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Abstract

Visual stimuli can evoke complex behavioral responses, but the underlying streams of neural activity in mammalian brains are difficult to follow because of their size. Here, I review the visual system of zebrafish larvae, highlighting where recent experimental evidence has localized the functional steps of visuomotor transformations to specific brain areas. The retina of a larva encodes behaviorally relevant visual information in neural activity distributed across feature-selective ganglion cells such that signals representing distinct stimulus properties arrive in different areas or layers of the brain. Motor centers in the hindbrain encode motor variables that are precisely tuned to behavioral needs within a given stimulus setting. Owing to rapid technological progress, larval zebrafish provide unique opportunities for obtaining a comprehensive understanding of the intermediate processing steps occurring between visual and motor centers, revealing how visuomotor transformations are implemented in a vertebrate brain.

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2019-09-15
2024-04-26
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Literature Cited

  1. Abbas F, Triplett MA, Goodhill GJ, Meyer MP 2017. A three-layer network model of direction selective circuits in the optic tectum. Front. Neural Circuits 11:88
    [Google Scholar]
  2. Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF et al. 2012. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485:471–77
    [Google Scholar]
  3. Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ 2013. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10:413–20
    [Google Scholar]
  4. Aizenberg M, Schuman EM. 2011. Cerebellar-dependent learning in larval zebrafish. J. Neurosci. 31:8708–12
    [Google Scholar]
  5. Allison WT, Barthel LK, Skebo KM, Takechi M, Kawamura S, Raymond PA 2010. Ontogeny of cone photoreceptor mosaics in zebrafish. J. Comp. Neurol. 518:4182–95
    [Google Scholar]
  6. Antinucci P, Nikolaou N, Meyer MP, Hindges R 2013. Teneurin-3 specifies morphological and functional connectivity of retinal ganglion cells in the vertebrate visual system. Cell Rep 5:582–92
    [Google Scholar]
  7. Antinucci P, Suleyman O, Monfries C, Hindges R 2016. Neural mechanisms generating orientation selectivity in the retina. Curr. Biol. 26:1802–15
    [Google Scholar]
  8. Avitan L, Pujic Z, Hughes NJ, Scott EK, Goodhill GJ 2016. Limitations of neural map topography for decoding spatial information. J. Neurosci. 36:5385–96
    [Google Scholar]
  9. Avitan L, Pujic Z, Molter J, Van De Poll M, Sun B et al. 2017. Spontaneous activity in the zebrafish tectum reorganizes over development and is influenced by visual experience. Curr. Biol. 27:2407–19.e4
    [Google Scholar]
  10. Baden T, Esposti F, Nikolaev A, Lagnado L 2011. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr. Biol. 21:1859–69
    [Google Scholar]
  11. Baden T, Nikolaev A, Esposti F, Dreosti E, Odermatt B, Lagnado L 2014. A synaptic mechanism for temporal filtering of visual signals. PLOS Biol 12:e1001972
    [Google Scholar]
  12. Bagnall MW, McLean DL. 2014. Modular organization of axial microcircuits in zebrafish. Science 343:197–200
    [Google Scholar]
  13. 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]
  14. Barker AJ, Baier H. 2015. Sensorimotor decision making in the zebrafish tectum. Curr. Biol. 25:2804–14
    [Google Scholar]
  15. Berg EM, Bjornfors ER, Pallucchi I, Picton LD, El Manira A 2018. Principles governing locomotion in vertebrates: lessons from zebrafish. Front. Neural Circuits 12:73
    [Google Scholar]
  16. Bergmann K, Meza Santoscoy P, Lygdas K, Nikolaeva Y, MacDonald RB et al. 2018. Imaging neuronal activity in the optic tectum of late stage larval zebrafish. J. Dev. Biol. 6:6
    [Google Scholar]
  17. Bhattacharyya K, McLean DL, MacIver MA 2017. Visual threat assessment and reticulospinal encoding of calibrated responses in larval zebrafish. Curr. Biol. 27:2751–62.e6
    [Google Scholar]
  18. Bianco IH, Engert F. 2015. Visuomotor transformations underlying hunting behavior in zebrafish. Curr. Biol. 25:831–46
    [Google Scholar]
  19. Bianco IH, Kampff AR, Engert F 2011. Prey capture behavior evoked by simple visual stimuli in larval zebrafish. Front. Syst. Neurosci. 5:101
    [Google Scholar]
  20. Bilotta J, Saszik S. 2001. The zebrafish as a model visual system. Int. J. Dev. Neurosci. 19:621–29
    [Google Scholar]
  21. Boulanger-Weill J, Candat V, Jouary A, Romano SA, Perez-Schuster V, Sumbre G 2017. Functional interactions between newborn and mature neurons leading to integration into established neuronal circuits. Curr. Biol. 27:1707–20.e5
    [Google Scholar]
  22. Briggman KL, Helmstaedter M, Denk W 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–88
    [Google Scholar]
  23. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE 1995. A behavioral screen for isolating zebrafish mutants with visual system defects. PNAS 92:10545–49
    [Google Scholar]
  24. Burgess HA, Schoch H, Granato M 2010. Distinct retinal pathways drive spatial orientation behaviors in zebrafish navigation. Curr. Biol. 20:381–86
    [Google Scholar]
  25. Burrill JD, Easter SS Jr 1994. Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). J. Comp. Neurol. 346:583–600
    [Google Scholar]
  26. Cang J, Savier E, Barchini J, Liu X 2018. Visual function, organization, and development of the mouse superior colliculus. Annu. Rev. Vis. Sci. 4:239–62
    [Google Scholar]
  27. Carr JA. 2015. I'll take the low road: the evolutionary underpinnings of visually triggered fear. Front. Neurosci. 9:414
    [Google Scholar]
  28. Chen X, Engert F. 2014. Navigational strategies underlying phototaxis in larval zebrafish. Front. Syst. Neurosci. 8:39
    [Google Scholar]
  29. Chen X, Mu Y, Hu Y, Kuan AT, Nikitchenko M et al. 2018. Brain-wide organization of neuronal activity and convergent sensorimotor transformations in larval zebrafish. Neuron 100:876–90.e5
    [Google Scholar]
  30. Cheng RK, Krishnan S, Lin Q, Kibat C, Jesuthasan S 2017. Characterization of a thalamic nucleus mediating habenula responses to changes in ambient illumination. BMC Biol 15:104
    [Google Scholar]
  31. Chinen A, Hamaoka T, Yamada Y, Kawamura S 2003. Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163:663–75
    [Google Scholar]
  32. Cong L, Wang Z, Chai Y, Hang W, Shang C et al. 2017. Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (Danio rerio). eLife 6:e28158
    [Google Scholar]
  33. Connaughton VP, Graham D, Nelson R 2004. Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. J. Comp. Neurol. 477:371–85
    [Google Scholar]
  34. Connaughton VP, Nelson R. 2010. Spectral responses in zebrafish horizontal cells include a tetraphasic response and a novel UV-dominated triphasic response. J. Neurophysiol. 104:2407–22
    [Google Scholar]
  35. Daie K, Goldman MS, Aksay ER 2015. Spatial patterns of persistent neural activity vary with the behavioral context of short-term memory. Neuron 85:847–60
    [Google Scholar]
  36. Dal Maschio M, Donovan JC, Helmbrecht TO, Baier H 2017. Linking neurons to network function and behavior by two-photon holographic optogenetics and volumetric imaging. Neuron 94:774–89.e5
    [Google Scholar]
  37. Del Bene F, Wyart C, Robles E, Tran A, Looger L et al. 2010. Filtering of visual information in the tectum by an identified neural circuit. Science 330:669–73
    [Google Scholar]
  38. Demb JB, Singer JH. 2015. Functional circuitry of the retina. Annu. Rev. Vis. Sci. 1:263–89
    [Google Scholar]
  39. Dhande OS, Huberman AD. 2014. Retinal ganglion cell maps in the brain: implications for visual processing. Curr. Opin. Neurobiol. 24:133–42
    [Google Scholar]
  40. Diamond JS. 2017. Inhibitory interneurons in the retina: types, circuitry, and function. Annu. Rev. Vis. Sci. 3:1–24
    [Google Scholar]
  41. Dill LM. 1974. The escape response of the zebra danio (Brachydanio rerio) I. The stimulus for escape. Anim. Behav. 22:711–22
    [Google Scholar]
  42. Dreosti E, Esposti F, Baden T, Lagnado L 2011. In vivo evidence that retinal bipolar cells generate spikes modulated by light. Nat. Neurosci. 14:951–52
    [Google Scholar]
  43. Dreosti E, Lopes G, Kampff AR, Wilson SW 2015. Development of social behavior in young zebrafish. Front. Neural Circuits 9:39
    [Google Scholar]
  44. Dreosti E, Vendrell Llopis N, Carl M, Yaksi E, Wilson SW 2014. Left-right asymmetry is required for the habenulae to respond to both visual and olfactory stimuli. Curr. Biol. 24:440–45
    [Google Scholar]
  45. Dunn TW, Gebhardt C, Naumann EA, Riegler C, Ahrens MB et al. 2016a. Neural circuits underlying visually evoked escapes in larval zebrafish. Neuron 89:613–28
    [Google Scholar]
  46. Dunn TW, Mu Y, Narayan S, Randlett O, Naumann EA et al. 2016b. Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion. eLife 5:e12741
    [Google Scholar]
  47. Easter SS Jr., Nicola GN. 1996. The development of vision in the zebrafish (Danio rerio). Dev. Biol. 180:646–63
    [Google Scholar]
  48. Emran F, Rihel J, Adolph AR, Wong KY, Kraves S, Dowling JE 2007. OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. PNAS 104:19126–31
    [Google Scholar]
  49. Esposti F, Johnston J, Rosa JM, Leung KM, Lagnado L 2013. Olfactory stimulation selectively modulates the OFF pathway in the retina of zebrafish. Neuron 79:97–110
    [Google Scholar]
  50. Euler T, Detwiler PB, Denk W 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418:845–52
    [Google Scholar]
  51. Euler T, Haverkamp S, Schubert T, Baden T 2014. Retinal bipolar cells: elementary building blocks of vision. Nat. Rev. Neurosci. 15:507–19
    [Google Scholar]
  52. Fajardo O, Zhu P, Friedrich RW 2013. Control of a specific motor program by a small brain area in zebrafish. Front. Neural Circuits 7:67
    [Google Scholar]
  53. Fernandes AM, Fero K, Arrenberg AB, Bergeron SA, Driever W, Burgess HA 2012. Deep brain photoreceptors control light-seeking behavior in zebrafish larvae. Curr. Biol. 22:2042–47
    [Google Scholar]
  54. Filosa A, Barker AJ, Dal Maschio M, Baier H 2016. Feeding state modulates behavioral choice and processing of prey stimuli in the zebrafish tectum. Neuron 90:596–608
    [Google Scholar]
  55. Franke K, Baden T. 2017. General features of inhibition in the inner retina. J. Physiol. 595:5507–15
    [Google Scholar]
  56. Friedrich RW, Jacobson GA, Zhu P 2010. Circuit neuroscience in zebrafish. Curr. Biol. 20:R371–81
    [Google Scholar]
  57. Gabriel JP, Trivedi CA, Maurer CM, Ryu S, Bollmann JH 2012. Layer-specific targeting of direction-selective neurons in the zebrafish optic tectum. Neuron 76:1147–60
    [Google Scholar]
  58. Gahtan E, Baier H. 2004. Of lasers, mutants, and see-through brains: functional neuroanatomy in zebrafish. J. Neurobiol. 59:147–61
    [Google Scholar]
  59. Gahtan E, O'Malley DM. 2003. Visually guided injection of identified reticulospinal neurons in zebrafish: a survey of spinal arborization patterns. J. Comp. Neurol. 459:186–200
    [Google Scholar]
  60. Gahtan E, Sankrithi N, Campos JB, O'Malley DM 2002. Evidence for a widespread brain stem escape network in larval zebrafish. J. Neurophysiol. 87:608–14
    [Google Scholar]
  61. Gahtan E, Tanger P, Baier H 2005. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. J. Neurosci. 25:9294–303
    [Google Scholar]
  62. Gandhi NJ, Katnani HA. 2011. Motor functions of the superior colliculus. Annu. Rev. Neurosci. 34:205–31
    [Google Scholar]
  63. Godinho L, Mumm JS, Williams PR, Schroeter EH, Koerber A et al. 2005. Targeting of amacrine cell neurites to appropriate synaptic laminae in the developing zebrafish retina. Development 132:5069–79
    [Google Scholar]
  64. Grama A, Engert F. 2012. Direction selectivity in the larval zebrafish tectum is mediated by asymmetric inhibition. Front. Neural Circuits 6:59
    [Google Scholar]
  65. Hale ME, Ritter DA, Fetcho JR 2001. A confocal study of spinal interneurons in living larval zebrafish. J. Comp. Neurol. 437:1–16
    [Google Scholar]
  66. Heap LA, Goh CC, Kassahn KS, Scott EK 2013. Cerebellar output in zebrafish: an analysis of spatial patterns and topography in eurydendroid cell projections. Front. Neural Circuits 7:53
    [Google Scholar]
  67. Heap LAL, Vanwalleghem G, Thompson AW, Favre-Bulle IA, Scott EK 2018. Luminance changes drive directional startle through a thalamic pathway. Neuron 99:293–301.e4
    [Google Scholar]
  68. Helmbrecht TO, Dal Maschio M, Donovan JC, Koutsouli S, Baier H 2018. Topography of a visuomotor transformation. Neuron 100:1429–45.e4
    [Google Scholar]
  69. Higashijima S, Schaefer M, Fetcho JR 2004. Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish. J. Comp. Neurol. 480:19–37
    [Google Scholar]
  70. Hinz FI, Aizenberg M, Tushev G, Schuman EM 2013. Protein synthesis-dependent associative long-term memory in larval zebrafish. J. Neurosci. 33:15382–87
    [Google Scholar]
  71. Hinz RC, de Polavieja GG 2017. Ontogeny of collective behavior reveals a simple attraction rule. PNAS 114:2295–300
    [Google Scholar]
  72. Horstick EJ, Bayleyen Y, Sinclair JL, Burgess HA 2017. Search strategy is regulated by somatostatin signaling and deep brain photoreceptors in zebrafish. BMC Biol 15:4
    [Google Scholar]
  73. Huang KH, Ahrens MB, Dunn TW, Engert F 2013. Spinal projection neurons control turning behaviors in zebrafish. Curr. Biol. 23:1566–73
    [Google Scholar]
  74. Hunter PR, Lowe AS, Thompson ID, Meyer MP 2013. Emergent properties of the optic tectum revealed by population analysis of direction and orientation selectivity. J. Neurosci. 33:13940–45
    [Google Scholar]
  75. Joshua M, Lisberger SG. 2015. A tale of two species: neural integration in zebrafish and monkeys. Neuroscience 296:80–91
    [Google Scholar]
  76. Jusuf PR, Harris WA. 2009. Ptf1a is expressed transiently in all types of amacrine cells in the embryonic zebrafish retina. Neural Dev 4:34
    [Google Scholar]
  77. Kawashima T, Zwart MF, Yang CT, Mensh BD, Ahrens MB 2016. The serotonergic system tracks the outcomes of actions to mediate short-term motor learning. Cell 167:933–46.e20
    [Google Scholar]
  78. Kim DH, Kim J, Marques JC, Grama A, Hildebrand DGC et al. 2017. Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish. Nat. Methods 14:1107–14
    [Google Scholar]
  79. Kimmel CB, Powell SL, Metcalfe WK 1982. Brain neurons which project to the spinal cord in young larvae of the zebrafish. J. Comp. Neurol. 205:112–27
    [Google Scholar]
  80. Kinkhabwala A, Riley M, Koyama M, Monen J, Satou C et al. 2011. A structural and functional ground plan for neurons in the hindbrain of zebrafish. PNAS 108:1164–69
    [Google Scholar]
  81. Kita EM, Scott EK, Goodhill GJ 2015. Topographic wiring of the retinotectal connection in zebrafish. Dev. Neurobiol. 75:542–56
    [Google Scholar]
  82. Knogler LD, Markov DA, Dragomir EI, Stih V, Portugues R 2017. Sensorimotor representations in cerebellar granule cells in larval zebrafish are dense, spatially organized, and non-temporally patterned. Curr. Biol. 27:1288–302
    [Google Scholar]
  83. Kohashi T, Oda Y. 2008. Initiation of Mauthner- or non-Mauthner-mediated fast escape evoked by different modes of sensory input. J. Neurosci. 28:10641–53
    [Google Scholar]
  84. Koyama M, Kinkhabwala A, Satou C, Higashijima S, Fetcho J 2011. Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. PNAS 108:1170–75
    [Google Scholar]
  85. Koyama M, Minale F, Shum J, Nishimura N, Schaffer CB, Fetcho JR 2016. A circuit motif in the zebrafish hindbrain for a two alternative behavioral choice to turn left or right. eLife 5:e16808
    [Google Scholar]
  86. Krauzlis RJ, Bogadhi AR, Herman JP, Bollimunta A 2018. Selective attention without a neocortex. Cortex 102:161–75
    [Google Scholar]
  87. Kubo F, Hablitzel B, Dal Maschio M, Driever W, Baier H, Arrenberg AB 2014. Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish. Neuron 81:1344–59
    [Google Scholar]
  88. Kunst M, Laurell E, Mokayes N, Kramer A, Kubo F, et al. 2019. A cellular-resolution atlas of the larval zebrafish brain. Neuron 103:21–38.e5
    [Google Scholar]
  89. Lacoste AM, Schoppik D, Robson DN, Haesemeyer M, Portugues R et al. 2015. A convergent and essential interneuron pathway for Mauthner-cell-mediated escapes. Curr. Biol. 25:1526–34
    [Google Scholar]
  90. Larsch J, Baier H. 2018. Biological motion as an innate perceptual mechanism driving social affiliation. Curr. Biol. 28:3523–32.e4
    [Google Scholar]
  91. Lee MM, Arrenberg AB, Aksay ER 2015. A structural and genotypic scaffold underlying temporal integration. J. Neurosci. 35:7903–20
    [Google Scholar]
  92. Liu KS, Fetcho JR 1999. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 23:325–35
    [Google Scholar]
  93. Lovett-Barron M, Andalman AS, Allen WE, Vesuna S, Kauvar I et al. 2017. Ancestral circuits for the coordinated modulation of brain state. Cell 171:1411–23.e17
    [Google Scholar]
  94. Lowe AS, Nikolaou N, Hunter PR, Thompson ID, Meyer MP 2013. A systems-based dissection of retinal inputs to the zebrafish tectum reveals different rules for different functional classes during development. J. Neurosci. 33:13946–56
    [Google Scholar]
  95. Marquart GD, Tabor KM, Brown M, Strykowski JL, Varshney GK et al. 2015. A 3D searchable database of transgenic zebrafish Gal4 and Cre lines for functional neuroanatomy studies. Front. Neural Circuits 9:78
    [Google Scholar]
  96. Marques JC, Lackner S, Felix R, Orger MB 2018. Structure of the zebrafish locomotor repertoire revealed with unsupervised behavioral clustering. Curr. Biol. 28:181–95.e5
    [Google Scholar]
  97. Masland RH. 2001. The fundamental plan of the retina. Nat. Neurosci. 4:877–86
    [Google Scholar]
  98. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:266–80
    [Google Scholar]
  99. Masseck OA, Hoffmann KP. 2009. Comparative neurobiology of the optokinetic reflex. Ann. N.Y. Acad. Sci. 1164:430–39
    [Google Scholar]
  100. Matsuda K, Yoshida M, Kawakami K, Hibi M, Shimizu T 2017. Granule cells control recovery from classical conditioned fear responses in the zebrafish cerebellum. Sci. Rep. 7:11865
    [Google Scholar]
  101. Matsui H, Namikawa K, Babaryka A, Koster RW 2014. Functional regionalization of the teleost cerebellum analyzed in vivo. PNAS 111:11846–51
    [Google Scholar]
  102. Mauss AS, Vlasits A, Borst A, Feller M 2017. Visual circuits for direction selectivity. Annu. Rev. Neurosci. 40:211–30
    [Google Scholar]
  103. McElligott MB, O'Malley DM. 2005. Prey tracking by larval zebrafish: axial kinematics and visual control. Brain Behav. Evol. 66:177–96
    [Google Scholar]
  104. McLean DL, Fan J, Higashijima S, Hale ME, Fetcho JR 2007. A topographic map of recruitment in spinal cord. Nature 446:71–75
    [Google Scholar]
  105. McLean DL, Fetcho JR. 2004. Relationship of tyrosine hydroxylase and serotonin immunoreactivity to sensorimotor circuitry in larval zebrafish. J. Comp. Neurol. 480:57–71
    [Google Scholar]
  106. McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR 2008. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat. Neurosci 11:1419–29
    [Google Scholar]
  107. Metcalfe WK, Mendelson B, Kimmel CB 1986. Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J. Comp. Neurol. 251:147–59
    [Google Scholar]
  108. Miri A, Daie K, Arrenberg AB, Baier H, Aksay E, Tank DW 2011a. Spatial gradients and multidimensional dynamics in a neural integrator circuit. Nat. Neurosci. 14:1150–59
    [Google Scholar]
  109. Miri A, Daie K, Burdine RD, Aksay E, Tank DW 2011b. Regression-based identification of behavior-encoding neurons during large-scale optical imaging of neural activity at cellular resolution. J. Neurophysiol. 105:964–80
    [Google Scholar]
  110. Mumm JS, Williams PR, Godinho L, Koerber A, Pittman AJ et al. 2006. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52:609–21
    [Google Scholar]
  111. Munch 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. 12:1308–16
    [Google Scholar]
  112. Muto A, Lal P, Ailani D, Abe G, Itoh M, Kawakami K 2017. Activation of the hypothalamic feeding centre upon visual prey detection. Nat. Commun. 8:15029
    [Google Scholar]
  113. Muto A, Ohkura M, Abe G, Nakai J, Kawakami K 2013. Real-time visualization of neuronal activity during perception. Curr. Biol. 23:307–11
    [Google Scholar]
  114. Nair A, Changsing K, Stewart WJ, McHenry MJ 2017. Fish prey change strategy with the direction of a threat. Proc. R. Soc. B 284: 2017.0393
    [Google Scholar]
  115. Naumann EA, Fitzgerald JE, Dunn TW, Rihel J, Sompolinsky H, Engert F 2016. From whole-brain data to functional circuit models: the zebrafish optomotor response. Cell 167:947–60.e20
    [Google Scholar]
  116. Neuhauss SC. 2003. Behavioral genetic approaches to visual system development and function in zebrafish. J. Neurobiol. 54:148–60
    [Google Scholar]
  117. Neuhauss SC, Biehlmaier O, Seeliger MW, Das T, Kohler K et al. 1999. Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J. Neurosci. 19:8603–15
    [Google Scholar]
  118. Niell CM, Smith SJ. 2005. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45:941–51
    [Google Scholar]
  119. Nikolaev A, Leung KM, Odermatt B, Lagnado L 2013. Synaptic mechanisms of adaptation and sensitization in the retina. Nat. Neurosci. 16:934–41
    [Google Scholar]
  120. Nikolaou N, Lowe AS, Walker AS, Abbas F, Hunter PR et al. 2012. Parametric functional maps of visual inputs to the tectum. Neuron 76:317–24
    [Google Scholar]
  121. Nikolaou N, Meyer MP. 2015. Lamination speeds the functional development of visual circuits. Neuron 88:999–1013
    [Google Scholar]
  122. Odermatt B, Nikolaev A, Lagnado L 2012. Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 73:758–73
    [Google Scholar]
  123. O'Malley DM, Kao YH, Fetcho JR 1996. Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron 17:1145–55
    [Google Scholar]
  124. Orger MB, Baier H. 2005. Channeling of red and green cone inputs to the zebrafish optomotor response. Vis. Neurosci. 22:275–81
    [Google Scholar]
  125. Orger MB, Kampff AR, Severi KE, Bollmann JH, Engert F 2008. Control of visually guided behavior by distinct populations of spinal projection neurons. Nat. Neurosci. 11:327–33
    [Google Scholar]
  126. Patterson BW, Abraham AO, MacIver MA, McLean DL 2013. Visually guided gradation of prey capture movements in larval zebrafish. J. Exp. Biol. 216:3071–83
    [Google Scholar]
  127. Perez-Schuster V, Kulkarni A, Nouvian M, Romano SA, Lygdas K et al. 2016. Sustained rhythmic brain activity underlies visual motion perception in zebrafish. Cell Rep 17:1098–112
    [Google Scholar]
  128. Pietri T, Romano SA, Perez-Schuster V, Boulanger-Weill J, Candat V, Sumbre G 2017. The emergence of the spatial structure of tectal spontaneous activity is independent of visual inputs. Cell Rep 19:939–48
    [Google Scholar]
  129. Portugues R, Engert F. 2011. Adaptive locomotor behavior in larval zebrafish. Front. Syst. Neurosci. 5:72
    [Google Scholar]
  130. Portugues R, Feierstein CE, Engert F, Orger MB 2014. Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior. Neuron 81:1328–43
    [Google Scholar]
  131. Preuss SJ, Trivedi CA, vom Berg-Maurer CM, Ryu S, Bollmann JH 2014. Classification of object size in retinotectal microcircuits. Curr. Biol. 24:2376–85
    [Google Scholar]
  132. Randlett O, Wee CL, Naumann EA, Nnaemeka O, Schoppik D et al. 2015. Whole-brain activity mapping onto a zebrafish brain atlas. Nat. Methods 12:1039–46
    [Google Scholar]
  133. Reinig S, Driever W, Arrenberg AB 2017. The descending diencephalic dopamine system is tuned to sensory stimuli. Curr. Biol. 27:318–33
    [Google Scholar]
  134. Roberts AC, Bill BR, Glanzman DL 2013. Learning and memory in zebrafish larvae. Front. Neural Circuits 7:126
    [Google Scholar]
  135. Robinson J, Schmitt EA, Harosi FI, Reece RJ, Dowling JE 1993. Zebrafish ultraviolet visual pigment: absorption spectrum, sequence, and localization. PNAS 90:6009–12
    [Google Scholar]
  136. 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]
  137. Romano SA, Pietri T, Perez-Schuster V, Jouary A, Haudrechy M, Sumbre G 2015. Spontaneous neuronal network dynamics reveal circuit's functional adaptations for behavior. Neuron 85:1070–85
    [Google Scholar]
  138. Ronneberger O, Liu K, Rath M, Ruebeta D, Mueller T et al. 2012. ViBE-Z: a framework for 3D virtual colocalization analysis in zebrafish larval brains. Nat. Methods 9:735–42
    [Google Scholar]
  139. Rosa JM, Ruehle S, Ding H, Lagnado L 2016. Crossover inhibition generates sustained visual responses in the inner retina. Neuron 90:308–19
    [Google Scholar]
  140. Roska B, Meister M. 2014. The retina dissects the visual scene into distinct features. The New Visual Neurosciences JS Werner, LM Chalupa 163–82 Cambridge, MA: MIT Press
    [Google Scholar]
  141. 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]
  142. Sato T, Hamaoka T, Aizawa H, Hosoya T, Okamoto H 2007. Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish. J. Neurosci. 27:5271–79
    [Google Scholar]
  143. Scalise K, Shimizu T, Hibi M, Sawtell NB 2016. Responses of cerebellar Purkinje cells during fictive optomotor behavior in larval zebrafish. J. Neurophysiol. 116:2067–80
    [Google Scholar]
  144. Schmitt EA, Dowling JE. 1999. Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J. Comp. Neurol. 404:515–36
    [Google Scholar]
  145. Schroeter EH, Wong RO, Gregg RG 2006. In vivo development of retinal ON-bipolar cell axonal terminals visualized in nyx::MYFP transgenic zebrafish. Vis. Neurosci. 23:833–43
    [Google Scholar]
  146. Schulze L, Henninger J, Kadobianskyi M, Chaigne T, Faustino AI et al. 2018. Transparent Danionella translucida as a genetically tractable vertebrate brain model. Nat. Methods 15:977–83
    [Google Scholar]
  147. Semmelhack JL, Donovan JC, Thiele TR, Kuehn E, Laurell E, Baier H 2014. A dedicated visual pathway for prey detection in larval zebrafish. eLife 3:e04878
    [Google Scholar]
  148. Severi KE, Portugues R, Marques JC, O'Malley DM, Orger MB, Engert F 2014. Neural control and modulation of swimming speed in the larval zebrafish. Neuron 83:692–707
    [Google Scholar]
  149. Song PI, Matsui JI, Dowling JE 2008. Morphological types and connectivity of horizontal cells found in the adult zebrafish (Danio rerio) retina. J. Comp. Neurol. 506:328–38
    [Google Scholar]
  150. Stowers JR, Hofbauer M, Bastien R, Griessner J, Higgins P et al. 2017. Virtual reality for freely moving animals. Nat. Methods 14:995–1002
    [Google Scholar]
  151. Stuermer CA. 1988. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J. Neurosci. 8:4513–30
    [Google Scholar]
  152. Svara FN, Kornfeld J, Denk W, Bollmann JH 2018. Volume EM reconstruction of spinal cord reveals wiring specificity in speed-related motor circuits. Cell Rep 23:2942–54
    [Google Scholar]
  153. Sylvester SJG, Lee MM, Ramirez AD, Lim S, Goldman MS, Aksay ERF 2017. Population-scale organization of cerebellar granule neuron signaling during a visuomotor behavior. Sci. Rep. 7:16240
    [Google Scholar]
  154. Symvoulidis P, Lauri A, Stefanoiu A, Cappetta M, Schneider S et al. 2017. NeuBtracker—imaging neurobehavioral dynamics in freely behaving fish. Nat. Methods 14:1079
    [Google Scholar]
  155. Tabor KM, Marquart GD, Hurt C, Smith TS, Geoca AK et al. 2019. Brain-wide cellular resolution imaging of Cre transgenic zebrafish lines for functional circuit-mapping. eLife 8:e42687
    [Google Scholar]
  156. Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W 2011. Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. Nat. Commun. 2:171
    [Google Scholar]
  157. Temizer I, Donovan JC, Baier H, Semmelhack JL 2015. A visual pathway for looming-evoked escape in larval zebrafish. Curr. Biol. 25:1823–34
    [Google Scholar]
  158. Thiele TR, Donovan JC, Baier H 2014. Descending control of swim posture by a midbrain nucleus in zebrafish. Neuron 83:679–91
    [Google Scholar]
  159. Thompson AW, Vanwalleghem GC, Heap LA, Scott EK 2016. Functional profiles of visual-, auditory-, and water flow-responsive neurons in the zebrafish tectum. Curr. Biol. 26:743–54
    [Google Scholar]
  160. Torvund MM, Ma TS, Connaughton VP, Ono F, Nelson RF 2017. Cone signals in monostratified and bistratified amacrine cells of adult zebrafish retina. J. Comp. Neurol. 525:1532–57
    [Google Scholar]
  161. Trivedi CA, Bollmann JH. 2013. Visually driven chaining of elementary swim patterns into a goal-directed motor sequence: a virtual reality study of zebrafish prey capture. Front. Neural Circuits 7:86
    [Google Scholar]
  162. Valente A, Huang KH, Portugues R, Engert F 2012. Ontogeny of classical and operant learning behaviors in zebrafish. Learn. Mem. 19:170–77
    [Google Scholar]
  163. Vendrell-Llopis N, Yaksi E. 2015. Evolutionary conserved brainstem circuits encode category, concentration and mixtures of taste. Sci. Rep. 5:17825
    [Google Scholar]
  164. Vishwanathan A, Daie K, Ramirez AD, Lichtman JW, Aksay ERF, Seung HS 2017. Electron microscopic reconstruction of functionally identified cells in a neural integrator. Curr. Biol. 27:2137–47.e3
    [Google Scholar]
  165. Wang K, Hinz J, Haikala V, Reiff DF, Arrenberg AB 2019. Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum. BMC Biol 17:29
    [Google Scholar]
  166. Wang WC, McLean DL. 2014. Selective responses to tonic descending commands by temporal summation in a spinal motor pool. Neuron 83:708–21
    [Google Scholar]
  167. Wassle H. 2004. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5:747–57
    [Google Scholar]
  168. Wolf S, Dubreuil AM, Bertoni T, Bohm UL, Bormuth V et al. 2017. Sensorimotor computation underlying phototaxis in zebrafish. Nat. Commun. 8:651
    [Google Scholar]
  169. Yao Y, Li X, Zhang B, Yin C, Liu Y et al. 2016. Visual cue-discriminative dopaminergic control of visuomotor transformation and behavior selection. Neuron 89:598–612
    [Google Scholar]
  170. Yin C, Li X, Du J 2019. Optic tectal superficial interneurons detect motion in larval zebrafish. Protein Cell 10:238–48
    [Google Scholar]
  171. Yokogawa T, Hannan MC, Burgess HA 2012. The dorsal raphe modulates sensory responsiveness during arousal in zebrafish. J. Neurosci. 32:15205–15
    [Google Scholar]
  172. Yoshimatsu T, Williams PR, D'Orazi FD, Suzuki SC, Fadool JM et al. 2014. Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells. Nat. Commun. 5:3699
    [Google Scholar]
  173. Zhang BB, Yao YY, Zhang HF, Kawakami K, Du JL 2017. Left habenula mediates light-preference behavior in zebrafish via an asymmetrical visual pathway. Neuron 93:914–28.e4
    [Google Scholar]
  174. Zhang RW, Li XQ, Kawakami K, Du JL 2016. Stereotyped initiation of retinal waves by bipolar cells via presynaptic NMDA autoreceptors. Nat. Commun. 7:12650
    [Google Scholar]
  175. Zhang RW, Wei HP, Xia YM, Du JL 2010. Development of light response and GABAergic excitation-to-inhibition switch in zebrafish retinal ganglion cells. J. Physiol. 588:2557–69
    [Google Scholar]
  176. Zimmermann MJY, Nevala NE, Yoshimatsu T, Osorio D, Nilsson DE et al. 2018. Zebrafish differentially process color across visual space to match natural scenes. Curr. Biol. 28:2018–32.e5
    [Google Scholar]
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