse retinas. Front. Neuroanat. 8:105 [Google Scholar]
  130. Tsukamoto Y, Omi N. 2014b. Effects of mGluR6-deficiency on photoreceptor ribbon synapse formation: comparison of electron microscopic analysis of serial sections with random sections. Vis. Neurosci. 31:39–46 [Google Scholar]
  131. Tu HY, Chiao CC. 2016. Cx36 expression in the AII-mediated rod pathway is activity dependent in the developing rabbit retina. Dev. Neurobiol. 76:473–86 [Google Scholar]
  132. Tummala SR, Dhingra A, Fina ME, Li JJ, Ramakrishnan H, Vardi N. 2016. Lack of mGluR6-related cascade elements leads to retrograde trans-synaptic effects on rod photoreceptor synapses via matrix-associated proteins. Eur. J. Neurosci. 43:1509–22 [Google Scholar]
  133. Vaney DI. 1990. The mosaic of amacrine cells in the mammalian retina. Prog. Retin. Res. 9:49–100 [Google Scholar]
  134. 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]
  135. Vaney DI, Taylor WR. 2002. Direction selectivity in the retina. Curr. Opin. Neurobiol. 12:405–10 [Google Scholar]
  136. 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]
  137. Völgyi B, Deans MR, Paul DL, Bloomfield SA. 2004. Convergence and segregation of the multiple rod pathways in mammalian retina. J. Neurosci. 24:11182–92 [Google Scholar]
  138. Wang Y, Fehlhaber KE, Sarria I, Cao Y, Ingram NT. et al. 2017. The auxiliary calcium channel subunit α2δ4 is required for axonal elaboration, synaptic transmission, and wiring of rod photoreceptors. Neuron 93:61359–74 [Google Scholar]
  139. Wässle H, Peichl L, Boycott BB. 1981. Dendritic territories of cat retinal ganglion cells. Nature 292:344–45 [Google Scholar]
  140. 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 349:70–74 [Google Scholar]
  141. Wilks TA, Harvey Alan R, Rodger J. 2013. Seeing with two eyes: integration of binocular retinal projections in the brain. Functional Brain Mapping and the Endeavor to Understand the Working Brain F Signorelli, D Chirchiglia 227–50 Rijeka, Croat.: InTech [Google Scholar]
  142. Williams SE, Mann F, Erskine L, Sakurai T, Wei S. et al. 2003. Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39:919–35 [Google Scholar]
  143. Williams SE, Mason CA, Herrera E. 2004. The optic chiasm as a midline choice point. Curr. Opin. Neurobiol. 14:51–60 [Google Scholar]
  144. Yamagata M, Sanes JR. 2008. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465–69 [Google Scholar]
  145. Yamagata M, Sanes JR. 2012. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J. Neurosci. 32:14402–14 [Google Scholar]
  146. 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]
  147. Yonehara K, Fiscella M, Drinnenberg A, Esposti F, Trenholm S. et al. 2016. Congenital nystagmus gene FRMD7 is necessary for establishing a neuronal circuit asymmetry for direction selectivity. Neuron 89:177–93 [Google Scholar]
  148. 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:e4320 [Google Scholar]
  149. Zabouri N, Haverkamp S. 2013. Calcium channel-dependent molecular maturation of photoreceptor synapses. PLOS ONE 8:e63853 [Google Scholar]
  150. Zhang C, Rompani SB, Roska B, McCall MA. 2014. Adeno-associated virus-RNAi of GlyRα1 and characterization of its synapse-specific inhibition in OFF alpha transient retinal ganglion cells. J. Neurophysiol. 112:3125–37 [Google Scholar]
  151. Zipursky SL, Sanes JR. 2010. Chemoaffinity revisited: Dscams, protocadherins, and neural circuit assembly. Cell 143:343–53 [Google Scholar]
/content/journals/10.1146/annurev-neuro-072116-031607
Loading
/content/journals/10.1146/annurev-neuro-072116-031607
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