Zebrafish Behavior: Opportunities and Challenges

Annual Review of Neuroscience

Volumn 40, Issue , 2017, Pages 125-147

  Orger, Michael B ^a   De Polavieja, Gonzalo G ^a  

^a CHAMPALIMAUD FOUNDATION   (Portugal)

Author keywords

Collective behavior; Computational models; Decision making; Imaging; Motor control; Tracking; Vision

Indexed keywords

AGGRESSION; ANIMAL BEHAVIOR; ARTICLE; BODY POSITION; BRAIN FUNCTION; CLASSIFICATION; DECISION MAKING; ESCAPE BEHAVIOR; FEEDING BEHAVIOR; GROUP DYNAMICS; ILLUMINATION; LARVA; LOCOMOTION; MATHEMATICAL MODEL; MATING; NERVE CELL NETWORK; NONHUMAN; ONTOGENY; OPTIC FLOW; PHOTOTAXIS; PREDATION; PRIORITY JOURNAL; SOCIAL BEHAVIOR; STARTLE REFLEX; SWIMMING; VIDEORECORDING; ZEBRA FISH; ANIMAL; BRAIN; NERVE CELL; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; NEURONS; SOCIAL BEHAVIOR; ZEBRAFISH;

EID: 85027026609     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-071714-033857     Document Type: Article

References (206)

1. Abrahamsson S, Chen J, Hajj B, Stallinga S, Katsov AY, et al. 2012. Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nat. Methods 10:60-63
2. Abril-de Abreu R, Cruz AS, Oliveira RF. 2015. Social dominance modulates eavesdropping in zebrafish. R. Soc. Open Sci. 2:150220
3. 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
4. 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
5. Aizenberg M, Schuman EM. 2011. Cerebellar-dependent learning in larval zebrafish. J. Neurosci. 31:8708-12
6. Al-Imari L, Gerlai R. 2008. Sight of conspecifics as reward in associative learning in zebrafish (Danio rerio). Behav. Brain Res. 189:216-19
7. Amo R, Fredes F, Kinoshita M, Aoki R, Aizawa H, et al. 2014. The habenulo-raphe serotonergic circuit encodes an aversive expectation value essential for adaptive active avoidance of danger. Neuron 84:1034-48
8. Arganda S, Perez-Escudero A, de Polavieja GG. 2012. A common rule for decisionmaking in animal collectives across species. PNAS 109:20508-13
9. Arrenberg AB, Bene FD, Baier H. 2009. Optical control of zebrafish behavior with halorhodopsin. PNAS 106:17968-73
10. Arunachalam M, Raja M, Vijayakumar C, Malaiammal P, Mayden RL. 2013. Natural history of zebrafish (Danio rerio) in India. Zebrafish 10:1-14
11. Auer TO, Duroure K, De Cian A, Concordet JP, Del Bene F. 2014. Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res. 24:142-53
12. Bak-Coleman J, Smith D, Coombs S. 2015. Animal behaviour. Anim. Behav. 107:7-17
13. Barker AJ, Baier H. 2015. Sensorimotor decision making in the zebrafish tectum. Curr. Biol. 25:2804-14
14. Beck JC, Gilland E, Tank DW, Baker R. 2004. Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J. Neurophysiol. 92:3546-61
15. Bergeron SA, Carrier N, Li GH, Ahn S, Burgess HA. 2014. Gsx1 expression defines neurons required for prepulse inhibition. Mol. Psychiatry 20:974-85
16. Berman GJ, Choi DM, Bialek W, Shaevitz JW. 2014. Mapping the stereotyped behaviour of freely moving fruit flies. J. R. Soc. Interface 11:20140672
17. Bernhardt RR, Chitnis AB, Lindamer L, Kuwada JY. 1990. Identification of spinal neurons in the embryonic and larval zebrafish. J. Comp. Neurol. 302:603-16
18. Bianco IH, Engert F. 2015. Visuomotor transformations underlying hunting behavior in zebrafish. Curr. Biol. 25:831-46
19. Bianco IH, Kampff AR, Engert F. 2011. Prey capture behavior evoked by simple visual stimuli in larval zebrafish. Front. Syst. Neurosci. 5:101
20. Bianco IH, Ma LH, Schoppik D, Robson DN, Orger MB, et al. 2012. The tangential nucleus controls a gravito-inertial vestibulo-ocular reflex. Curr. Biol. 22:1285-95
21. Billeh YN, Schaub MT, Anastassiou CA, Barahona M, Koch C. 2014. Revealing cell assemblies at multiple levels of granularity. J. Neurosci. Methods 236:92-106
22. Borla MA, Palecek B, Budick S, O'Malley DM. 2002. Prey capture by larval zebrafish: Evidence for fine axial motor control. Brain Behav. Evol. 60:207-29
23. Bouchard MB, Voleti V, Mendes CS, Lacefield C, Grueber WB, et al. 2015. Swept confocally-aligned planar excitation (SCAPE) microscopy for high speed volumetric imaging of behaving organisms. Nat. Photonics 9:113-19
24. Britten KH. 2008. Mechanisms of self-motion perception. Annu. Rev. Neurosci. 31:389-410
25. 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
26. Brown AEX, Yemini EI, Grundy LJ, Jucikas T, Schafer WR. 2013. A dictionary of behavioral motifs reveals clusters of genes affecting Caenorhabditis elegans locomotion. PNAS 110:791-96
27. Brown KH, Dobrinski KP, Lee AS, Gokcumen O, Mills RE, et al. 2012. Extensive genetic diversity and substructuring among zebrafish strains revealed through copy number variant analysis. PNAS 109:529-34
28. Bruni G, Rennekamp AJ, Velenich A, Mc Carroll M, Gendelev L, et al. 2016. Zebrafish behavioral profiling identifies multitarget antipsychotic-like compounds. Nat. Chem. Biol. 12:559-66
29. Budick S, O'Malley DM. 2000. Locomotor repertoire of the larval zebrafish: Swimming, turning and prey capture. J. Exp. Biol. 203:2565-79
30. Burgess HA, Granato M. 2007a. Modulation of locomotor activity in larval zebrafish during light adaptation. J. Exp. Biol. 210:2526-39
31. Burgess HA, Granato M. 2007b. Sensorimotor gating in larval zebrafish. J. Neurosci. 27:4984-94
32. Burgess HA, Schoch H, Granato M. 2010. Distinct retinal pathways drive spatial orientation behaviors in zebrafish navigation. Curr. Biol. 20:381-86
33. Buske C, Gerlai R. 2011. Shoaling develops with age in zebrafish (Danio rerio). Prog. Neuro-Psychopharmacol. Biol. Psychiatry 35:1409-15
34. Buss RR, Drapeau P. 2001. Synaptic drive tomotoneurons during fictive swimming in the developing zebrafish. J. Neurophysiol. 86:197-210
35. Butail S, Polverino G, Phamduy P, Del Sette F, Porfiri M. 2014. Influence of robotic shoal size, configuration, and activity on zebrafish behavior in a free-swimming environment. Behav. Brain Res. 275:269-80
36. Cachat J, Stewart A, Utterback E, Hart P, Gaikwad S, et al. 2011. Three-dimensional neurophenotyping of adult zebrafish behavior. PLOS ONE 6:e17597
37. Chen S, Chiu CN, Mc Arthur KL, Fetcho J.R., Prober DA. 2015. TRP channel mediated neuronal activation and ablation in freely behaving zebrafish. Nat. Methods 13:147-50
38. Chen X, Engert F. 2014. Navigational strategies underlying phototaxis in larval zebrafish. Front. Syst. Neurosci. 8:39
39. Cheng RK, Krishnan S, Jesuthasan S. 2016. Activation and inhibition of tph2 serotonergic neurons operate in tandem to influence larval zebrafish preference for light over darkness. Sci. Rep. 6:20788
40. Chhetri RK, Amat F, Wan Y, H ockendorf B, Lemon WC, Keller PJ. 2015. Whole-animal functional and developmental imaging with isotropic spatial resolution. Nat. Methods 12:1171-78
41. Choleris E, Pfaff DW, Kavaliers M, eds. 2013. Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior. Cambridge, UK: Cambridge Univ. Press
42. Clark DT. 1981. Visual responses in developing zebrafish (Brachydanio rerio). Ph D Thesis, Univ. Oregon, Eugene
43. Couzin ID. 2009. Collective cognition in animal groups. Trends Cogn. Sci. 13:36-43
44. Cunningham JP, Yu BM. 2014. Dimensionality reduction for large-scale neural recordings. Nat. Neurosci. 17:1500-9
45. Daie K, Goldman MS, Aksay ERF. 2015. Spatial patterns of persistent neural activity vary with the behavioral context of short-term memory. Neuron 85:847-60
46. Darrow KO, Harris WA. 2004. Characterization and development of courtship in zebrafish, Danio rerio. Zebrafish 1:40-45
47. Dell AI, Bender JA, Branson K, Couzin ID, de Polavieja GG, et al. 2014. Automated image-based tracking and its application in ecology. Trends Ecol. Evol. 29:417-28
48. Dreosti E, Lopes G, Kampff A, Wilson S. 2015. Development of social behaviour in young zebrafish. Front. Neural Circuits 9:39
49. 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
50. Dunn TW, Mu Y, Narayan S, Randlett O, Naumann EA, et al. 2016b. Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion. e Life 5:e12741
51. Easter SS, Nicola GN. 1997. The development of eye movements in the zebrafish (Danio rerio). Dev. Psychobiol. 31:267-76
52. Eaton RC, Farley RD. 1973. Development of the Mauthner neurons in embryos and larvae of the zebrafish, Brachydanio rerio. Copeia 4:673-82
53. Eaton RC, Nissanov J, Wieland CM. 1984. Differential activation of Mauthner and non-Mauthner startle circuits in the zebrafish: Implications for functional substitution. J. Comp. Physiol. 155:813-20
54. Emran F, Rihel J, Dowling JE. 2008. A behavioral assay to measure responsiveness of zebrafish to changes in light intensities. J. Vis. Exp. 20:e923
55. Enquist M, Ghirlanda S. 2005. Neural Networks and Animal Behavior. Princeton, NJ: Princeton Univ. Press
56. Fajardo O, Zhu P, Friedrich RW. 2013. Control of a specificmotor program by a small brain area in zebrafish. Front. Neural Circuits 7:67
57. Feierstein CE, Portugues R, Orger MB. 2015. Seeing the whole picture: A comprehensive imaging approach to functional mapping of circuits in behaving zebrafish. Neuroscience 296:26-38
58. 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
59. Fero K, Yokogawa T, Burgess HA. 2011. The behavioral repertoire of larval zebrafish. In Neuromethods, Vol. 52: Zebrafish Models in Neurobehavioral Research, ed. AV Kaleuff, JM Cachat, pp. 249-91. New York: Humana Press
60. Filosa A, Barker AJ, Maschio MD, Baier H. 2016. Feeding state modulates behavioral choice and processing of prey stimuli in the zebrafish tectum. Neuron 90:596-608
61. Fontaine E, Lentink D, Kranenbarg S, Muller UK, Van Leeuwen JL, et al. 2008. Automated visual tracking for studying the ontogeny of zebrafish swimming. J. Exp. Biol. 211:1305-16
62. Fosque BF, Sun Y, Dana H, Yang CT, Ohyama T, et al. 2015. Labeling of active neural circuits in vivo with designed calcium integrators. Science 347:755-60
63. Friedmann D, Hoagland A, Berlin S, Isacoff EY. 2014. A spinal opsin controls early neural activity and drives a behavioral light response. Curr. Biol. 25:69-74
64. Gabriel JP, Mahmood R, Walter AM, Kyriakatos A, Hauptmann G, et al. 2007. Locomotor pattern in the adult zebrafish spinal cord in vitro. J. Neurophysiol. 99:37-48
65. Gahtan E. 2005. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. J. Neurosci. 25:9294-303
66. Gerlai R. 2014. Social behavior of zebrafish: From synthetic images to biological mechanisms of shoaling. J. Neurosci. Methods 234:59-65
67. Gerlai R, Lahav M, Guo S, Rosenthal A. 2000. Drinks like a fish: Zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol. Biochem. Behav. 67:773-82
68. Gillis DM, Kramer DL. 1987. Ideal interference distributions: Population density and patch use by zebrafish. Anim. Behav. 35:1875-82
69. Girdhar K, Gruebele M, Chemla YR. 2015. The behavioral space of zebrafish locomotion and its neural network analog. PLOS ONE 10:e0128668
70. Gomez-Marin A, Paton JJ, Kampff AR, Costa RM, Mainen ZF. 2014. Big behavioral data: Psychology, ethology and the foundations of neuroscience. Nat. Neurosci. 17:1455-62
71. Goodson JL. 2005. The vertebrate social behavior network: Evolutionary themes and variations. Horm. Behav. 48:11-22
72. Gould TD, Gottesman II. 2006. Psychiatric endophenotypes and the development of valid animal models. Genes Brain Behav. 5:113-19
73. Grabowicz PA, Romero-Ferrero F, Lins T, de Polavieja GG, Benevenuto F, Gummadi KP. 2015. An experimental study of opinion influenceability. ar Xiv:1512.00770 [physics.soc-ph]
74. Grant JW, Kramer DL. 1992. Temporal clumping of food arrival reduces its monopolization and defence by zebrafish, Brachydanio rerio. Anim. Behav. 44:101-10
75. Green MH, Ho RK, Hale ME. 2011. Movement and function of the pectoral fins of the larval zebrafish (Danio rerio) during slow swimming. J. Exp. Biol. 214:3111-23
76. Haesemeyer M, Robson DN, Li JM, Schier AF, Engert F. 2015. The structure and timescales of heat perception in larval zebrafish. Cell Syst. 1:338-48
77. Hale ME, Katz HR, Peek MY, Fremont RT. 2016. Neural circuits that drive startle behavior, with a focus on the Mauthner cells and spiral fiber neurons of fishes. J. Neurogenet. 30:89-100
78. Herbert-Read JE, Krause S, Morrell LJ, Schaerf TM, Krause J, Ward AJW. 2013. The role of individuality in collective group movement. Proc. R. Soc. B 280:20122564
79. Hinz FI, Aizenberg M, Tushev G, Schuman EM. 2013. Protein synthesis-dependent associative long-term memory in larval zebrafish. J. Neurosci. 33:15382-87
80. Hoffman EJ, Turner KJ, Fernandez JM, Cifuentes D, Ghosh M, et al. 2016. Estrogens suppress a behavioral phenotype in zebrafish mutants of the autism risk gene, CNTNAP2. Neuron 89:725-33
81. Horstick EJ, Mueller T, Burgess HA. 2016. Motivated state control in larval zebrafish: Behavioral paradigms and anatomical substrates. J. Neurogenet. 30:122-32
82. Huang YY, Tschopp M, Neuhauss SCF. 2009. Illusionary self-motion perception in zebrafish. PLOS ONE 4:e6550
83. Huber-Reggi SP, Mueller KP, Neuhauss SCF. 2012. Analysis of optokinetic response in zebrafish by computerbased eye tracking. In Methods in Molecular Biology, Vol. 935: Retinal Degeneration: Methods and Protocols, ed. BHF Weber, T Langmann, pp. 139-60. Totowa, NJ: Humana Press
84. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, et al. 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31:227-29
85. Ioannou CC, Guttal V, Couzin ID. 2012. Predatory fish select for coordinated collective motion in virtual prey. Science 337:1212-15
86. Jetti SK, Vendrell-Llopis N, Yaksi E. 2014. Spontaneous activity governs olfactory representations in spatially organized habenular microcircuits. Curr. Biol. 24:434-39
87. Kabra M, Robie AA, Rivera-Alba M, Branson S, Branson K. 2012. JAABA: Interactive machine learning for automatic annotation of animal behavior. Nat. Methods 10:64-67
88. Kalueff AV, Cachat J, eds. 2011. Neuromethods, vol. 52: Zebrafish Models in Neurobehavioral Research. New York: Humana Press. 1st ed.
89. Kalueff AV, Gebhardt M, Stewart AM, Cachat JM, Brimmer M, et al. 2013. Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish 10: 70-86
90. Kimmel CB, Patterson J, Kimmel RO. 1974. The development and behavioral characteristics of the startle response in the zebra fish. Dev. Psychobiol. 7:47-60
91. Kimura Y, Satou C, Fujioka S, Shoji W, Umeda K, et al. 2013. Hindbrain V2a neuronsin the excitation of spinal locomotor circuits during zebrafish swimming. Curr. Biol. 23:843-49
92. 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
93. Kobak D, Brendel W, Constantinidis C, Feierstein CE, Kepecs A, et al. 2016. Demixed principal component analysis of neural population data. e Life 5:e10989
94. Kohashi T, Nakata N, Oda Y. 2012. Effective sensory modality activating an escape triggering neuron switches during early development in zebrafish. J. Neurosci. 32:5810-20
95. Kokel D, Bryan J, Laggner C, White R, Cheung CYJ, et al. 2010. Rapid behavior-based identification of neuroactive small molecules in the zebrafish. Nat. Methods 6:231-37
96. Kokel D, Dunn TW, Ahrens MB, Alshut R, Cheung CYJ, et al. 2013. Identification of nonvisual photomotor response cells in the vertebrate hindbrain. J. Neurosci. 33:3834-43
97. Kokko H. 2007. Modelling for Field Biologists and Other Interesting People. Cambridge, UK: Cambridge Univ. Press
98. Koyama M, Kinkhabwala A, Satou C, Higashijima SI, Fetcho J. 2011. Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. PNAS 108:1170-75
99. Koyama M, Minale F, Shum J, Nishimura N, Schaffer CB, Fetcho J.R. 2016. A circuit motif in the zebrafish hindbrain for a two alternative behavioral choice to turn left or right. e Life 5:e16808
100. Krause J, Ruxton GD. 2002. Living in Groups. Oxford, UK: Oxford Univ. Press
101. Kubo F, Hablitzel B, Maschio MD, 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
102. La Coste AMB, 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
103. Lange M, Neuzeret F, Fabreges B, Froc C, Bedu S, et al. 2013. Inter-individual and inter-strain variations in zebrafish locomotor ontogeny. PLOS ONE 8:e70172
104. Lee A, Mathuru AS, Teh C, Kibat C, Korzh V, et al. 2010. The habenula prevents helpless behavior in larval zebrafish. Curr. Biol. 20:2211-16
105. Leshner A, Pfaff DW. 2011. Quantification of behavior. PNAS 108(Suppl. 3):15537-41
106. Levoy M, Ng R, Adams A, Footer M. 2006. Light field microscopy. ACM Trans. Graph. 25(3):1-11
107. Li G, Muller UK, Van Leeuwen JL, Liu H. 2012. Body dynamics and hydrodynamics of swimming fish larvae: A computational study. J. Exp. Biol. 215:4015-33
108. Li G, Muller UK, Van Leeuwen JL, Liu H. 2014. Escape trajectories are deflected when fish larvae intercept their own C-start wake. J. R. Soc. Interface 11:20140848
109. Li Y, Lee JM, Chon TS, Liu Y, Kim H, Bae MJ. 2013. Analysis of movement behavior of zebrafish (Danio rerio) under chemical stress using hidden Markov model. Mod. Phys. Lett. B 27:1350014
110. Lindeyer CM, Reader SM. 2010. Social learning of escape routes in zebrafish and the stability of behavioural traditions. Anim. Behav. 79:827-34
111. Liu KS, Fetcho J.R. 1999. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 23:325-35
112. Liu Y, Lee SH, Chon TS. 2011. Analysis of behavioral changes of zebrafish (Danio rerio) in response to formaldehyde using Self-organizing map and a hidden Markov model. Ecol. Model. 222:2191-201
113. Liu YC, Hale ME. 2014. Alternative forms of axial startle behaviors in fishes. Zoology 117:36-47
114. Lorent K, Liu KS, Fetcho J.R., Granato M. 2001. The zebrafish space cadet gene controls axonal pathfinding of neurons that modulate fast turning movements. Development 128:2131-42
115. Lum PY, Singh G, Lehman A, Ishkanov T, Vejdemo-Johansson M, et al. 2013. Extracting insights from the shape of complex data using topology. Sci. Rep. 3:1236
116. Ma LH, Grove CL, Baker R. 2014. Development of oculomotor circuitry independent of hox3 genes. Nat. Commun. 5:4221
117. Madirolas G, de Polavieja GG. 2015. Improving collective estimations using resistance to social influence. PLOS Comput. Biol. 11:e1004594
118. Martineau PR, Mourrain P. 2013. Tracking zebrafish larvae in group-status and perspectives. Methods 62:292-303
119. Masino MA, Fetcho J.R. 2005. Fictive swimming motor patterns in wild type and mutant larval zebrafish. J. Neurophysiol. 93:3177-88
120. Masseck OA, Hoffmann KP. 2009. Comparative neurobiology of the optokinetic reflex. Ann. N. Y. Acad. Sci. 1164:430-39
121. Mc Clenahan P, Troup M, Scott EK. 2012. Fin-tail coordination during escape and predatory behavior in larval zebrafish. PLOS ONE 7:e32295
122. Mc Elligott MB, O'Malley DM. 2005. Prey tracking by larval zebrafish: Axial kinematics and visual control. Brain Behav. Evol. 66:177-96
123. Mc Henry MJ, Feitl KE, Strother JA, Van Trump WJ. 2009. Larval zebrafish rapidly sense the water flow of a predator's strike. Biol. Lett. 5:477-79
124. Mc Lean DL, Fan J, Higashijima SI, Hale ME, Fetcho J.R. 2007. A topographic map of recruitment in spinal cord. Nature 446:71-75
125. Mc Lean DL, Fetcho J.R. 2008. Using imaging and genetics in zebrafish to study developing spinal circuits in vivo. Dev. Neurobiol. 68:817-34
126. Miller N, Gerlai R. 2007. Quantification of shoaling behaviour in zebrafish (Danio rerio). Behav. Brain Res. 184:157-66
127. Mirat O, Sternberg J.R., Severi KE, Wyart C. 2013. Zebra Zoom: An automated program for high-throughput behavioral analysis and categorization. Front. Neural Circ. 7:107
128. 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
129. Miri A, Daie K, Burdine RD, Aksay E, Tank DW. 2011b. Regression-based identification of behaviorencoding neurons during large-scale optical imaging of neural activity at cellular resolution. J. Neurophysiol. 105:964-80
130. Mnih V, Kavukcuoglu K, Silver D, Rusu AA, Veness J, et al. 2015. Human-level control through deep reinforcement learning. Nature 518:529-33
131. Muto A, Ohkura M, Abe G, Nakai J, Kawakami K. 2013. Real-time visualization of neuronal activity during perception. Curr. Biol. 23:307-11
132. Mwaffo V, Anderson RP, Butail S, Porfiri M. 2015. A jump persistent turning walker to model zebrafish locomotion. J. R. Soc. Interface 12:20140884
133. Nair A, Azatian G, Mc Henry MJ. 2015. The kinematics of directional control in the fast start of zebrafish larvae. J. Exp. Biol. 218:3996-4004
134. Neri P. 2012. Feature binding in zebrafish. Anim. Behav. 84:485-93
135. 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
136. Nguyen JP, Shipley FB, Linder AN, Plummer GS, Liu M, et al. 2016. Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans. PNAS 113:E1074-81
137. Norton W, Bally-Cuif L. 2010. Adult zebrafish as a model organism for behavioural genetics. BMC Neurosci. 11:90
138. O'Connell LA, Hofmann HA. 2011. The vertebrate mesolimbic reward system and social behavior network: A comparative synthesis. J. Comp. Neurol 519:3599-639
139. Olive R, Wolf S, Dubreuil A, Bormuth V, Debregeas G, Candelier R. 2016. Rheotaxis of larval zebrafish: Behavioral study of a multi-sensory process. Front. Syst. Neurosci. 10:413
140. Oliveira RF. 2013. Mind the fish: Zebrafish as a model in cognitive social neuroscience. Front. Neural Circ. 7:131
141. Oliveira RF, Silva JF, Sim oes JM. 2011. Fighting zebrafish: Characterization of aggressive behavior andwinner-loser effects. Zebrafish 8:73-81
142. Olszewski J, Haehnel M, Taguchi M, Liao JC. 2012. Zebrafish larvae exhibit rheotaxis and can escape a continuous suction source using their lateral line. PLOS ONE 7:e36661
143. O'Malley DM, Kao YH, Fetcho J.R. 1996. Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron 17:1145-55
144. Ono F, Higashijima S, Shcherbatko A, Fetcho J.R., Brehm P. 2001. Paralytic zebrafish lacking acetylcholine receptors fail to localize rapsyn clusters to the synapse. J. Neurosci. 21:5439-48
145. Orger MB, Baier H. 2005. Channeling of red and green cone inputs to the zebrafish optomotor response. Visual Neurosci. 22:275-81
146. 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
147. Panier T, Romano SA, Olive R, Pietri T, Sumbre G, et al. 2013. Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy. Front. Neural Circ. 7:65
148. Parichy DM. 2015. Advancing biology through a deeper understanding of zebrafish ecology and evolution. e Life 4:e05635
149. Pelkowski SD, Kapoor M, Richendrfer HA, Wang X, Colwill RM, Creton R. 2011. A novel high-throughput imaging system for automated analyses of avoidance behavior in zebrafish larvae. Behav. Brain Res. 223:135-44
150. Perez-Escudero A, Vicente-Page J, Hinz RC, Arganda S, de Polavieja GG. 2014. id Tracker: Tracking individuals in a group by automatic identification of unmarked animals. Nat. Methods 11:743-48
151. Petreanu L, Gutnisky DA, Huber D, Xu N, O'Connor DH, et al. 2012. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489:299-303
152. Portugues R, Engert F. 2011. Adaptive locomotor behavior in larval zebrafish. Front. Syst. Neurosci. 5:72
153. Portugues R, Feierstein CE, Engert F, Orger MB. 2014. Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior. Neuron 81:1328-43
154. Portugues R, Haesemeyer M, Blum ML, Engert F. 2015. Whole-field visual motion drives swimming in larval zebrafish via a stochastic process. J. Exp. Biol. 218:1433-43
155. Portugues R, Severi KE, Wyart C, Ahrens MB. 2013. Optogenetics in a transparent animal: Circuit function in the larval zebrafish. Curr. Opin. Neurobiol. 23:119-26
156. Pritchard V, Lawrence J, Butlin RK, Krause J. 2001. Shoal choice in zebrafish, Danio rerio: The influence of shoal size and activity. Anim. Behav. 62:1085-88
157. Prober DA, Rihel J, Onah AA, Sung RJ, Schier AF. 2006. Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J. Neurosci. 26:13400-10
158. Quirin S, Vladimirov N, Yang CT, Peterka DS, Yuste R, Ahrens MB. 2016. Calcium imaging of neural circuits with extended depth-of-field light-sheet microscopy. Opt. Lett. 41:855-58
159. Renninger SL, Orger MB. 2013. Two-photon imaging of neural population activity in zebrafish. Methods 62:255-67
160. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, et al. 2010. Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327:348-51
161. Roberts AC, Bill BR, Glanzman DL. 2013. Learning andmemory in zebrafish larvae. Front. Neural Circ. 7:126
162. 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
163. Ruhl N, Mc Robert SP. 2005. The effect of sex and shoal size on shoaling behaviour in Danio rerio. J. Fish Biol. 67:1318-26
164. Saint-Amant L, Drapeau P. 1998. Time course of the development ofmotor behaviors in the zebrafish embryo. J. Neurobiol. 37:622-32
165. Saint-Amant L, Drapeau P. 2000. Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J. Neurosci. 20:3964-72
166. Satou C, Kimura Y, Kohashi T, Takeda H, Oda Y, Higashijima SI. 2009. Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish. J. Neurosci. 29:6780-93
167. Saverino C, Gerlai R. 2008. The social zebrafish: Behavioral responses to conspecific, heterospecific, and computer animated fish. Behav. Brain Res. 191:77-87
168. Schlegel T, Schuster S. 2008. Small circuits for large tasks: High-speed decision-making in archerfish. Science 319:104-6
169. Scott EK, Mason L, Arrenberg AB, Ziv L, Gosse NJ, et al. 2007. Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. Nat. Methods 4:323-26
170. Sela G, Lauri A, Dean-Ben XL, Kneipp M. 2015. Functional optoacoustic neuro-tomography (FONT) for whole-brain monitoring of calcium indicators. ar Xiv:1501.02450 [q-bio.NC]
171. Semmelhack JL, Donovan JC, Thiele TR, Kuehn E, Laurell E, Baier H. 2014. A dedicated visual pathway for prey detection in larval zebrafish. e Life 3:e04878
172. Serra EL, Medalha CC, Mattioli R. 1999. Natural preference of zebrafish (Danio rerio) for a dark environment. Braz. J. Med. Biol. Res. 32:1551-53
173. 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
174. Shoham Y, Leyton-Brown K. 2009. Multiagent Systems: Algorithmic, Game-Theoretic, and Logical Foundations. Cambridge, UK: Cambridge Univ. Press
175. Singh G, Memoli F, Ishkhanov T, Sapiro G, Carlsson G, Ringach DL. 2008. Topological analysis of population activity in visual cortex. J. Vis. 8:11
176. Snekser JL, Ruhl N, Bauer K, Mc Robert SP. 2010. The influence of sex and phenotype on shoaling decisions in zebrafish. Int. J. Comp. Psychol. 23:70-81
177. Spence R, Gerlach G, Lawrence C, Smith C. 2008. The behaviour and ecology of the zebrafish, Danio rerio. Biol. Rev. Camb. Philos. Soc. 83:13-34
178. Sternberg J.R., Severi KE, Fidelin K, Gomez J, Ihara H, et al. 2016. Optimization of a neurotoxin to investigate the contribution of excitatory interneurons to speed modulation in vivo. Curr. Biol. 26:2319-28
179. Stewart AM, Grieco F, Tegelenbosch RA, Kyzar EJ, Nguyen M, et al. 2015. A novel 3D method of locomotor analysis in adult zebrafish: Implications for automated detection of CNS drug-evoked phenotypes. J. Neurosci. Methods 255:66-74
180. Suli A, Watson GM, Rubel EW, Raible DW. 2012. Rheotaxis in larval zebrafish is mediated by lateral line mechanosensory hair cells. PLOS ONE 7:e29727
181. Sumpter DJT. 2011. Collective Animal Behavior. Princeton, NJ: Princeton Univ. Press
182. Suriyampola PS, Shelton DS, Shukla R, Roy T, Bhat A, Martins EP. 2016. Zebrafish social behavior in the wild. Zebrafish 13:1-8
183. Tabor KM, Bergeron SA, Horstick EJ, Jordan DC, Aho V, et al. 2014. Direct activation of the Mauthner cell by electric field pulses drives ultra-rapid escape responses. J. Neurophysiol. 112:834-44
184. Temizer I, Donovan JC, Baier H, Semmelhack JL. 2015. A visual pathway for looming-evoked escape in larval zebrafish. Curr. Biol. 25:1823-34
185. 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
186. Tinbergen N. 1951. The Study of Instinct. Oxford, UK: Clarendon Press
187. 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 Circ. 7:86
188. Valente A, Huang KH, Portugues R, Engert F. 2012. Ontogeny of classical and operant learning behaviors in zebrafish. Learn. Memory 19:170-77
189. Vendrell-Llopis N, Yaksi E. 2015. Evolutionary conserved brainstem circuits encode category, concentration and mixtures of taste. Sci. Rep. 5:17825
190. Venkatachalam V, Ji N, Wang X, Clark C, Mitchell JK, et al. 2016. Pan-neuronal imaging in roaming Caenorhabditis elegans. PNAS 113:E1082-88
191. Vladimirov N, Mu Y, Kawashima T, Bennett DV, Yang CT, et al. 2014. Light-sheet functional imaging in fictively behaving zebrafish. Nat. Methods 11:883-84
192. Voesenek CJ, Pieters RPM, van Leeuwen JL. 2016. Automated reconstruction of three-dimensional fish motion, forces, and torques. PLOS ONE 11:e0146682
193. Wang YN, Hou YY, Sun MZ, Zhang CY, Bai G, et al. 2014. Behavioural screening of zebrafish using neuroactive traditional Chinese medicine prescriptions and biological targets. Sci. Rep. 4:5311
194. Ward AJW, Sumpter DJT, Couzin ID, Hart PJB, Krause J. 2008. Quorum decision-making facilitates information transfer in fish shoals. PNAS 105:6948-53
195. Warp E, Agarwal G, Wyart C, Friedmann D, Oldfield CS, et al. 2012. Emergence of patterned activity in the developing zebrafish spinal cord. Curr. Biol. 22:93-102
196. 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
197. Wiltschko AB, Johnson MJ, Iurilli G, Peterson RE, Katon JM, et al. 2015. Mapping sub-second structure in mouse behavior. Neuron 88:1121-35
198. Wolf S, Supatto W, Debregeas G, Mahou P, Kruglik SG, et al. 2015. Whole-brain functional imaging with two-photon light-sheet microscopy. Nat. Methods 12:379-80
199. Wolman MA, Jain RA, Liss L, Granato M.2011. Chemical modulation ofmemory formation in larval zebrafish. PNAS 108:15468-73
200. Woods IG, Schoppik D, Shi VJ, Zimmerman S, Coleman HA, et al. 2014. Neuropeptidergic signaling partitions arousal behaviors in zebrafish. J. Neurosci. 34:3142-60
201. Wright D, Nakamichi R, Krause J, Butlin RK. 2006. QTL analysis of behavioral and morphological differentiation between wild and laboratory zebrafish (Danio rerio). Behav. Genet. 36:271-84
202. 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
203. Zhou Y, Cattley RT, Cario CL, Bai Q, Burton EA. 2014. Quantification of larval zebrafish motor function in multiwell plates using open-source MATLAB applications. Nat. Protoc. 9:1533-48
204. Zhu L, Weng W. 2007. Catadioptric stereo-vision system for the real-time monitoring of 3D behavior in aquatic animals. Physiol. Behav. 91:106-19
205. Zhu P, Fajardo O, Shum J, Scharer YPZ, Friedrich RW. 2012. High-resolution optical control of spatiotemporal neuronal activity patterns in zebrafish using a digital micromirror device. Nat. Protoc. 7:1410-25
206. Zhu P, Narita Y, Bundschuh ST, Fajardo O, Scharer YPZ, et al. 2009. Optogenetic dissection of neuronal circuits in zebrafish using viral gene transfer and the Tet system. Front. Neural Circ. 3:21