1932

Abstract

Visual information is encoded in distinct retinal ganglion cell (RGC) types in the eye tuned to specific features of the visual space. These streams of information project to the visual thalamus, the first station of the image-forming pathway. In the mouse, this connection between RGCs and thalamocortical neurons, the retinogeniculate synapse, has become a powerful experimental model for understanding how circuits in the thalamus are constructed to process these incoming lines of information. Using modern molecular and genetic tools, recent studies have suggested a more complex circuit organization than was previously understood. In this review, we summarize the current understanding of the structural and functional organization of the retinogeniculate synapse in the mouse. We discuss a framework by which a seemingly complex circuit can effectively integrate and parse information to downstream stations of the visual pathway. Finally, we review how activity and visual experience can sculpt this exquisite connectivity.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-121219-081753
2020-09-15
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/vision/6/1/annurev-vision-121219-081753.html?itemId=/content/journals/10.1146/annurev-vision-121219-081753&mimeType=html&fmt=ahah

Literature Cited

  1. Alonso JM, Usrey WM, Reid RC 1996. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383:6603815–19
    [Google Scholar]
  2. Baden T, Berens P, Franke K, Román Rosón M, Bethge M, Euler T 2016. The functional diversity of retinal ganglion cells in the mouse. Nature 529:7586345–50
    [Google Scholar]
  3. Bickford ME. 2019. Synaptic organization of the dorsal lateral geniculate nucleus. Eur. J. Neurosci. 49:7938–47
    [Google Scholar]
  4. 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. 35:2910523–34
    [Google Scholar]
  5. Blankvoort S, Witter MP, Noonan J, Cotney J, Kentros C 2018. Marked diversity of unique cortical enhancers enables neuron-specific tools by enhancer-driven gene expression. Curr. Biol. 28:132103–14.e5
    [Google Scholar]
  6. Casagrande VA. 1994. A third parallel visual pathway to primate area V1. Trends Neurosci 17:7305–10
    [Google Scholar]
  7. Casagrande VA, Yazar F, Jones KD, Ding Y 2007. The morphology of the koniocellular axon pathway in the macaque monkey. Cereb. Cortex 17:102334–45
    [Google Scholar]
  8. Cheadle L, Tzeng CP, Kalish BT, Harmin DA, Rivera S et al. 2018. Visual experience-dependent expression of Fn14 is required for retinogeniculate refinement. Neuron 99:3525–39.e10
    [Google Scholar]
  9. Chen C, Regehr WG. 2000. Developmental remodeling of the retinogeniculate synapse. Neuron 28:955–66
    [Google Scholar]
  10. 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]
  11. Cleland BG, Dubin MW, Levick WR 1971a. Simultaneous recording of input and output of lateral geniculate neurones. Nat. New Biol. 231:23191–92
    [Google Scholar]
  12. Cleland BG, Dubin MW, Levick WR 1971b. Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J. Physiol. 217:2473–96
    [Google Scholar]
  13. Cleland BG, Levick WR. 1974a. Brisk and sluggish concentrically organized ganglion cells in the cat's retina. J. Physiol. 240:2421–56
    [Google Scholar]
  14. Cleland BG, Levick WR. 1974b. Properties of rarely encountered types of ganglion cells in the cat's retina and on overall classification. J. Physiol. 240:2457–92
    [Google Scholar]
  15. Conley M, Fitzpatrick D. 1989. Morphology of retinogeniculate axons in the macaque. Vis. Neurosci. 2:03287–96
    [Google Scholar]
  16. 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]
  17. Dacey DM, Packer OS. 2003. Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr. Opin. Neurobiol. 13:4421–27
    [Google Scholar]
  18. Denman DJ, Contreras D. 2016. On parallel streams through the mouse dorsal lateral geniculate nucleus. Front. Neural Circuits 10:20
    [Google Scholar]
  19. Dhande OS, Stafford BK, Lim JA, Huberman AD 2015. Contributions of retinal ganglion cells to subcortical visual processing and behaviors. Annu. Rev. Vis. Sci. 1:291–328
    [Google Scholar]
  20. Dhande OS, Hua EW, Guh E, Yeh J, Bhatt S et al. 2011. Development of single retinofugal axon arbors in normal and 2 knock-out mice. J. Neurosci. 31:93384–99
    [Google Scholar]
  21. Dimidschstein J, Chen Q, Tremblay R, Rogers SL, Saldi GA et al. 2016. A viral strategy for targeting and manipulating interneurons across vertebrate species. Nat. Neurosci. 19:121743–49
    [Google Scholar]
  22. Duan X, Qiao M, Bei F, Kim IJ, Sanes JR 2015. Subtype-specific regeneration of retinal ganglion cells following axotomy: effects of osteopontin and mTOR signaling. Neuron 85:61244–56
    [Google Scholar]
  23. Eiber CD, Rahman AS, Pietersen ANJ, Zeater N, Dreher B et al. 2018. Receptive field properties of koniocellular On/Off neurons in the lateral geniculate nucleus of marmoset monkeys. J. Neurosci. 38:4810384–98
    [Google Scholar]
  24. Feldheim DA, Vanderhaeghen P, Hansen MJ, Frisén J, Lu Q et al. 1998. Topographic guidance labels in a sensory projection to the forebrain. Neuron 21:61303–13
    [Google Scholar]
  25. Fitzpatrick D, Itoh K, Diamond IT 1983. The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). J. Neurosci. 3:4673–702
    [Google Scholar]
  26. Garraghty PE, Sur M, Weller RE, Sherman SM 1986. Morphology of retinogeniculate X and Y axon arbors in monocularly enucleated cats. J. Comp. Neurol. 251:2198–215
    [Google Scholar]
  27. Graham J. 1977. An autoradiographic study of the efferent connections of the superior colliculus in the cat. J. Comp. Neurol. 173:4629–54
    [Google Scholar]
  28. Grant E, Hoerder-Suabedissen A, Molnár Z 2016. The regulation of corticofugal fiber targeting by retinal inputs. Cereb. Cortex 26:31336–48
    [Google Scholar]
  29. Grubb MS, Thompson ID. 2003. Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. J. Neurophysiol. 90:63594–607
    [Google Scholar]
  30. 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. Vis. Res. 44:283365–76
    [Google Scholar]
  31. Guido W. 2008. Refinement of the retinogeniculate pathway. J. Physiol. 586:Pt. 184357–62
    [Google Scholar]
  32. Guido W. 2018. Development, form, and function of the mouse visual thalamus. J. Neurophysiol. 120:1211–25
    [Google Scholar]
  33. 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 12:101575–83
    [Google Scholar]
  34. Hamos JE, Van Horn SC, Raczkowski D, Sherman SM 1987. Synaptic circuits involving an individual retinogeniculate axon in the cat. J. Comp. Neurol. 259:2165–92
    [Google Scholar]
  35. Harting JK, Casagrande VA, Weber JT 1978. The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons. Brain Res 150:3593–99
    [Google Scholar]
  36. 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]
  37. Hendry SH, Reid RC. 2000. The koniocellular pathway in primate vision. Annu. Rev. Neurosci. 23:127–53
    [Google Scholar]
  38. Hickey TL, Guillery RW. 1974. An autoradiographic study of retinogeniculate pathways in the cat and the fox. J. Comp. Neurol. 156:2239–53
    [Google Scholar]
  39. Hodge RD, Bakken TE, Miller JA, Smith KA, Barkan ER et al. 2019. Conserved cell types with divergent features in human versus mouse cortex. Nature 573:777261–68
    [Google Scholar]
  40. Hong YK, Burr EF, Sanes JR, Chen C 2019. Heterogeneity of retinogeniculate axon arbors. Eur. J. Neurosci. 49:7948–56
    [Google Scholar]
  41. Hong YK, Chen C. 2011. Wiring and rewiring of the retinogeniculate synapse. Curr. Opin. Neurobiol. 21:2228–37
    [Google Scholar]
  42. Hong YK, Park S, Litvina EY, Morales J, Sanes JR, Chen C 2014. Refinement of the retinogeniculate synapse by bouton clustering. Neuron 84:2332–39
    [Google Scholar]
  43. Hooks BM, Chen C. 2006. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52:2281–91
    [Google Scholar]
  44. Hooks BM, Chen C. 2008. Vision triggers an experience-dependent sensitive period at the retinogeniculate synapse. J. Neurosci. 28:184807–17
    [Google Scholar]
  45. Howarth M, Walmsley L, Brown TM 2014. Binocular integration in the mouse lateral geniculate nuclei. Curr. Biol. 24:111241–47
    [Google Scholar]
  46. Hubel DH, Wiesel TN. 1961. Integrative action in the cat's lateral geniculate body. J. Physiol. 155:385–98
    [Google Scholar]
  47. 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]
  48. Huberman AD, Feller MB, Chapman B 2008a. Mechanisms underlying development of visual maps and receptive fields. Annu. Rev. Neurosci. 31:479–509
    [Google Scholar]
  49. 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]
  50. 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]
  51. Irvin GE, Casagrande VA, Norton TT 1993. Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus. Vis. Neurosci. 10:2363–73
    [Google Scholar]
  52. Irvin GE, Norton TT, Sesma MA, Casagrande VA 1986. W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Res 362:2254–70
    [Google Scholar]
  53. Isaac JT, Nicoll RA, Malenka RC 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron 15:2427–34
    [Google Scholar]
  54. Jacobs EC, Campagnoni C, Kampf K, Reyes SD, Kalra SD et al. 2007. Visualization of corticofugal projections during early cortical development in a τ-GFP-transgenic mouse. Eur. J. Neurosci. 25:117–30
    [Google Scholar]
  55. Jaepel J, Hübener M, Bonhoeffer T, Rose T 2017. Lateral geniculate neurons projecting to primary visual cortex show ocular dominance plasticity in adult mice. Nat. Neurosci. 20:121708–14
    [Google Scholar]
  56. Jaubert-Miazza L, Green E, Lo FS, 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]
  57. Jones EG, Hendry SH. 1989. Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur. J. Neurosci. 1:3222–46
    [Google Scholar]
  58. Jurgens CW, Bell KA, McQuiston AR, Guido W 2012. Optogenetic stimulation of the corticothalamic pathway affects relay cells and GABAergic neurons differently in the mouse visual thalamus. PLOS ONE 7:9e45717
    [Google Scholar]
  59. Kalish BT, Cheadle L, Hrvatin S, Nagy MA, Rivera S et al. 2018. Single-cell transcriptomics of the developing lateral geniculate nucleus reveals insights into circuit assembly and refinement. PNAS 115:5E1051–60
    [Google Scholar]
  60. Kaplan E, Shapley R. 1984. The origin of the S (slow) potential in the mammalian lateral geniculate nucleus. Exp. Brain Res. 55:1111–16
    [Google Scholar]
  61. 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. 31:217753–62
    [Google Scholar]
  62. Kerschensteiner D, Guido W. 2017. Organization of the dorsal lateral geniculate nucleus in the mouse. Vis. Neurosci. 34:80–89
    [Google Scholar]
  63. Kielland A, Bochorishvili G, Corson J, Zhang L, Rosin DL et al. 2009. Activity patterns govern synapse-specific AMPA receptor trafficking between deliverable and synaptic pools. Neuron 62:184–101
    [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. 30:41452–62
    [Google Scholar]
  65. Krahe TE, El-Danat 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]
  66. Kratz KE, Sherman SM, Kalil R 1979. Lateral geniculate nucleus in dark-reared cats: loss of Y cells without changes in cell size. Science 203:43871353–55
    [Google Scholar]
  67. Kühn NK, Gollisch T. 2019. Activity correlations between direction-selective retinal ganglion cells synergistically enhance motion decoding from complex visual scenes. Neuron 101:5963–76.e7
    [Google Scholar]
  68. Lachica EA, Casagrande VA. 1993. The morphology of collicular and retinal axons ending on small relay (W-like) cells of the primate lateral geniculate nucleus. Vis. Neurosci. 10:3403–18
    [Google Scholar]
  69. Lehmkuhle S, Kratz KE, Mangel SC, Sherman SM 1978. An effect of early monocular lid suture upon the development of X-cells in the cat's lateral geniculate nucleus. Brain Res 157:2346–50
    [Google Scholar]
  70. Levick WR, Cleland BG, Dubin MW 1972. Lateral geniculate neurons of cat: retinal inputs and physiology. Investig. Ophthalmol. 11:5302–11
    [Google Scholar]
  71. Li YT, Ma WP, Li LY, Ibrahim LA, Wang SZ, Tao HW 2012. Broadening of inhibitory tuning underlies contrast-dependent sharpening of orientation selectivity in mouse visual cortex. J. Neurosci. 32:4616466–77
    [Google Scholar]
  72. Liang L, Fratzl A, Goldev O, Ramesh RN, Sugden AU et al. 2018. A fine-scale functional logic to convergence from retina to thalamus. Cell 173:61343–55.e24
    [Google Scholar]
  73. Litvina EY, Chen C. 2017a. An evolving view of retinogeniculate transmission. Vis. Neurosci. 34:E013
    [Google Scholar]
  74. Litvina EY, Chen C. 2017b. Functional convergence at the retinogeniculate synapse. Neuron 96:2330–38.e5
    [Google Scholar]
  75. Liu X, Chen C. 2008. Different roles for AMPA and NMDA receptors in transmission at the immature retinogeniculate synapse. J. Neurophysiol. 99:2629–43
    [Google Scholar]
  76. Lund RD, Bunt AH. 1976. Prenatal development of central optic pathways in albino rats. J. Comp. Neurol. 165:2247–64
    [Google Scholar]
  77. Lund RD, Lund JS. 1976. Plasticity in the developing visual system: the effects of retinal lesions made in young rats. J. Comp. Neurol. 169:2133–54
    [Google Scholar]
  78. Lund RD, Lund JS, Wise RP 1974. The organization of the retinal projection to the dorsal lateral geniculate nucleus in pigmented and albino rats. J. Comp. Neurol. 158:4383–403
    [Google Scholar]
  79. 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]
  80. Martersteck EM, Hirokawa KE, Evarts M, Bernard A, Duan X et al. 2017. Diverse central projection patterns of retinal ganglion cells. Cell Rep 18:82058–72
    [Google Scholar]
  81. Martin PR. 1986. The projection of different retinal ganglion cell classes to the dorsal lateral geniculate nucleus in the hooded rat. Exp. Brain Res. 62:177–88
    [Google Scholar]
  82. Martin PR, White AJ, Goodchild AK, Wilder HD, Sefton AE 1997. Evidence that blue‐on cells are part of the third geniculocortical pathway in primates. Eur. J. Neurosci. 9:71536–41
    [Google Scholar]
  83. Martinez LM, Molano-Mazón M, Wang X, Sommer FT, Hirsch JA 2014. Statistical wiring of thalamic receptive fields optimizes spatial sampling of the retinal image. Neuron 81:4943–56
    [Google Scholar]
  84. Mason CA. 1982. Development of terminal arbors of retino-geniculate axons in the kitten—I. Light microscopical observations. Neuroscience 7:3541–59
    [Google Scholar]
  85. Mastronarde DN. 1987. Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J. Neurophysiol. 57:2381–413
    [Google Scholar]
  86. Mastronarde DN. 1992. Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: receptive-field properties and retinal inputs. Vis. Neurosci. 8:5407–41
    [Google Scholar]
  87. McIlhinney RA, Bacon SJ, Smith AD 1988. A simple and rapid method for the production of cholera B-chain coupled to horseradish peroxidase for neuronal tracing. J. Neurosci. Methods 22:3189–94
    [Google Scholar]
  88. Meister M, Lagnado L, Baylor DA 1995. Concerted signaling by retinal ganglion cells. Science 270:52391207–10
    [Google Scholar]
  89. Mize RR, Spencer RF, Horner LH 1986. Quantitative comparison of retinal synapses in the dorsal and ventral (parvicellular) C laminae of the cat dorsal lateral geniculate nucleus. J. Comp. Neurol. 248:157–73
    [Google Scholar]
  90. Monavarfeshani A, Sabbagh U, Fox MA 2017. Not a one-trick pony: diverse connectivity and functions of the rodent lateral geniculate complex. Vis. Neurosci. 34:E012
    [Google Scholar]
  91. Moore BD IV, Kiley CW, Sun C, Usrey WM 2011. Rapid plasticity of visual responses in the adult lateral geniculate nucleus. Neuron 71:5812–19
    [Google Scholar]
  92. Morgan JL, Berger DR, Wetzel AW, Lichtman JW 2016. The fuzzy logic of network connectivity in mouse visual thalamus. Cell 165:1192–206
    [Google Scholar]
  93. Mower GD, Burchfiel JL, Duffy FH 1982. Animal models of strabismic amblyopia: physiological studies of visual cortex and the lateral geniculate nucleus. Brain Res 281:3311–27
    [Google Scholar]
  94. Muir-Robinson G, Hwang BJ, Feller MB 2002. Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J. Neurosci. 22:135259–64
    [Google Scholar]
  95. Nassi JJ, Callaway EM. 2009. Parallel processing strategies of the primate visual system. Nat. Rev. Neurosci. 10:5360–72
    [Google Scholar]
  96. Peichl L, Wässle H. 1979. Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. J. Physiol. 291:1117–41
    [Google Scholar]
  97. Peng YR, Shekhar K, Yan W, Herrmann D, Sappington A et al. 2019. Molecular classification and comparative taxonomics of foveal and peripheral cells in primate retina. Cell 176:51222–37.e22
    [Google Scholar]
  98. Peters A, Payne BR. 1993. Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cerebrol. Cortex 3:169–78
    [Google Scholar]
  99. 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]
  100. 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]
  101. Rafols JA, Valverde F. 1973. The structure of the dorsal lateral geniculate nucleus in the mouse: a Golgi and electron microscopic study. J. Comp. Neurol. 150:3303–32
    [Google Scholar]
  102. Reese BE. 1988. “Hidden lamination” in the dorsal lateral geniculate nucleus: the functional organization of this thalamic region in the rat. Brain Res. Rev. 13:2119–37
    [Google Scholar]
  103. Rheaume BA, Jereen A, Bolisetty M, Sajid MS, Yang Y et al. 2018. Single cell transcriptome profiling of retinal ganglion cells identifies cellular subtypes. Nat. Commun. 9:12759
    [Google Scholar]
  104. 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]
  105. Rodieck RW. 1967. Receptive fields in the cat retina: a new type. Science 157:378490–92
    [Google Scholar]
  106. Román Rosón M, Bauer Y, Kotkat AH, Berens P, Euler T, Busse L 2019. Mouse dLGN receives functional input from a diverse population of retinal ganglion cells with limited convergence. Neuron 102:2462–76.e8
    [Google Scholar]
  107. Rompani SB, Müllner FE, Wanner A, Zhang C, Roth CN et al. 2017. Different modes of visual integration in the lateral geniculate nucleus revealed by single-cell-initiated transsynaptic tracing. Neuron 93:4767–76.e6
    [Google Scholar]
  108. Rose T, Bonhoeffer T. 2018. Experience-dependent plasticity in the lateral geniculate nucleus. Curr. Opin. Neurobiol. 53:22–28
    [Google Scholar]
  109. Rousso DL, Qiao M, Kagan RD, Yamagata M, Palmiter RD, Sanes JR 2016. Two pairs of ON and OFF retinal ganglion cells are defined by intersectional patterns of transcription factor expression. Cell Rep 15:91930–44
    [Google Scholar]
  110. 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]
  111. Schein SJ, de Monasterio FM 1987. Mapping of retinal and geniculate neurons onto striate cortex of macaque. J. Neurosci. 7:4996–1009
    [Google Scholar]
  112. Scholl B, Tan AY, Corey J, Priebe NJ 2013. Emergence of orientation selectivity in the mammalian visual pathway. J. Neurosci. 33:2610616–24
    [Google Scholar]
  113. Seabrook TA, El-Danaf RN, Krahe TE, Fox MA, Guido W 2013. Retinal input regulates the timing of corticogeniculate innervation. J. Neurosci. 33:2410085–97
    [Google Scholar]
  114. Shatz CJ, Rakic P. 1981. The genesis of efferent connections from the visual cortex of the fetal rhesus monkey. J. Comp. Neurol. 196:2287–307
    [Google Scholar]
  115. Sherman SM, Guillery RW. 2001. Exploring the Thalamus Amsterdam: Elsevier
  116. Sherman SM, Spear PD. 1982. Organization of visual pathways in normal and visually deprived cats. Physiol. Rev. 62:2738–855
    [Google Scholar]
  117. Sincich LC, Adams DL, Economides JR, Horton JC 2007. Transmission of spike trains at the retinogeniculate synapse. J. Neurosci. 27:102683–92
    [Google Scholar]
  118. Sommeijer J-P, Ahmadlou M, Saiepour MH, Seignette K, Min R et al. 2017. Thalamic inhibition regulates critical-period plasticity in visual cortex and thalamus. Nat. Neurosci. 20:121715–21
    [Google Scholar]
  119. Spear PD, Kim CB, Ahmad A, Tom BW 1996. Relationship between numbers of retinal ganglion cells and lateral geniculate neurons in the rhesus monkey. Vis. Neurosci. 13:1199–203
    [Google Scholar]
  120. Sretavan DW, Shatz CJ. 1987. Axon trajectories and pattern of terminal arborization during the prenatal development of the cat's retinogeniculate pathway. J. Comp. Neurol. 255:3386–400
    [Google Scholar]
  121. Sretavan DW, Shatz CJ, Stryker MP 1988. Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:6198468–71
    [Google Scholar]
  122. Stafford BK, Huberman AD. 2017. Signal integration in thalamus: Labeled lines go cross-eyed and blurry. Neuron 93:4717–20
    [Google Scholar]
  123. Stanford LR, Friedlander MJ, Sherman SM 1983. Morphological and physiological properties of geniculate W-cells of the cat: a comparison with X- and Y-cells. J. Neurophysiol. 50:3582–608
    [Google Scholar]
  124. Stone J. 1978. The number and distribution of ganglion cells in the cat's retina. J. Comp. Neurol. 180:4753–71
    [Google Scholar]
  125. Stone J. 2013. Parallel Processing in the Visual System Berlin: Springer
  126. Stone J, Fabian M. 1966. Specialized receptive fields of the cat's retina. Science 152:37261277–79
    [Google Scholar]
  127. Stone J, Fukuda Y. 1974. Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells. J. Neurophysiol. 37:4722–48
    [Google Scholar]
  128. 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. 5:266–47
    [Google Scholar]
  129. Sun W, Tan Z, Mensh BD, Ji N 2016. Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs. Nat. Neurosci. 19:2308–15
    [Google Scholar]
  130. Sur M, Esguerra M, Garraghty PE, Kritzer MF, Sherman SM 1987. Morphology of physiologically identified retinogeniculate X- and Y-axons in the cat. J. Neurophysiol. 58:11–32
    [Google Scholar]
  131. Sur M, Sherman SM. 1982. Retinogeniculate terminations in cats: morphological differences between X and Y cell axons. Science 218:4570389–91
    [Google Scholar]
  132. Suresh V, Çiftçioğlu UM, Wang X, Lala BM, Ding KR et al. 2016. Synaptic contributions to receptive field structure and response properties in the rodent lateral geniculate nucleus of the thalamus. J. Neurosci. 36:4310949–63
    [Google Scholar]
  133. Tailby C, Solomon SG, Dhrug NT, Majaj NJ, Sokol SH, Lennie P 2007. A new code for contrast in the primate visual pathway. J. Neurosci. 27:143904–9
    [Google Scholar]
  134. Tang J, Ardila Jimenez SC, Chakraborty S, Schultz SR 2016. Visual receptive field properties of neurons in the mouse lateral geniculate nucleus. PLOS ONE 11:1e0146017
    [Google Scholar]
  135. Thompson AD, Picard N, Min L, Fagiolini M, Chen C 2016. Cortical feedback regulates feedforward retinogeniculate refinement. Neuron 91:51021–33
    [Google Scholar]
  136. Torborg CL, Feller MB. 2004. Unbiased analysis of bulk axonal segregation patterns. J. Neurosci. Methods 135:1–217–26
    [Google Scholar]
  137. Tschetter WW, Govindaiah G, Etherington IM, Guido W, Niell CM 2018. Refinement of spatial receptive fields in the developing mouse lateral geniculate nucleus is coordinated with excitatory and inhibitory remodeling. J. Neurosci. 38:194531–42
    [Google Scholar]
  138. Usrey WM, Alitto HJ. 2015. Visual functions of the thalamus. Annu. Rev. Vis. Sci. 1:351–71
    [Google Scholar]
  139. Usrey WM, Reppas JB, Reid RC 1999. Specificity and strength of retinogeniculate connections. J. Neuro-physiol. 82:63527–40
    [Google Scholar]
  140. Wallace DJ, Fitzpatrick D, Kerr JND 2016. Primate thalamus: more than meets an eye. Curr. Biol. 26:2R60–61
    [Google Scholar]
  141. Wässle H, Boycott BB, Illing RB 1981. Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proc. R. Soc. Lond. B 212:1187177–95
    [Google Scholar]
  142. Weyand TG. 2016. The multifunctional lateral geniculate nucleus. Rev. Neurosci. 27:2135–57
    [Google Scholar]
  143. White AJ, Solomon SG, Martin PR 2001. Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus. J. . Physiol 533:Pt. 2519–35
    [Google Scholar]
  144. Williams RW, Strom RC, Rice DS, Goldowitz D 1996. Genetic and environmental control of variation in retinal ganglion cell number in mice. J. Neurosci. 16:227193–205
    [Google Scholar]
  145. Wilson PD, Rowe MH, Stone J 1976. Properties of relay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells. J. Neurophysiol. 39:61193–209
    [Google Scholar]
  146. Xu X, Ichida JM, Allison JD, Boyd JD, Bonds AB, Casagrande VA 2001. A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). J. Physiol. 531:Pt. 1203–18
    [Google Scholar]
  147. Yeh CI, Stoelzel CR, Weng C, Alonso JM 2009. Functional consequences of neuronal divergence within the retinogeniculate pathway. J. Neurophysiol. 101:42166–85
    [Google Scholar]
  148. Zeater N, Cheong SK, Solomon SG, Dreher B, Martin PR 2015. Binocular visual responses in the primate lateral geniculate nucleus. Curr. Biol. 25:243190–95
    [Google Scholar]
  149. 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]
/content/journals/10.1146/annurev-vision-121219-081753
Loading
/content/journals/10.1146/annurev-vision-121219-081753
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