1932

Abstract

Visual motion on the retina activates a cohort of retinal ganglion cells (RGCs). This population activity encodes multiple streams of information extracted by parallel retinal circuits. Motion processing in the retina is best studied in the direction-selective circuit. The main focus of this review is the neural basis of direction selectivity, which has been investigated in unprecedented detail using state-of-the-art functional, connectomic, and modeling methods. Mechanisms underlying the encoding of other motion features by broader RGC populations are also discussed. Recent discoveries at both single-cell and population levels highlight the dynamic and stimulus-dependent engagement of multiple mechanisms that collectively implement robust motion detection under diverse visual conditions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-091517-034048
2018-09-15
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/vision/4/1/annurev-vision-091517-034048.html?itemId=/content/journals/10.1146/annurev-vision-091517-034048&mimeType=html&fmt=ahah

Literature Cited

  1. Ackert JM, Farajian R, Völgyi B, Bloomfield SA 2009. GABA blockade unmasks an OFF response in ON direction selective ganglion cells in the mammalian retina. J. Physiol. 587:184481–95
    [Google Scholar]
  2. Ackert JM, Wu SH, Lee JC, Abrams J, Hu EH et al. 2006. Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. J. Neurosci. 26:164206–15
    [Google Scholar]
  3. Amthor FR, Keyser KT, Dmitrieva NA 2002. Effects of the destruction of starburst-cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity. Vis. Neurosci. 19:4495–509
    [Google Scholar]
  4. Amthor FR, Oyster CW 1995. Spatial organization of retinal information about the direction of image motion. PNAS 92:94002–5
    [Google Scholar]
  5. Amthor FR, Oyster CW, Takahashi ES 1984. Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Res 298:1187–90
    [Google Scholar]
  6. Amthor FR, Takahashi ES, Oyster CW 1989. Morphologies of rabbit retinal ganglion cells with complex receptive fields. J. Comp. Neurol. 280:197–121
    [Google Scholar]
  7. Amthor FR, Tootle JS, Grzywacz NM 2005. Stimulus-dependent correlated firing in directionally selective retinal ganglion cells. Vis. Neurosci. 22:6769–87
    [Google Scholar]
  8. 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]
  9. Barlow HB, Hill RM 1963. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139:3553412–14
    [Google Scholar]
  10. Barlow HB, Hill RM, Levick WR 1964. Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol. 173:377–407
    [Google Scholar]
  11. Barlow HB, Levick WR 1965. The mechanism of directionally selective units in rabbit's retina. J. Physiol. 178:3477–504
    [Google Scholar]
  12. Berry MJ, Brivanlou IH, Jordan TA, Meister M 1999. Anticipation of moving stimuli by the retina. Nature 398:6725334–38
    [Google Scholar]
  13. Berson DM 2008. Retinal ganglion cell types and their central projections. The Senses: A Comprehensive Reference, Vol. 1 TD Albright, R Masland 491–520 San Diego, CA: Academic
    [Google Scholar]
  14. Brecha N, Johnson D, Peichl L, Wässle H 1988. Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. PNAS 85:166187–91
    [Google Scholar]
  15. Briggman KL, Helmstaedter M, Denk W 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:7337183–88
    [Google Scholar]
  16. Brombas A, Kalita-de Croft S, Cooper-Williams EJ, Williams SR 2017. Dendro-dendritic cholinergic excitation controls dendritic spike initiation in retinal ganglion cells. Nat. Commun. 8:15683
    [Google Scholar]
  17. Buhl EH, Peichl L 1986. Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. J. Comp. Neurol. 253:2163–74
    [Google Scholar]
  18. Buldyrev I, Taylor WR 2013. Inhibitory mechanisms that generate centre and surround properties in ON and OFF brisk-sustained ganglion cells in the rabbit retina. J. Physiol. 591:1303–25
    [Google Scholar]
  19. Cafaro J, Rieke F 2010. Noise correlations improve response fidelity and stimulus encoding. Nature 468:7326964–67
    [Google Scholar]
  20. Chen M, Lee S, Park SJH, Looger LL, Zhou ZJ 2014. Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina. J. Neurophysiol. 112:81950–62
    [Google Scholar]
  21. Chen Q, Pei Z, Koren D, Wei W 2016. Stimulus-dependent recruitment of lateral inhibition underlies retinal direction selectivity. eLife 5:e21053
    [Google Scholar]
  22. Chen Q, Wei W 2018. Stimulus-dependent engagement of neural mechanisms for reliable motion detection in the mouse retina. J. Neurophysiol. In press. https://doi.org/10.1152/jn.00716.2017
    [Crossref] [Google Scholar]
  23. Chiao C-C, Masland RH 2003. Contextual tuning of direction-selective retinal ganglion cells. Nat. Neurosci. 6:121251–52
    [Google Scholar]
  24. Chichilnisky EJ, Kalmar RS 2002. Functional asymmetries in ON and OFF ganglion cells of primate retina. J. Neurosci. 22:72737–47
    [Google Scholar]
  25. Clark DA, Demb JB 2016. Parallel computations in insect and mammalian visual motion processing. Curr. Biol. 26:20R1062–72
    [Google Scholar]
  26. 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]
  27. David SV, Vinje WE, Gallant JL 2004. Natural stimulus statistics alter the receptive field structure of V1 neurons. J. Neurosci. 24:316991–7006
    [Google Scholar]
  28. Deny S, Ferrari U, Macé E, Yger P, Caplette R et al. 2017. Multiplexed computations in retinal ganglion cells of a single type. Nat. Commun. 8:11964
    [Google Scholar]
  29. Devries SH, Baylor DA 1997. Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J. Neurophysiol. 78:42048–60
    [Google Scholar]
  30. 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]
  31. Ding H, Smith RG, Poleg-Polsky A, Diamond JS, Briggman KL 2016. Species-specific wiring for direction selectivity in the mammalian retina. Nature 535:7610105–10
    [Google Scholar]
  32. Elstrott J, Anishchenko A, Greschner M, Sher A, Litke AM et al. 2008. Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves. Neuron 58:4499–506
    [Google Scholar]
  33. Euler T, Detwiler PB, Denk W 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:6900845–52
    [Google Scholar]
  34. Famiglietti EV 1983. “Starburst” amacrine cells and cholinergic neurons: mirror-symmetric on and off amacrine cells of rabbit retina. Brain Res 261:1138–44
    [Google Scholar]
  35. 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. 309:140–70
    [Google Scholar]
  36. Famiglietti EV 1992. Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. J. Comp. Neurol. 324:3322–35
    [Google Scholar]
  37. Felsen G, Dan Y 2005. A natural approach to studying vision. Nat. Neurosci. 8:121643–46
    [Google Scholar]
  38. Felsen G, Touryan J, Han F, Dan Y 2005. Cortical sensitivity to visual features in natural scenes. PLOS Biol 3:10e342
    [Google Scholar]
  39. Fiscella M, Franke F, Farrow K, Müller J, Roska B et al. 2015. Visual coding with a population of direction-selective neurons. J. Neurophysiol. 114:42485–99
    [Google Scholar]
  40. Franke K, Berens P, Schubert T, Bethge M, Euler T, Baden T 2017. Inhibition decorrelates visual feature representations in the inner retina. Nature 542:439–44
    [Google Scholar]
  41. Fransen JW, Borghuis BG 2017. Temporally diverse excitation generates direction-selective responses in ON- and OFF-type retinal starburst amacrine cells. Cell Rep 18:61356–65
    [Google Scholar]
  42. Fried SI, Münch TA, Werblin FS 2002. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420:6914411–14
    [Google Scholar]
  43. Fried SI, Münch TA, Werblin FS 2005. Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46:1117–27
    [Google Scholar]
  44. Gavrikov KE, Nilson JE, Dmitriev AV, Zucker CL, Mangel SC 2006. Dendritic compartmentalization of chloride cotransporters underlies directional responses of starburst amacrine cells in retina. PNAS 103:4918793–98
    [Google Scholar]
  45. Geffen MN, de Vries SEJ, Meister M 2007. Retinal ganglion cells can rapidly change polarity from Off to On. PLOS Biol 5:3e65
    [Google Scholar]
  46. Greene MJ, Kim JS, Seung HS, EyeWirers 2016. Analogous convergence of sustained and transient inputs in parallel on and off pathways for retinal motion computation. Cell Rep 14:81892–1900
    [Google Scholar]
  47. Grzywacz NM, Amthor FR, Merwine DK 1998.a Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit. J. Physiol. 512:2575–81
    [Google Scholar]
  48. Grzywacz NM, Merwine DK, Amthor FR 1998.b Complementary roles of two excitatory pathways in retinal directional selectivity. Vis. Neurosci. 15:61119–27
    [Google Scholar]
  49. 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]
  50. Hausselt SE, Euler T, Detwiler PB, Denk W 2007. A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLOS Biol 5:7e185
    [Google Scholar]
  51. He S, Masland RH 1998. ON direction-selective ganglion cells in the rabbit retina: dendritic morphology and pattern of fasciculation. Vis. Neurosci. 15:2369–75
    [Google Scholar]
  52. Hedges JH, Gartshteyn Y, Kohn A, Rust NC, Shadlen MN et al. 2011. Dissociation of neuronal and psychophysical responses to local and global motion. Curr. Biol. 21:232023–28
    [Google Scholar]
  53. Helmstaedter M, Briggman KL, Turaga SC, Jain V, Seung HS, Denk W 2013. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500:7461168–74
    [Google Scholar]
  54. Hillier D, Fiscella M, Drinnenberg A, Trenholm S, Rompani SB et al. 2017. Causal evidence for retina-dependent and -independent visual motion computations in mouse cortex. Nat. Neurosci. 20:7960–68
    [Google Scholar]
  55. Hoshi H, Tian L-M, Massey SC, Mills SL 2011. Two distinct types of ON directionally selective ganglion cells in the rabbit retina. J. Comp. Neurol. 519:132509–21
    [Google Scholar]
  56. 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]
  57. Ichinose T, Fyk-Kolodziej B, Cohn J 2014. Roles of ON cone bipolar cell subtypes in temporal coding in the mouse retina. J. Neurosci. 34:268761–71
    [Google Scholar]
  58. Im M, Fried SI 2016. Directionally selective retinal ganglion cells suppress luminance responses during natural viewing. Sci. Rep. 6:135708
    [Google Scholar]
  59. 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. 35:207992–8003
    [Google Scholar]
  60. Jacoby J, Schwartz GW 2017. Three small-receptive-field ganglion cells in the mouse retina are distinctly tuned to size, speed, and object motion. J. Neurosci. 37:3610–25
    [Google Scholar]
  61. Jakobs TC, Koizumi A, Masland RH 2008. The spatial distribution of glutamatergic inputs to dendrites of retinal ganglion cells. J. Comp. Neurol. 510:2221–36
    [Google Scholar]
  62. Jeon C-J, Kong J-H, Strettoi E, Rockhill R, Stasheff SF, Masland RH 2002. Pattern of synaptic excitation and inhibition upon direction-selective retinal ganglion cells. J. Comp. Neurol. 449:2195–205
    [Google Scholar]
  63. Joesch M, Meister M 2016. A neuronal circuit for colour vision based on rod-cone opponency. Nature 532:7598236–39
    [Google Scholar]
  64. Johnston J, Ding H, Seibel SH, Esposti F, Lagnado L 2014. Rapid mapping of visual receptive fields by filtered back projection: application to multi-neuronal electrophysiology and imaging. J. Physiol. 592:224839–54
    [Google Scholar]
  65. Kanjhan R, Sivyer B 2010. Two types of ON direction-selective ganglion cells in rabbit retina. Neurosci. Lett. 483:2105–9
    [Google Scholar]
  66. Kanjhan R, Vaney DI 2008. Semi-loose seal Neurobiotin electroporation for combined structural and functional analysis of neurons. Pflügers Arch. Eur. J. Physiol. 457:2561–68
    [Google Scholar]
  67. 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]
  68. Keeley PW, Whitney IE, Raven MA, Reese BE 2007. Dendritic spread and functional coverage of starburst amacrine cells. J. Comp. Neurol. 505:5539–46
    [Google Scholar]
  69. 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]
  70. 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]
  71. Kim T, Kerschensteiner D 2017. Inhibitory control of feature selectivity in an object motion sensitive circuit of the retina. Cell Rep 19:71343–50
    [Google Scholar]
  72. Kim T, Soto F, Kerschensteiner D 2015. An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in the mouse retina. eLife 4:e08025
    [Google Scholar]
  73. Kittila CA, Massey SC 1995. Effect of ON pathway blockade on directional selectivity in the rabbit retina. J. Neurophysiol. 73:2703–12
    [Google Scholar]
  74. Kittila CA, Massey SC 1997. Pharmacology of directionally selective ganglion cells in the rabbit retina. J. Neurophysiol. 77:2675–89
    [Google Scholar]
  75. Komban SJ, Kremkow J, Jin J, Wang Y, Lashgari R et al. 2014. Neuronal and perceptual differences in the temporal processing of darks and lights. Neuron 82:1224–34
    [Google Scholar]
  76. Koren D, Grove JCR, Wei W 2017. Cross-compartmental modulation of dendritic signals for retinal direction selectivity. Neuron 95:4914–27.e4
    [Google Scholar]
  77. Kostadinov D, Sanes JR 2015. Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function. eLife 4:e08964
    [Google Scholar]
  78. Krishnamoorthy V, Weick M, Gollisch T 2017. Sensitivity to image recurrence across eye-movement-like image transitions through local serial inhibition in the retina. eLife 6:e22431
    [Google Scholar]
  79. 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]
  80. Kuo SP, Schwartz GW, Rieke F 2016. Nonlinear spatiotemporal integration by electrical and chemical synapses in the retina. Neuron 90:2320–32
    [Google Scholar]
  81. Lee K-S, Huang X, Fitzpatrick D 2016. Topology of ON and OFF inputs in visual cortex enables an invariant columnar architecture. Nature 533:760190–94
    [Google Scholar]
  82. 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]
  83. Lee S, Kim K, Zhou ZJ 2010. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68:61159–72
    [Google Scholar]
  84. Lee S, Zhang Y, Chen M, Zhou ZJ 2016. Segregated glycine-glutamate co-transmission from vGluT3 amacrine cells to contrast-suppressed and contrast-enhanced retinal circuits. Neuron 90:127–34
    [Google Scholar]
  85. Lee S, Zhou ZJ 2006. The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51:6787–99
    [Google Scholar]
  86. Liang L, Fratzl A, Goldey G, 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]
  87. Lien AD, Scanziani M 2018. Cortical direction selectivity emerges at convergence of thalamic synapses. Nature 558:770880–86
    [Google Scholar]
  88. Lipin MY, Taylor WR, Smith RG 2015. Inhibitory input to the direction-selective ganglion cell is saturated at low contrast. J. Neurophysiol. 114:2927–41
    [Google Scholar]
  89. Litvina EY, Chen C 2017. Functional convergence at the retinogeniculate synapse. Neuron 96:2330–38.e5
    [Google Scholar]
  90. Manookin MB, Patterson SS, Linehan CM 2018. Neural mechanisms mediating motion sensitivity in parasol ganglion cells of the primate retina. Neuron 97:61327–40.e4
    [Google Scholar]
  91. Marques T, Summers MT, Fioreze G, Fridman M, Dias RF et al. 2018. A role for mouse primary visual cortex in motion perception. Curr. Biol. 28:111703–13.e6
    [Google Scholar]
  92. Marre O, Amodei D, Deshmukh N, Sadeghi K, Soo F et al. 2012. Mapping a complete neural population in the retina. J. Neurosci. 32:4314859–73
    [Google Scholar]
  93. 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]
  94. Masseck OA, Hoffmann K-P 2009. Comparative neurobiology of the optokinetic reflex. Ann. N. Y. Acad. Sci. 1164:1430–39
    [Google Scholar]
  95. Mauss AS, Vlasits A, Borst A, Feller M 2017. Visual circuits for direction selectivity. Annu. Rev. Neurosci. 40:211–30
    [Google Scholar]
  96. Miller RF, Bloomfield SA 1983. Electroanatomy of a unique amacrine cell in the rabbit retina. PNAS 80:103069–73
    [Google Scholar]
  97. 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]
  98. 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. 35:259281–86
    [Google Scholar]
  99. Morrie RD, Feller MB 2016. Development of synaptic connectivity in the retinal direction selective circuit. Curr. Opin. Neurobiol. 40:45–52
    [Google Scholar]
  100. Morrie RD, Feller MB 2018. A dense starburst plexus is critical for generating direction selectivity. Curr. Biol. 28:81204–12.e5
    [Google Scholar]
  101. 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]
  102. Münch TA, Werblin FS 2006. Symmetric interactions within a homogeneous starburst cell network can lead to robust asymmetries in dendrites of starburst amacrine cells. J. Neurophysiol. 96:1471–77
    [Google Scholar]
  103. Nath A, Schwartz GW 2017. Electrical synapses convey orientation selectivity in the mouse retina. Nat. Commun. 8:12025
    [Google Scholar]
  104. Nichols Z, Nirenberg S, Victor J 2013. Interacting linear and nonlinear characteristics produce population coding asymmetries between ON and OFF cells in the retina. J. Neurosci. 33:3714958–73
    [Google Scholar]
  105. Oesch N, Euler T, Taylor WR 2005. Direction-selective dendritic action potentials in rabbit retina. Neuron 47:5739–50
    [Google Scholar]
  106. Oesch NW, Taylor WR 2010. Tetrodotoxin-resistant sodium channels contribute to directional responses in starburst amacrine cells. PLOS ONE 5:8e12447
    [Google Scholar]
  107. Ölveczky BP, Baccus SA, Meister M 2003. Segregation of object and background motion in the retina. Nature 423:6938401–8
    [Google Scholar]
  108. Oyster CW 1968. The analysis of image motion by the rabbit retina. J. Physiol. 199:3613–35
    [Google Scholar]
  109. Ozaita A, Petit-Jacques J, Völgyi B, Ho CS, Joho RH et al. 2004. A unique role for Kv3 voltage-gated potassium channels in starburst amacrine cell signaling in mouse retina. J. Neurosci. 24:337335–43
    [Google Scholar]
  110. Park SJH, Borghuis BG, Rahmani P, Zeng Q, Kim I-J, Demb JB 2015. Function and circuitry of VIP+ interneurons in the mouse retina. J. Neurosci. 35:3010685–700
    [Google Scholar]
  111. Park SJH, Kim I-J, Looger LL, Demb JB, Borghuis BG 2014. Excitatory synaptic inputs to mouse on-off direction-selective retinal ganglion cells lack direction tuning. J. Neurosci. 34:113976–81
    [Google Scholar]
  112. Pearson JT, Kerschensteiner D 2015. Ambient illumination switches contrast preference of specific retinal processing streams. J. Neurophysiol. 114:1540–50
    [Google Scholar]
  113. Pei Z, Chen Q, Koren D, Giammarinaro B, Acaron Ledesma H, Wei W 2015. Conditional knock-out of vesicular GABA transporter gene from starburst amacrine cells reveals the contributions of multiple synaptic mechanisms underlying direction selectivity in the retina. J. Neurosci. 35:3813219–32
    [Google Scholar]
  114. Percival KA, Venkataramani S, Smith RG, Rowland Taylor W 2018. Directional excitatory input to direction-selective ganglion cells in the rabbit retina. J. Comp. Neurol. In press. https://doi.org/10.1002/cne.24207
    [Crossref] [Google Scholar]
  115. 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]
  116. Poleg-Polsky A, Diamond JS 2011. Imperfect space clamp permits electrotonic interactions between inhibitory and excitatory synaptic conductances, distorting voltage clamp recordings. PLOS ONE 6:4e19463
    [Google Scholar]
  117. Poleg-Polsky A, Diamond JS 2016.a NMDA receptors multiplicatively scale visual signals and enhance directional motion discrimination in retinal ganglion cells. Neuron 89:61277–90
    [Google Scholar]
  118. Poleg-Polsky A, Diamond JS 2016.b Retinal circuitry balances contrast tuning of excitation and inhibition to enable reliable computation of direction selectivity. J. Neurosci. 36:215861–76
    [Google Scholar]
  119. Poleg-Polsky A, Ding H, Diamond JS 2018. Functional compartmentalization within starburst amacrine cell dendrites in the retina. Cell Rep 22:112898–908
    [Google Scholar]
  120. Ratliff CP, Borghuis BG, Kao Y-H, Sterling P, Balasubramanian V 2010. Retina is structured to process an excess of darkness in natural scenes. PNAS 107:4017368–73
    [Google Scholar]
  121. Rekauzke S, Nortmann N, Staadt R, Hock HS, Schoner G, Jancke D 2016. Temporal asymmetry in dark-bright processing initiates propagating activity across primary visual cortex. J. Neurosci. 36:61902–13
    [Google Scholar]
  122. Rivlin-Etzion M, Wei W, Feller MBB 2012. Visual stimulation reverses the directional preference of direction-selective retinal ganglion cells. Neuron 76:3518–25
    [Google Scholar]
  123. 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]
  124. 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 93:61519
    [Google Scholar]
  125. Rosa JM, Morrie RD, Baertsch HC, Feller MB 2016. Contributions of rod and cone pathways to retinal direction selectivity through development. J. Neurosci. 36:379683–95
    [Google Scholar]
  126. Roska B, Werblin F 2003. Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nat. Neurosci. 6:6600–608
    [Google Scholar]
  127. 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]
  128. Sabbah S, Gemmer JA, Bhatia-Lin A, Manoff G, Castro G et al. 2017. A retinal code for motion along the gravitational and body axes. Nature 546:7659492–97
    [Google Scholar]
  129. 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]
  130. Schachter MJ, Oesch N, Smith RG, Taylor WR 2010. Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell. PLOS Comput. Biol. 6:8e1000899
    [Google Scholar]
  131. Schwartz G, Taylor S, Fisher C, Harris R, Berry MJ 2007. Synchronized firing among retinal ganglion cells signals motion reversal. Neuron 55:6958–69
    [Google Scholar]
  132. Sethuramanujam S, McLaughlin AJ, deRosenroll G, Hoggarth A, Schwab DJ, Awatramani GB 2016. A central role for mixed acetylcholine/GABA transmission in direction coding in the retina. Neuron 90:61243–56
    [Google Scholar]
  133. Sethuramanujam S, Yao X, deRosenroll G, Briggman KL, Field GD, Awatramani GB 2017. “Silent” NMDA synapses enhance motion sensitivity in a mature retinal circuit. Neuron 96:51099–111.e3
    [Google Scholar]
  134. Shi X, Barchini J, Ledesma HA, Koren D, Jin Y et al. 2017. Retinal origin of direction selectivity in the superior colliculus. Nat. Neurosci. 20:4550–58
    [Google Scholar]
  135. Simpson JI 1984. The accessory optic system. Annu. Rev. Neurosci. 7:13–41
    [Google Scholar]
  136. 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. 588:173243–53
    [Google Scholar]
  137. Sivyer B, Williams SR 2013. Direction selectivity is computed by active dendritic integration in retinal ganglion cells. Nat. Neurosci. 16:121848–56
    [Google Scholar]
  138. Stasheff SF, Masland RH 2002. Functional inhibition in direction-selective retinal ganglion cells: spatiotemporal extent and intralaminar interactions. J. Neurophysiol. 88:21026–39
    [Google Scholar]
  139. Stincic T, Smith RG, Taylor WR 2016. Time course of EPSCs in ON-type starburst amacrine cells is independent of dendritic location. J. Physiol. 594:195685–94
    [Google Scholar]
  140. 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 86:4971–84
    [Google Scholar]
  141. 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 342:61581241974
    [Google Scholar]
  142. Sun W, Deng Q, Levick WR, He S 2006. ON direction-selective ganglion cells in the mouse retina. J. Physiol. 576:1197–202
    [Google Scholar]
  143. Taylor WR, Vaney DI 2002. Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. J. Neurosci. 22:177712–20
    [Google Scholar]
  144. Tikidji-Hamburyan A, Reinhard K, Seitter H, Hovhannisyan A, Procyk CA et al. 2014. Retinal output changes qualitatively with every change in ambient illuminance. Nat. Neurosci. 18:166–74
    [Google Scholar]
  145. Trenholm S, Johnson K, Li X, Smith RG, Awatramani GB 2011. Parallel mechanisms encode direction in the retina. Neuron 71:4683–94
    [Google Scholar]
  146. Trenholm S, McLaughlin AJ, Schwab DJ, Turner MH, Smith RG et al. 2014. Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations. Nat. Neurosci. 17:121759–66
    [Google Scholar]
  147. Tukker JJ, Taylor WR, Smith RG 2004. Direction selectivity in a model of the starburst amacrine cell. Vis. Neurosci. 21:4611–25
    [Google Scholar]
  148. Turner MH, Rieke F 2016. Synaptic rectification controls nonlinear spatial integration of natural visual inputs. Neuron 90:61257–71
    [Google Scholar]
  149. 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]
  150. Vaney DI, Young HM 1988. GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res 438:1–2369–73
    [Google Scholar]
  151. Vlasits AL, Bos R, Morrie RD, Fortuny C, Flannery JG et al. 2014. Visual stimulation switches the polarity of excitatory input to starburst amacrine cells. Neuron 83:51172–84
    [Google Scholar]
  152. 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 89:61317–30
    [Google Scholar]
  153. Wei W, Hamby AM, Zhou K, Feller MB 2011. Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469:7330402–6
    [Google Scholar]
  154. Weng S, Sun W, He S 2005. Identification of ON-OFF direction-selective ganglion cells in the mouse retina. J. Physiol. 562:3915–23
    [Google Scholar]
  155. Wyatt HJ, Daw NW 1975. Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed. J. Neurophysiol. 38:3613–26
    [Google Scholar]
  156. Yang G, Masland RH 1992. Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258:50901949–52
    [Google Scholar]
  157. Yang G, Masland RH 1994. Receptive fields and dendritic structure of directionally selective retinal ganglion cells. J. Neurosci. 14:95267–80
    [Google Scholar]
  158. Yonehara K, Balint K, Noda M, Nagel G, Bamberg E, Roska B 2011. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469:7330407–10
    [Google Scholar]
  159. 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]
  160. 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 89:1177–93
    [Google Scholar]
  161. 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]
  162. 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]
  163. 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]
  164. Zaghloul KA, Boahen K, Demb JB 2003. Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J. Neurosci. 23:72645–54
    [Google Scholar]
  165. Zhang Y, Kim I-J, Sanes JR, Meister M, Vitaladevuni S et al. 2012. The most numerous ganglion cell type of the mouse retina is a selective feature detector. PNAS 109:36E2391–98
    [Google Scholar]
  166. Zylberberg J, Cafaro J, Turner MH, Shea-Brown E, Rieke F 2016. Direction-selective circuits shape noise to ensure a precise population code. Neuron 89:2369–83
    [Google Scholar]
/content/journals/10.1146/annurev-vision-091517-034048
Loading
/content/journals/10.1146/annurev-vision-091517-034048
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