Zebrafish

Living reference work entry

Abstract

The zebrafish (Danio rerio) is a cost-effective vertebrate model system amenable to pharmacological investigation. Many of the available drug assays are relatively straightforward to perform, as small molecules dissolved directly in the water can be directly taken up by the zebrafish to elicit biological effects in target tissues. The low cost and ease of drug administration have especially enabled the adoption of high-throughput pharmacological screening in whole, intact animals. In addition, a fully sequenced genome and numerous tools to manipulate genes allow for the rapid generation of zebrafish disease models. Finally, the high conservation between zebrafish and mammalian drug targets facilitates bringing zebrafish pharmacological discoveries into the clinic.

References and Further Reading

General Considerations

  1. Auer TO, Del Bene F (2014) CRISPR/Cas9 and TALEN-mediated knock-in approaches in zebrafish. Methods 69:142–150PubMedGoogle Scholar
  2. Bedell VM, Ekker SC (2015) Using engineered endonucleases to create knockout and knockin zebrafish models. Methods Mol Biol 1239:291–305PubMedGoogle Scholar
  3. Chang T-Y, Shi P, Steinmeyer JD, Chatnuntawech I, Tillberg P, Love KT, Eimon PM, Anderson DG, Yanik MF (2014) Organ-targeted high-throughput in vivo biologics screen identifies materials for RNA delivery. Integr Biol (Camb) 6:926–934Google Scholar
  4. Dunér T, Conlon JM, Kukkonen JP, Akerman KEO, Yan Y-L, Postlethwait JH, Larhammar D (2002) Cloning, structural characterization and functional expression of a zebrafish bradykinin B2-related receptor. Biochem J 364:817–824PubMedCentralPubMedGoogle Scholar
  5. Eliceiri BP, Gonzalez AM, Baird A (2011) Zebrafish model of the blood-brain barrier: morphological and permeability studies. Methods Mol Biol 686:371–378PubMedCentralPubMedGoogle Scholar
  6. Fleming A, Diekmann H, Goldsmith P (2013) Functional characterisation of the maturation of the blood-brain barrier in larval zebrafish. PLoS One 8:e77548PubMedCentralPubMedGoogle Scholar
  7. Gonzalez-Nuñez V, Fernández M, de Velasco E, Arsequell G, Valencia G, Rodríguez RE (2007) Identification of dynorphin a from zebrafish: a comparative study with mammalian dynorphin A. Neuroscience 144:675–684PubMedGoogle Scholar
  8. Hossain MS, Larsson A, Scherbak N, Olsson P-E, Orban L (2008) Zebrafish androgen receptor: isolation, molecular, and biochemical characterization. Biol Reprod 78:361–369PubMedGoogle Scholar
  9. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503PubMedCentralPubMedGoogle Scholar
  10. Hsieh DJ-Y, Liao C-F (2002) Zebrafish M2 muscarinic acetylcholine receptor: cloning, pharmacological characterization, expression patterns and roles in embryonic bradycardia. Br J Pharmacol 137:782–792PubMedCentralPubMedGoogle Scholar
  11. Jeong J-Y, Kwon H-B, Ahn J-C, Kang D, Kwon S-H, Park JA, Kim K-W (2008) Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain Res Bull 75:619–628PubMedGoogle Scholar
  12. Kawakami K, Abe G, Asada T, Asakawa K, Fukuda R, Ito A, Lal P, Mouri N, Muto A, Suster ML et al (2010) zTrap: zebrafish gene trap and enhancer trap database. BMC Dev Biol 10:105PubMedCentralPubMedGoogle Scholar
  13. Kettleborough RNW, Busch-Nentwich EM, Harvey SA, Dooley CM, de Bruijn E, van Eeden F, Sealy I, White RJ, Herd C, Nijman IJ et al (2013) A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 496:494–497PubMedCentralPubMedGoogle Scholar
  14. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310PubMedGoogle Scholar
  15. Kondrychyn I, Teh C, Garcia-Lecea M, Guan Y, Kang A, Korzh V (2011) Zebrafish enhancer TRAP transgenic line database ZETRAP 2.0. Zebrafish 8:181–182PubMedGoogle Scholar
  16. Kyzar E, Zapolsky I, Green J, Gaikwad S, Pham M, Collins C, Roth A, Stewart AM, St-Pierre P, Hirons B et al (2012a) The Zebrafish Neurophenome Database (ZND): a dynamic open-access resource for zebrafish neurophenotypic data. Zebrafish 9:8–14PubMedGoogle Scholar
  17. Nüsslein-Volhard C (2012) The zebrafish issue of development. Development 139:4099–4103PubMedGoogle Scholar
  18. Pardo-Martin C, Chang T-Y, Koo BK, Gilleland CL, Wasserman SC, Yanik MF (2010) High-throughput in vivo vertebrate screening. Nat Methods 7:634–636PubMedCentralPubMedGoogle Scholar
  19. Parng C (2005) In vivo zebrafish assays for toxicity testing. Curr Opin Drug Discov Devel 8:100–106PubMedGoogle Scholar
  20. Peitsaro N, Sundvik M, Anichtchik OV, Kaslin J, Panula P (2007) Identification of zebrafish histamine H1, H2 and H3 receptors and effects of histaminergic ligands on behavior. Biochem Pharmacol 73:1205–1214PubMedGoogle Scholar
  21. Peterson RT, Fishman MC (2011) Designing zebrafish chemical screens. Methods Cell Biol 105:525–541PubMedGoogle Scholar
  22. Pfriem A, Pylatiuk C, Alshut R, Ziegener B, Schulz S, Bretthauer G (2012) A modular, low-cost robot for zebrafish handling. Conf Proc IEEE Eng Med Biol Soc 2012:980–983PubMedGoogle Scholar
  23. Pugach EK, Li P, White R, Zon L (2009) Retro-orbital injection in adult zebrafish. J Vis Exp 34. pii: 1645Google Scholar
  24. Radi M, Evensen L, Dreassi E, Zamperini C, Caporicci M, Falchi F, Musumeci F, Schenone S, Lorens JB, Botta M (2012) A combined targeted/phenotypic approach for the identification of new antiangiogenics agents active on a zebrafish model: from in silico screening to cyclodextrin formulation. Bioorg Med Chem Lett 22:5579–5583PubMedGoogle Scholar
  25. Renier C, Faraco JH, Bourgin P, Motley T, Bonaventure P, Rosa F, Mignot E (2007a) Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenet Genomics 17:237–253PubMedGoogle Scholar
  26. Rennekamp AJ, Peterson RT (2015) 15 years of zebrafish chemical screening. Curr Opin Chem Biol 24C:58–70Google Scholar
  27. Ringholm A, Fredriksson R, Poliakova N, Yan Y-L, Postlethwait JH, Larhammar D, Schiöth HB (2002) One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology. J Neurochem 82:6–18PubMedGoogle Scholar
  28. Rivas-Boyero AA, Herrero-Turrión MJ, Gonzalez-Nunez V, Sánchez-Simón FM, Barreto-Valer K, Rodríguez RE (2011) Pharmacological characterization of a nociceptin receptor from zebrafish (Danio rerio). J Mol Endocrinol 46:111–123PubMedGoogle Scholar
  29. Ruuskanen JO, Peitsaro N, Kaslin JVM, Panula P, Scheinin M (2005) Expression and function of alpha-adrenoceptors in zebrafish: drug effects, mRNA and receptor distributions. J Neurochem 94:1559–1569PubMedGoogle Scholar
  30. Spaink HP, Cui C, Wiweger MI, Jansen HJ, Veneman WJ, Marín-Juez R, de Sonneville J, Ordas A, Torraca V, van der Ent W et al (2013) Robotic injection of zebrafish embryos for high-throughput screening in disease models. Methods 62:246–254PubMedGoogle Scholar
  31. Sprague J, Bayraktaroglu L, Bradford Y, Conlin T, Dunn N, Fashena D, Frazer K, Haendel M, Howe DG, Knight J et al (2008) The Zebrafish Information Network: the zebrafish model organism database provides expanded support for genotypes and phenotypes. Nucleic Acids Res 36:D768–D772PubMedCentralPubMedGoogle Scholar
  32. Tamplin OJ, White RM, Jing L, Kaufman CK, Lacadie SA, Li P, Taylor AM, Zon LI (2012) Small molecule screening in zebrafish: swimming in potential drug therapies. Wiley Interdiscip Rev Dev Biol 1:459–468PubMedGoogle Scholar
  33. Tan JL, Zon LI (2011) Chemical screening in zebrafish for novel biological and therapeutic discovery. Methods Cell Biol 105:493–516PubMedGoogle Scholar
  34. Wang W, Liu X, Gelinas D, Ciruna B, Sun Y (2007) A fully automated robotic system for microinjection of zebrafish embryos. PLoS One 2:e862PubMedCentralPubMedGoogle Scholar
  35. Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio), 4th edn. University of Oregon Press, EugeneGoogle Scholar
  36. Williams FE, Messer WS (2004) Muscarinic acetylcholine receptors in the brain of the zebrafish (Danio rerio) measured by radioligand binding techniques. Comp Biochem Physiol C Toxicol Pharmacol 137:349–353PubMedGoogle Scholar
  37. Xie J, Farage E, Sugimoto M, Anand-Apte B (2010) A novel transgenic zebrafish model for blood-brain and blood-retinal barrier development. BMC Dev Biol 10:76PubMedCentralPubMedGoogle Scholar

Developmental Signalling, Cell Proliferation, and Cancer

  1. Alvarez Y, Astudillo O, Jensen L, Reynolds AL, Waghorne N, Brazil DP, Cao Y, O’Connor JJ, Kennedy BN (2009) Selective inhibition of retinal angiogenesis by targeting PI3 kinase. PLoS One 4:e7867PubMedCentralPubMedGoogle Scholar
  2. Anelli V, Santoriello C, Distel M, Köster RW, Ciccarelli FD, Mione M (2009) Global repression of cancer gene expression in a zebrafish model of melanoma is linked to epigenetic regulation. Zebrafish 6:417–424PubMedGoogle Scholar
  3. Brion F, Le Page Y, Piccini B, Cardoso O, Tong S-K, Chung B, Kah O (2012) Screening estrogenic activities of chemicals or mixtures in vivo using transgenic (cyp19a1b-GFP) zebrafish embryos. PLoS One 7:e36069PubMedCentralPubMedGoogle Scholar
  4. Choi W-Y, Gemberling M, Wang J, Holdway JE, Shen M-C, Karlstrom RO, Poss KD (2013a) In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development 140:660–666PubMedCentralPubMedGoogle Scholar
  5. Das BC, McCartin K, Liu T-C, Peterson RT, Evans T (2010) A forward chemical screen in zebrafish identifies a retinoic acid derivative with receptor specificity. PLoS One 5:e10004PubMedCentralPubMedGoogle Scholar
  6. Dovey M, White RM, Zon LI (2009) Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish 6:397–404PubMedCentralPubMedGoogle Scholar
  7. Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J, Stemple DL, Stainier DY, Zwartkruis F, Abdelilah S, Rangini Z et al (1996) A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123:37–46PubMedGoogle Scholar
  8. Dryja TP, O’Neil-Dryja M, Pawelek JM, Albert DM (1978) Demonstration of tyrosinase in the adult bovine uveal tract and retinal pigment epithelium. Invest Ophthalmol Vis Sci 17:511–514PubMedGoogle Scholar
  9. Gebruers E, Cordero-Maldonado ML, Gray AI, Clements C, Harvey AL, Edrada-Ebel R, de Witte PAM, Crawford AD, Esguerra CV (2013) A phenotypic screen in zebrafish identifies a novel small-molecule inducer of ectopic tail formation suggestive of alterations in non-canonical Wnt/PCP signaling. PLoS One 8:e83293PubMedCentralPubMedGoogle Scholar
  10. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3:688–694PubMedCentralPubMedGoogle Scholar
  11. de Groh ED, Swanhart LM, Cosentino CC, Jackson RL, Dai W, Kitchens CA, Day BW, Smithgall TE, Hukriede NA (2010) Inhibition of histone deacetylase expands the renal progenitor cell population. J Am Soc Nephrol 21:794–802PubMedCentralPubMedGoogle Scholar
  12. Gutierrez A, Pan L, Groen RWJ, Baleydier F, Kentsis A, Marineau J, Grebliunaite R, Kozakewich E, Reed C, Pflumio F et al (2014) Phenothiazines induce PP2A-mediated apoptosis in T cell acute lymphoblastic leukemia. J Clin Invest 124:644–655PubMedCentralPubMedGoogle Scholar
  13. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP et al (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123:1–36PubMedGoogle Scholar
  14. Hao J, Ao A, Zhou L, Murphy CK, Frist AY, Keel JJ, Thorne CA, Kim K, Lee E, Hong CC (2013) Selective small molecule targeting β-catenin function discovered by in vivo chemical genetic screen. Cell Rep 4:898–904PubMedCentralPubMedGoogle Scholar
  15. Holder N, Hill J (1991) Retinoic acid modifies development of the midbrain-hindbrain border and affects cranial ganglion formation in zebrafish embryos. Development 113:1159–1170PubMedGoogle Scholar
  16. Jung D-W, Williams D, Khersonsky SM, Kang T-W, Heidary N, Chang Y-T, Orlow SJ (2005) Identification of the F1F0 mitochondrial ATPase as a target for modulating skin pigmentation by screening a tagged triazine library in zebrafish. Mol Biosyst 1:85–92PubMedGoogle Scholar
  17. Kitambi SS, McCulloch KJ, Peterson RT, Malicki JJ (2009) Small molecule screen for compounds that affect vascular development in the zebrafish retina. Mech Dev 126:464–477PubMedCentralPubMedGoogle Scholar
  18. Klein PS, Melton DA (1996) A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 93:8455–8459PubMedCentralPubMedGoogle Scholar
  19. Langenau DM, Traver D, Ferrando AA, Kutok JL, Aster JC, Kanki JP, Lin S, Prochownik E, Trede NS, Zon LI et al (2003) Myc-induced T cell leukemia in transgenic zebrafish. Science 299:887–890PubMedGoogle Scholar
  20. Langheinrich U, Hennen E, Stott G, Vacun G (2002) Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr Biol 12:2023–2028PubMedGoogle Scholar
  21. Mathew LK, Sengupta S, Kawakami A, Andreasen EA, Löhr CV, Loynes CA, Renshaw SA, Peterson RT, Tanguay RL (2007a) Unraveling tissue regeneration pathways using chemical genetics. J Biol Chem 282:35202–35210PubMedGoogle Scholar
  22. Michailidou C, Jones M, Walker P, Kamarashev J, Kelly A, Hurlstone AFL (2009) Dissecting the roles of Raf- and PI3K-signalling pathways in melanoma formation and progression in a zebrafish model. Dis Model Mech 2:399–411PubMedGoogle Scholar
  23. Molina G, Vogt A, Bakan A, Dai W, Queiroz de Oliveira P, Znosko W, Smithgall TE, Bahar I, Lazo JS, Day BW et al (2009) Zebrafish chemical screening reveals an inhibitor of Dusp6 that expands cardiac cell lineages. Nat Chem Biol 5:680–687PubMedCentralPubMedGoogle Scholar
  24. Murphey RD, Stern HM, Straub CT, Zon LI (2006) A chemical genetic screen for cell cycle inhibitors in zebrafish embryos. Chem Biol Drug Des 68:213–219PubMedGoogle Scholar
  25. Neumann CJ, Grandel H, Gaffield W, Schulte-Merker S, Nüsslein-Volhard C (1999) Transient establishment of anteroposterior polarity in the zebrafish pectoral fin bud in the absence of sonic hedgehog activity. Development 126:4817–4826PubMedGoogle Scholar
  26. North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR, Lord AM, Weber GJ, Bowman TV, Jang I-H, Grosser T et al (2007) Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447:1007–1011PubMedCentralPubMedGoogle Scholar
  27. North TE, Goessling W, Peeters M, Li P, Ceol C, Lord AM, Weber GJ, Harris J, Cutting CC, Huang P et al (2009) Hematopoietic stem cell development is dependent on blood flow. Cell 137:736–748PubMedCentralPubMedGoogle Scholar
  28. Paik EJ, de Jong JLO, Pugach E, Opara P, Zon LI (2010) A chemical genetic screen in zebrafish for pathways interacting with cdx4 in primitive hematopoiesis. Zebrafish 7:61–68PubMedCentralPubMedGoogle Scholar
  29. Papalopulu N, Clarke JD, Bradley L, Wilkinson D, Krumlauf R, Holder N (1991) Retinoic acid causes abnormal development and segmental patterning of the anterior hindbrain in Xenopus embryos. Development 113:1145–1158PubMedGoogle Scholar
  30. Patton EE, Widlund HR, Kutok JL, Kopani KR, Amatruda JF, Murphey RD, Berghmans S, Mayhall EA, Traver D, Fletcher CDM et al (2005) BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr Biol 15:249–254PubMedGoogle Scholar
  31. Peterson RT, Link BA, Dowling JE, Schreiber SL (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc Natl Acad Sci U S A 97:12965–12969PubMedCentralPubMedGoogle Scholar
  32. Ridges S, Heaton WL, Joshi D, Choi H, Eiring A, Batchelor L, Choudhry P, Manos EJ, Sofla H, Sanati A et al (2012) Zebrafish screen identifies novel compound with selective toxicity against leukemia. Blood 119:5621–5631PubMedCentralPubMedGoogle Scholar
  33. Rovira M, Huang W, Yusuff S, Shim JS, Ferrante AA, Liu JO, Parsons MJ (2011) Chemical screen identifies FDA-approved drugs and target pathways that induce precocious pancreatic endocrine differentiation. Proc Natl Acad Sci U S A 108:19264–19269PubMedCentralPubMedGoogle Scholar
  34. Sachidanandan C, Yeh J-RJ, Peterson QP, Peterson RT (2008) Identification of a novel retinoid by small molecule screening with zebrafish embryos. PLoS One 3:ple1–ple9, e1947Google Scholar
  35. Sandoval IT, Manos EJ, Van Wagoner RM, Delacruz RGC, Edes K, Winge DR, Ireland CM, Jones DA (2013) Juxtaposition of chemical and mutation-induced developmental defects in zebrafish reveal a copper-chelating activity for kalihinol F. Chem Biol 20:753–763PubMedCentralPubMedGoogle Scholar
  36. Santoriello C, Gennaro E, Anelli V, Distel M, Kelly A, Köster RW, Hurlstone A, Mione M (2010) Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PLoS One 5:e15170PubMedCentralPubMedGoogle Scholar
  37. Saydmohammed M, Vollmer LL, Onuoha EO, Vogt A, Tsang M (2011) A high-content screening assay in transgenic zebrafish identifies two novel activators of fgf signaling. Birth Defects Res C Embryo Today 93:281–287PubMedCentralPubMedGoogle Scholar
  38. Stachel SE, Grunwald DJ, Myers PZ (1993) Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 117:1261–1274PubMedGoogle Scholar
  39. Sugiyama M, Sakaue-Sawano A, Iimura T, Fukami K, Kitaguchi T, Kawakami K, Okamoto H, Higashijima S, Miyawaki A (2009) Illuminating cell-cycle progression in the developing zebrafish embryo. Proc Natl Acad Sci U S A 106:20812–20817PubMedCentralPubMedGoogle Scholar
  40. Terriente J, Pujades C (2013) Use of zebrafish embryos for small molecule screening related to cancer. Dev Dyn 242:97–107PubMedGoogle Scholar
  41. Thisse C, Thisse B (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3:59–69PubMedGoogle Scholar
  42. Tran TC, Sneed B, Haider J, Blavo D, White A, Aiyejorun T, Baranowski TC, Rubinstein AL, Doan TN, Dingledine R et al (2007a) Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish. Cancer Res 67:11386–11392PubMedGoogle Scholar
  43. Tsuji N, Ninov N, Delawary M, Osman S, Roh AS, Gut P, Stainier DYR (2014) Whole organism high content screening identifies stimulators of pancreatic beta-cell proliferation. PLoS One 9:e104112PubMedCentralPubMedGoogle Scholar
  44. Wang C, Tao W, Wang Y, Bikow J, Lu B, Keating A, Verma S, Parker TG, Han R, Wen X-Y (2010) Rosuvastatin, identified from a zebrafish chemical genetic screen for antiangiogenic compounds, suppresses the growth of prostate cancer. Eur Urol 58:418–426PubMedGoogle Scholar
  45. White RM, Cech J, Ratanasirintrawoot S, Lin CY, Rahl PB, Burke CJ, Langdon E, Tomlinson ML, Mosher J, Kaufman C et al (2011) DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 471:518–522PubMedCentralPubMedGoogle Scholar
  46. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A, Price E, Liu M, Barton ER, Kahn CR et al (2013a) A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909–921PubMedCentralPubMedGoogle Scholar
  47. Yeh J-RJ, Munson KM, Elagib KE, Goldfarb AN, Sweetser DA, Peterson RT (2009) Discovering chemical modifiers of oncogene-regulated hematopoietic differentiation. Nat Chem Biol 5:236–243PubMedCentralPubMedGoogle Scholar
  48. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, Lin HY, Bloch KD, Peterson RT (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4:33–41PubMedCentralPubMedGoogle Scholar
  49. Zhang Z-R, Li J-H, Li S, Liu A-L, Hoi P-M, Tian H-Y, Ye W-C, Lee SM-Y, Jiang R-W (2014a) In vivo angiogenesis screening and mechanism of action of novel tanshinone derivatives produced by one-pot combinatorial modification of natural tanshinone mixture from Salvia miltiorrhiza. PLoS One 9:e100416PubMedCentralPubMedGoogle Scholar
  50. Zhou L, Ishizaki H, Spitzer M, Taylor KL, Temperley ND, Johnson SL, Brear P, Gautier P, Zeng Z, Mitchell A et al (2012) ALDH2 mediates 5-nitrofuran activity in multiple species. Chem Biol 19:883–892PubMedCentralPubMedGoogle Scholar

Fin Regeneration

  1. Andreasen EA, Mathew L, Tanguay RL (2006) Regenerative growth is impacted by TCDD: gene expression analysis reveals extracellular matrix modulation. Toxicol Sci 92(1):254–269PubMedGoogle Scholar
  2. Andreasen EA, Mathew LK, Löhr CV, Hasson R, Tanguay RL (2007) Aryl hydrocarbon receptor activation impairs extracellular matrix remodeling during zebra fish fin regeneration. Toxicol Sci 95:215–226PubMedGoogle Scholar
  3. Bayliss PE, Bellavance KL, Whitehead GG, Abrams JM, Aegerter S, Robbins HS, Cowan DB, Keating MT, O’Reilly T, Wood JM et al (2006) Chemical modulation of receptor signaling inhibits regenerative angiogenesis in adult zebrafish. Nat Chem Biol 2:265–273PubMedCentralPubMedGoogle Scholar
  4. Gemberling M, Bailey TJ, Hyde DR, Poss KD (2013) The zebrafish as a model for complex tissue regeneration. Trends Genet 29:611–620PubMedGoogle Scholar
  5. Goessling W, North TE (2014) Repairing quite swimmingly: advances in regenerative medicine using zebrafish. Dis Model Mech 7:769–776PubMedCentralPubMedGoogle Scholar
  6. Jaźwińska A, Badakov R, Keating MT (2007) Activin-betaA signaling is required for zebrafish fin regeneration. Curr Biol 17:1390–1395PubMedGoogle Scholar
  7. Johnson SL, Weston JA (1995) Temperature-sensitive mutations that cause stage-specific defects in zebrafish fin regeneration. Genetics 141:1583–1595PubMedCentralPubMedGoogle Scholar
  8. Kawakami A, Fukazawa T, Takeda H (2004) Early fin primordia of zebrafish larvae regenerate by a similar growth control mechanism with adult regeneration. Dev Dyn 231(4):693–699PubMedGoogle Scholar
  9. Mathew LK, Andreasen EA, Tanguay RL (2006) Aryl hydrocarbon receptor activation inhibits regenerative growth. Mol Pharmacol 69:257–265PubMedGoogle Scholar
  10. Mathew LK, Sengupta S, Kawakami A, Andreasen EA, Löhr CV, Loynes CA, Renshaw SA, Peterson RT, Tanguay RL (2007b) Unraveling tissue regeneration pathways using chemical genetics. J Biol Chem 282:35202–35210PubMedGoogle Scholar
  11. Moon H-Y, Kim O-H, Kim H-T, Choi J-H, Yeo S-Y, Kim N-S, Park D-S, Oh H-W, You K-H, De Zoysa M et al (2013) Establishment of a transgenic zebrafish EF1α:Kaede for monitoring cell proliferation during regeneration. Fish Shellfish Immunol 34:1390–1394PubMedGoogle Scholar
  12. Niethammer P, Grabher C, Look AT, Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996–999PubMedCentralPubMedGoogle Scholar
  13. O’Donnell EF, Saili KS, Koch DC, Kopparapu PR, Farrer D, Bisson WH, Mathew LK, Sengupta S, Kerkvliet NI, Tanguay RL et al (2010) The anti-inflammatory drug leflunomide is an agonist of the aryl hydrocarbon receptor. PLoS One 5:e13128PubMedCentralPubMedGoogle Scholar
  14. Oppedal D, Goldsmith MI (2010) A chemical screen to identify novel inhibitors of fin regeneration in zebrafish. Zebrafish 7:53–60PubMedCentralPubMedGoogle Scholar
  15. Poss KD, Shen J, Nechiporuk A, McMahon G, Thisse B, Thisse C, Keating MT (2000) Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol 222:347–358PubMedGoogle Scholar
  16. Rieger S, Sagasti A (2011) Hydrogen peroxide promotes injury-induced peripheral sensory axon regeneration in the zebrafish skin. PLoS Biol 9:e1000621PubMedCentralPubMedGoogle Scholar
  17. Smith A, Avaron F, Guay D, Padhi BK, Akimenko MA (2006) Inhibition of BMP signaling during zebrafish fin regeneration disrupts fin growth and scleroblasts differentiation and function. Dev Biol 299:438–454PubMedGoogle Scholar
  18. Stoick-Cooper CL, Weidinger G, Riehle KJ, Hubbert C, Major MB, Fausto N, Moon RT (2007) Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Dev Camb Engl 134:479–489Google Scholar
  19. Whitehead GG, Makino S, Lien C-L, Keating MT (2005) fgf20 is essential for initiating zebrafish fin regeneration. Science 310:1957–1960PubMedGoogle Scholar
  20. Zodrow JM, Tanguay RL (2003) 2,3,7,8-tetrachlorodibenzo-p-dioxin inhibits zebrafish caudal fin regeneration. Toxicol Sci 76:151–161PubMedGoogle Scholar

Heart Regeneration

  1. Chablais F, Jazwinska A (2012a) The regenerative capacity of the zebrafish heart is dependent on TGFβ signaling. Dev Camb Engl 139:1921–1930Google Scholar
  2. Chablais F, Jaźwińska A (2012b) Induction of myocardial infarction in adult zebrafish using cryoinjury. J Vis Exp 62:e3666Google Scholar
  3. Choi W-Y, Gemberling M, Wang J, Holdway JE, Shen M-C, Karlstrom RO, Poss KD (2013b) In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Dev Camb Engl 140:660–666Google Scholar
  4. Dickover MS, Zhang R, Han P, Chi NC (2013) Zebrafish cardiac injury and regeneration models: a noninvasive and invasive in vivo model of cardiac regeneration. Methods Mol Biol 1037:463–473PubMedCentralPubMedGoogle Scholar
  5. González-Rosa JM, Mercader N (2012) Cryoinjury as a myocardial infarction model for the study of cardiac regeneration in the zebrafish. Nat Protoc 7:782–788PubMedGoogle Scholar
  6. Huang W-C, Yang C-C, Chen I-H, Liu Y-ML, Chang S-J, Chuang Y-J (2013a) Treatment of glucocorticoids inhibited early immune responses and impaired cardiac repair in adult zebrafish. PLoS One 8:e66613PubMedCentralPubMedGoogle Scholar
  7. Huang Y, Harrison MR, Osorio A, Kim J, Baugh A, Duan C, Sucov HM, Lien C-L (2013b) Igf signaling is required for cardiomyocyte proliferation during zebrafish heart development and regeneration. PLoS One 8:e67266PubMedCentralPubMedGoogle Scholar
  8. Itou J, Oishi I, Kawakami H, Glass TJ, Richter J, Johnson A, Lund TC, Kawakami Y (2012) Migration of cardiomyocytes is essential for heart regeneration in zebrafish. Dev Camb Engl 139:4133–4142Google Scholar
  9. Itou J, Akiyama R, Pehoski S, Yu X, Kawakami H, Kawakami Y (2014) Regenerative responses after mild heart injuries for cardiomyocyte proliferation in zebrafish. Dev Dyn 243:1477–1486PubMedGoogle Scholar
  10. Jopling C, Sleep E, Raya M, Martí M, Raya A, Izpisúa Belmonte JC (2010) Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464:606–609PubMedCentralPubMedGoogle Scholar
  11. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DYR, Poss KD (2010) Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464:601–605PubMedCentralPubMedGoogle Scholar
  12. Kim J, Rubin N, Huang Y, Tuan TL, Lien CL (2012) In vitro culture of epicardial cells from adult zebrafish heart on a fibrin matrix. Nat Protoc 7(2):247–255PubMedCentralPubMedGoogle Scholar
  13. Kim J, Wu Q, Zhang Y, Wiens KM, Huang Y, Rubin N, Shimada H, Handin RI, Chao MY, Tuan T-L et al (2010) PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc Natl Acad Sci U S A 107:17206–17210PubMedCentralPubMedGoogle Scholar
  14. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298:2188–2190PubMedGoogle Scholar
  15. Wang J, Panáková D, Kikuchi K, Holdway JE, Gemberling M, Burris JS, Singh SP, Dickson AL, Lin Y-F, Sabeh MK, Werdich AA, Yelon D, MacRae CA, Poss KD (2011) The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion. Development 138(16):3421–3430PubMedCentralPubMedGoogle Scholar
  16. Zhang R, Han P, Yang H, Ouyang K, Lee D, Lin Y-F, Ocorr K, Kang G, Chen J, Stainier DYR et al (2013) In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 498:497–501PubMedCentralPubMedGoogle Scholar
  17. Zhao L, Borikova AL, Ben-Yair R, Guner-Ataman B, MacRae CA, Lee RT, Burns CG, Burns CE (2014a) Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration. Proc Natl Acad Sci U S A 111:1403–1408PubMedCentralPubMedGoogle Scholar

Hair Cell Damage and Regeneration

  1. Chiu LL, Cunningham LL, Raible DW, Rubel EW, Ou HC (2008) Using the zebrafish lateral line to screen for ototoxicity. J Assoc Res Otolaryngol 9:178–190PubMedCentralPubMedGoogle Scholar
  2. Esterberg R, Coffin AB, Ou H, Simon JA, Raible DW, Rubel EW (2013). Fish in a dish: drug discovery for hearing habilitation. Drug Discov Today Dis Model 10(1). doi:10.1016/j.ddmod.2012.02.001Google Scholar
  3. He Y, Cai C, Tang D, Sun S, Li H (2014) Effect of histone deacetylase inhibitors trichostatin A and valproic acid on hair cell regeneration in zebrafish lateral line neuromasts. Front Cell Neurosci 8:382PubMedCentralPubMedGoogle Scholar
  4. Hernández PP, Moreno V, Olivari FA, Allende ML (2006) Sub-lethal concentrations of waterborne copper are toxic to lateral line neuromasts in zebrafish (Danio rerio). Hear Res 213:1–10PubMedGoogle Scholar
  5. Hirose Y, Simon JA, Ou HC (2011) Hair cell toxicity in anti-cancer drugs: evaluating an anti-cancer drug library for independent and synergistic toxic effects on hair cells using the zebrafish lateral line. J Assoc Res Otolaryngol 12:719–728PubMedCentralPubMedGoogle Scholar
  6. Ma EY, Rubel EW, Raible DW (2008) Notch signaling regulates the extent of hair cell regeneration in the zebrafish lateral line. J Neurosci 28:2261–2273PubMedGoogle Scholar
  7. Mackenzie SM, Raible DW (2012) Proliferative regeneration of zebrafish lateral line hair cells after different ototoxic insults. PLoS One 7:e47257PubMedCentralPubMedGoogle Scholar
  8. Moon IS, So J-H, Jung Y-M, Lee W-S, Kim EY, Choi J-H, Kim C-H, Choi JY (2011) Fucoidan promotes mechanosensory hair cell regeneration following amino glycoside-induced cell death. Hear Res 282:236–242PubMedGoogle Scholar
  9. Murakami SL, Cunningham LL, Werner LA, Bauer E, Pujol R, Raible DW, Rubel EW (2003) Developmental differences in susceptibility to neomycin-induced hair cell death in the lateral line neuromasts of zebrafish (Danio rerio). Hear Res 186:47–56PubMedGoogle Scholar
  10. Namdaran P, Reinhart KE, Owens KN, Raible DW, Rubel EW (2012) Identification of modulators of hair cell regeneration in the zebrafish lateral line. J Neurosci 32:3516–3528PubMedCentralPubMedGoogle Scholar
  11. Ou HC, Raible DW, Rubel EW (2007) Cisplatin-induced hair cell loss in zebrafish (Danio rerio) lateral line. Hear Res 233:46–53PubMedCentralPubMedGoogle Scholar
  12. Owens KN, Santos F, Roberts B, Linbo T, Coffin AB, Knisely AJ, Simon JA, Rubel EW, Raible DW (2008) Identification of genetic and chemical modulators of zebrafish mechanosensory hair cell death. PLoS Genet 4:e1000020PubMedCentralPubMedGoogle Scholar
  13. Pisano GC, Mason SM, Dhliwayo N, Intine RV, Sarras MP (2014) An assay for lateral line regeneration in adult zebrafish. J Vis Exp 86. doi:10.3791/51343Google Scholar
  14. Santos F, MacDonald G, Rubel EW, Raible DW (2006) Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hear Res 213:25–33PubMedGoogle Scholar
  15. Seiler C, Nicolson T (1999) Defective calmodulin-dependent rapid apical endocytosis in zebrafish sensory hair cell mutants. J Neurobiol 41:424–434PubMedGoogle Scholar
  16. Ton C, Parng C (2005) The use of zebrafish for assessing ototoxic and otoprotective agents. Hear Res 208:79–88PubMedGoogle Scholar
  17. Thomas AJ, Wu P, Raible DW, Rubel EW, Simon JA, Ou HC (2015) Identification of small molecule inhibitors of cisplatin-induced hair cell death: results of a 10,000 compound screen in the zebrafish lateral line. Otol Neurotol 36:519–525PubMedGoogle Scholar

Retinal Regeneration

  1. Ariga J, Walker SL, Mumm JS (2010) Multicolor time-lapse imaging of transgenic zebrafish: visualizing retinal stem cells activated by targeted neuronal cell ablation. J Vis Exp 43. pii: 2093Google Scholar
  2. Bernardos RL, Barthel LK, Meyers JR, Raymond PA (2007) Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J Neurosci 27:7028–7040PubMedGoogle Scholar
  3. Cameron DA (2000) Cellular proliferation and neurogenesis in the injured retina of adult zebrafish. Vis Neurosci 17:789–797PubMedGoogle Scholar
  4. Fimbel SM, Montgomery JE, Burket CT, Hyde DR (2007) Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J Neurosci 27:1712–1724PubMedGoogle Scholar
  5. Fraser B, DuVal MG, Wang H, Allison WT (2013) Regeneration of cone photoreceptors when cell ablation is primarily restricted to a particular cone subtype. PLoS One 8:e55410PubMedCentralPubMedGoogle Scholar
  6. Goldman D (2014) Müller glial cell reprogramming and retina regeneration. Nat Rev Neurosci 15:431–442PubMedCentralPubMedGoogle Scholar
  7. Hitchcock PF, Lindsey Myhr KJ, Easter SS, Mangione-Smith R, Jones DD (1992) Local regeneration in the retina of the goldfish. J Neurobiol 23:187–203PubMedGoogle Scholar
  8. Lenkowski JR, Qin Z, Sifuentes CJ, Thummel R, Soto CM, Moens CB, Raymond PA (2013) Retinal regeneration in adult zebrafish requires regulation of TGFβ signaling. Glia 61:1687–1697PubMedCentralPubMedGoogle Scholar
  9. Montgomery JE, Parsons MJ, Hyde DR (2010) A novel model of retinal ablation demonstrates that the extent of rod cell death regulates the origin of the regenerated zebrafish rod photoreceptors. J Comp Neurol 18(6):800–814Google Scholar
  10. Meyers JR, Hu L, Moses A, Kaboli K, Papandrea A, Raymond PA (2012) β-catenin/Wnt signaling controls progenitor fate in the developing and regenerating zebrafish retina. Neural Dev 7:30PubMedCentralPubMedGoogle Scholar
  11. Rajaram K, Summerbell ER, Patton JG (2014a) Technical brief: constant intense light exposure to lesion and initiate regeneration in normally pigmented zebrafish. Mol Vis 20:1075–1084PubMedCentralPubMedGoogle Scholar
  12. Rajaram K, Harding RL, Hyde DR, Patton JG (2014b) miR-203 regulates progenitor cell proliferation during adult zebrafish retina regeneration. Dev Biol 392:393–403PubMedGoogle Scholar
  13. Ramachandran R, Zhao X-F, Goldman D (2011) Ascl1a/Dkk/beta-catenin signaling pathway is necessary and glycogen synthase kinase-3beta inhibition is sufficient for zebrafish retina regeneration. Proc Natl Acad Sci U S A 108:15858–15863PubMedCentralPubMedGoogle Scholar
  14. Raymond PA, Reifler MJ, Rivlin PK (1988) Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol 19:431–463PubMedGoogle Scholar
  15. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev Biol 6:36PubMedCentralPubMedGoogle Scholar
  16. Senut M-C, Gulati-Leekha A, Goldman D (2004) An element in the alpha1-tubulin promoter is necessary for retinal expression during optic nerve regeneration but not after eye injury in the adult zebrafish. J Neurosci 24:7663–7673PubMedGoogle Scholar
  17. Sherpa T, Fimbel SM, Mallory DE, Maaswinkel H, Spritzer SD, Sand JA, Li L, Hyde DR, Stenkamp DL (2008) Ganglion cell regeneration following whole-retina destruction in zebrafish. Dev Neurobiol 68:166–181PubMedCentralPubMedGoogle Scholar
  18. Taylor S, Chen J, Luo J, Hitchcock P (2012a) Light-induced photoreceptor degeneration in the retina of the zebrafish. Methods Mol Biol Clifton NJ 884:247–254Google Scholar
  19. Vihtelic TS, Hyde DR (2000) Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol 44:289–307PubMedGoogle Scholar
  20. Wan J, Zhao X-F, Vojtek A, Goldman D (2014) Retinal injury, growth factors, and cytokines converge on β-catenin and pStat3 signaling to stimulate retina regeneration. Cell Rep 9:285–297PubMedCentralPubMedGoogle Scholar
  21. Zhao X-F, Wan J, Powell C, Ramachandran R, Myers MG, Goldman D (2014b) Leptin and IL-6 family cytokines synergize to stimulate Müller glia reprogramming and retina regeneration. Cell Rep 9:272–284PubMedCentralPubMedGoogle Scholar

Spinal Cord Regeneration

  1. Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 377:577–595PubMedGoogle Scholar
  2. Dias TB, Yang Y-J, Ogai K, Becker T, Becker CG (2012) Notch signaling controls generation of motor neurons in the lesioned spinal cord of adult zebrafish. J Neurosci 32:3245–3252PubMedGoogle Scholar
  3. Goldshmit Y, Sztal TE, Jusuf PR, Hall TE, Nguyen-Chi M, Currie PD (2012) Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J Neurosci 32:7477–7492PubMedGoogle Scholar
  4. Reimer MM, Sörensen I, Kuscha V, Frank RE, Liu C, Becker CG, Becker T (2008) Motor neuron regeneration in adult zebrafish. J Neurosci 28:8510–8516PubMedGoogle Scholar
  5. Reimer MM, Kuscha V, Wyatt C, Sörensen I, Frank RE, Knüwer M, Becker T, Becker CG (2009) Sonic hedgehog is a polarized signal for motor neuron regeneration in adult zebrafish. J Neurosci 29:15073–15082PubMedCentralPubMedGoogle Scholar
  6. Reimer MM, Norris A, Ohnmacht J, Patani R, Zhong Z, Dias TB, Kuscha V, Scott AL, Chen Y-C, Rozov S et al (2013) Dopamine from the brain promotes spinal motor neuron generation during development and adult regeneration. Dev Cell 25:478–491PubMedGoogle Scholar

Brain Puncture Injury and Regeneration

  1. Kizil C, Kaslin J, Kroehne V, Brand M (2012a) Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol 72:429–461PubMedGoogle Scholar
  2. Kizil C, Dudczig S, Kyritsis N, Machate A, Blaesche J, Kroehne V, Brand M (2012b) The chemokine receptor cxcr5 regulates the regenerative neurogenesis response in the adult zebrafish brain. Neural Dev 7:27PubMedCentralPubMedGoogle Scholar
  3. Kizil C, Kyritsis N, Dudczig S, Kroehne V, Freudenreich D, Kaslin J, Brand M (2012c) Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of Gata3. Dev Cell 23:1230–1237PubMedGoogle Scholar
  4. Kroehne V, Freudenreich D, Hans S, Kaslin J, Brand M (2011) Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors. Dev Camb Engl 138:4831–4841Google Scholar
  5. Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J, Freudenreich D, Iltzsche A, Brand M (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338:1353–1356PubMedGoogle Scholar
  6. März M, Schmidt R, Rastegar S, Strähle U (2011) Regenerative response following stab injury in the adult zebrafish telencephalon. Dev Dyn 240:2221–2231PubMedGoogle Scholar
  7. Morcos PA, Li Y, Jiang S (2008) Vivo-morpholinos: a non-peptide transporter delivers morpholinos into a wide array of mouse tissues. Biotechniques 45:613–614, 616, 618 passimPubMedGoogle Scholar
  8. Schmidt R, Beil T, Strähle U, Rastegar S (2014) Stab wound injury of the zebrafish adult telencephalon: a method to investigate vertebrate brain neurogenesis and regeneration. J Vis Exp 90:e51753PubMedGoogle Scholar

Birefringence

  1. Bassett DI, Bryson-Richardson RJ, Daggett DF, Gautier P, Keenan DG, Currie PD (2003) Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 130:5851–5860PubMedGoogle Scholar
  2. Berger J, Sztal T, Currie PD (2012) Quantification of birefringence readily measures the level of muscle damage in zebrafish. Biochem Biophys Res Commun 423:785–788PubMedGoogle Scholar
  3. Gibbs EM, Horstick EJ, Dowling JJ (2013) Swimming into prominence: the zebrafish as a valuable tool for studying human myopathies and muscular dystrophies. FEBS J 280:4187–4197PubMedCentralPubMedGoogle Scholar
  4. Goody MF, Kelly MW, Reynolds CJ, Khalil A, Crawford BD, Henry CA (2012) NAD+ biosynthesis ameliorates a zebrafish model of muscular dystrophy. PLoS Biol 10:e1001409PubMedCentralPubMedGoogle Scholar
  5. Guyon JR, Mosley AN, Zhou Y, O’Brien KF, Sheng X, Chiang K, Davidson AJ, Volinski JM, Zon LI, Kunkel LM (2003) The dystrophin associated protein complex in zebrafish. Hum Mol Genet 12:601–615PubMedGoogle Scholar
  6. Guyon JR, Goswami J, Jun SJ, Thorne M, Howell M, Pusack T, Kawahara G, Steffen LS, Galdzicki M, Kunkel LM (2009) Genetic isolation and characterization of a splicing mutant of zebrafish dystrophin. Hum Mol Genet 18:202–211PubMedCentralPubMedGoogle Scholar
  7. Hall TE, Bryson-Richardson RJ, Berger S, Jacoby AS, Cole NJ, Hollway GE, Berger J, Currie PD (2007) The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin alpha2-deficient congenital muscular dystrophy. Proc Natl Acad Sci U S A 104:7092–7097PubMedCentralPubMedGoogle Scholar
  8. Johnson NM, Farr GH, Maves L (2013) The HDAC inhibitor TSA ameliorates a zebrafish model of Duchenne muscular dystrophy. PLoS Curr 5. pii: ecurrents.md.8273cf41db10e2d15dd3ab827cb4b027Google Scholar
  9. Kawahara G, Guyon JR, Nakamura Y, Kunkel LM (2010) Zebrafish models for human FKRP muscular dystrophies. Hum Mol Genet 19:623–633PubMedCentralPubMedGoogle Scholar
  10. Kawahara G, Karpf JA, Myers JA, Alexander MS, Guyon JR, Kunkel LM (2011) Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 108:5331–5336PubMedCentralPubMedGoogle Scholar
  11. Kawahara G, Kunkel LM (2013) Zebrafish based small molecule screens for novel DMD drugs. Drug Discov Today Technol 10:e91–e96PubMedCentralGoogle Scholar
  12. Kawahara G, Gasperini MJ, Myers JA, Widrick JJ, Eran A, Serafini PR, Alexander MS, Pletcher MT, Morris CA, Kunkel LM (2014) Dystrophic muscle improvement in zebrafish via increased heme oxygenase signaling. Hum Mol Genet 23:1869–1878PubMedCentralPubMedGoogle Scholar
  13. Li M, Andersson-Lendahl M, Sejersen T, Arner A (2014) Muscle dysfunction and structural defects of dystrophin-null sapje mutant zebrafish larvae are rescued by ataluren treatment. FASEB J 28:1593–1599PubMedGoogle Scholar
  14. Maves L (2014) Recent advances using zebrafish animal models for muscle disease drug discovery. Expert Opin Drug Discov 9:1033–1045PubMedGoogle Scholar
  15. Mitsuhashi H, Mitsuhashi S, Lynn-Jones T, Kawahara G, Kunkel LM (2013) Expression of DUX4 in zebrafish development recapitulates facioscapulohumeral muscular dystrophy. Hum Mol Genet 22:568–577PubMedCentralPubMedGoogle Scholar
  16. Smith LL, Beggs AH, Gupta VA (2013) Analysis of skeletal muscle defects in larval zebrafish by birefringence and touch-evoke escape response assays. J Vis Exp 82:e50925PubMedGoogle Scholar
  17. Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, Ladner KJ, Guttridge D, Yang J, Harper SQ (2011) DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann Neurol 69:540–552PubMedCentralPubMedGoogle Scholar
  18. Winder SJ, Lipscomb L, Angela Parkin C, Juusola M (2011) The proteasomal inhibitor MG132 prevents muscular dystrophy in zebrafish. PLoS Curr 3:RRN1286PubMedCentralPubMedGoogle Scholar
  19. Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A, Price E, Liu M, Barton ER, Kahn CR et al (2013b) A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909–921PubMedCentralPubMedGoogle Scholar

Foetal Alcohol Syndrome

  1. Ali S, Champagne DL, Alia A, Richardson MK (2011a) Large-scale analysis of acute ethanol exposure in zebrafish development: a critical time window and resilience. PLoS One 6:e20037PubMedCentralPubMedGoogle Scholar
  2. Arenzana FJ, Carvan MJ, Aijón J, Sánchez-González R, Arévalo R, Porteros A (2006) Teratogenic effects of ethanol exposure on zebrafish visual system development. Neurotoxicol Teratol 28:342–348PubMedGoogle Scholar
  3. Bilotta J, Saszik S, Givin CM, Hardesty HR, Sutherland SE (2002a) Effects of embryonic exposure to ethanol on zebrafish visual function. Neurotoxicol Teratol 24:759–766PubMedGoogle Scholar
  4. Buske C, Gerlai R (2011a) Early embryonic ethanol exposure impairs shoaling and the dopaminergic and serotoninergic systems in adult zebrafish. Neurotoxicol Teratol 33:698–707PubMedCentralPubMedGoogle Scholar
  5. Carvan MJ, Loucks E, Weber DN, Williams FE (2004) Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicol Teratol 26:757–768PubMedGoogle Scholar
  6. Dlugos CA, Rabin RA (2010) Structural and functional effects of developmental exposure to ethanol on the zebrafish heart. Alcohol Clin Exp Res 34:1013–1021PubMedGoogle Scholar
  7. Fernandes Y, Gerlai R (2009a) Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcohol Clin Exp Res 33:601–609PubMedCentralPubMedGoogle Scholar
  8. Flentke GR, Klingler RH, Tanguay RL, Carvan MJ, Smith SM (2014) An evolutionarily conserved mechanism of calcium-dependent neurotoxicity in a zebrafish model of fetal alcohol spectrum disorders. Alcohol Clin Exp Res 38:1255–1265PubMedCentralPubMedGoogle Scholar
  9. Li Y-X, Yang H-T, Zdanowicz M, Sicklick JK, Qi Y, Camp TJ, Diehl AM (2007) Fetal alcohol exposure impairs Hedgehog cholesterol modification and signaling. Lab Invest 87:231–240PubMedGoogle Scholar
  10. Lockwood B, Bjerke S, Kobayashi K, Guo S (2004) Acute effects of alcohol on larval zebrafish: a genetic system for large-scale screening. Pharmacol Biochem Behav 77:647–654PubMedGoogle Scholar
  11. Mahabir S, Chatterjee D, Gerlai R (2014) Strain dependent neurochemical changes induced by embryonic alcohol exposure in zebrafish. Neurotoxicol Teratol 41:1–7PubMedCentralPubMedGoogle Scholar
  12. Marrs JA, Clendenon SG, Ratcliffe DR, Fielding SM, Liu Q, Bosron WF (2010) Zebrafish fetal alcohol syndrome model: effects of ethanol are rescued by retinoic acid supplement. Alcohol 44:707–715PubMedCentralPubMedGoogle Scholar
  13. McCarthy N, Wetherill L, Lovely CB, Swartz ME, Foroud TM, Eberhart JK (2013) Pdgfra protects against ethanol-induced craniofacial defects in a zebrafish model of FASD. Development 140:3254–3265PubMedCentralPubMedGoogle Scholar
  14. Sarmah S, Muralidharan P, Curtis CL, McClintick JN, Buente BB, Holdgrafer DJ, Ogbeifun O, Olorungbounmi OC, Patino L, Lucas R et al (2013) Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects. Biol Open 2:1013–1021PubMedCentralPubMedGoogle Scholar
  15. Swartz ME, Wells MB, Griffin M, McCarthy N, Lovely CB, McGurk P, Rozacky J, Eberhart JK (2014) A screen of zebrafish mutants identifies ethanol-sensitive genetic loci. Alcohol Clin Exp Res 38:694–703PubMedCentralPubMedGoogle Scholar
  16. Zhang C, Frazier JM, Chen H, Liu Y, Lee J-A, Cole GJ (2014b) Molecular and morphological changes in zebrafish following transient ethanol exposure during defined developmental stages. Neurotoxicol Teratol 44:70–80PubMedGoogle Scholar

Heart Rate

  1. Berghmans S, Butler P, Goldsmith P, Waldron G, Gardner I, Golder Z, Richards FM, Kimber G, Roach A, Alderton W et al (2008a) Zebrafish based assays for the assessment of cardiac, visual and gut function–potential safety screens for early drug discovery. J Pharmacol Toxicol Methods 58:59–68PubMedGoogle Scholar
  2. Burns CG, Milan DJ, Grande EJ, Rottbauer W, MacRae CA, Fishman MC (2005) High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat Chem Biol 1:263–264PubMedGoogle Scholar
  3. Chan PK, Lin CC, Cheng SH (2009) Noninvasive technique for measurement of heartbeat regularity in zebrafish (Danio rerio) embryos. BMC Biotechnol 9:11PubMedCentralPubMedGoogle Scholar
  4. Craig MP, Gilday SD, Hove JR (2006) Dose-dependent effects of chemical immobilization on the heart rate of embryonic zebrafish. Lab Anim (NY) 35:41–47Google Scholar
  5. De Luca E, Zaccaria GM, Hadhoud M, Rizzo G, Ponzini R, Morbiducci U, Santoro MM (2014) ZebraBeat: a flexible platform for the analysis of the cardiac rate in zebrafish embryos. Sci Rep. doi:10.1038/srep04898Google Scholar
  6. Freeman JL, Weber GJ, Peterson SM, Nie LH (2014) Embryonic ionizing radiation exposure results in expression alterations of genes associated with cardiovascular and neurological development, function, and disease and modified cardiovascular function in zebrafish. Front Genet 5:268PubMedCentralPubMedGoogle Scholar
  7. Lai Y-C, Chang W-T, Lin K-Y, Liau I (2014) Optical assessment of the cardiac rhythm of contracting cardiomyocytes in vitro and a pulsating heart in vivo for pharmacological screening. Biomed Opt Express 5:1616–1625PubMedCentralPubMedGoogle Scholar
  8. Langheinrich U, Vacun G, Wagner T (2003) Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. Toxicol Appl Pharmacol 193:370–382PubMedGoogle Scholar
  9. Mickoleit M, Schmid B, Weber M, Fahrbach FO, Hombach S, Reischauer S, Huisken J (2014) High-resolution reconstruction of the beating zebrafish heart. Nat Methods 11:919–922PubMedGoogle Scholar
  10. Milan DJ, Peterson TA, Ruskin JN, Peterson RT, MacRae CA (2003) Drugs that induce repolarization abnormalities cause bradycardia in zebrafish. Circulation 107:1355–1358PubMedGoogle Scholar
  11. Miller S, Pollack J, Bradshaw J, Kumai Y, Perry SF (2014) Cardiac responses to hypercapnia in larval zebrafish (Danio rerio): the links between CO2 chemoreception, catecholamines and carbonic anhydrase. J Exp Biol 217:3569–3578PubMedGoogle Scholar
  12. Mittelstadt SW, Hemenway CL, Craig MP, Hove JR (2008) Evaluation of zebrafish embryos as a model for assessing inhibition of hERG. J Pharmacol Toxicol Methods 57:100–105PubMedGoogle Scholar
  13. Parker T, Libourel P-A, Hetheridge MJ, Cumming RI, Sutcliffe TP, Goonesinghe AC, Ball JS, Owen SF, Chomis Y, Winter MJ (2014a) A multi-endpoint in vivo larval zebrafish (Danio rerio) model for the assessment of integrated cardiovascular function. J Pharmacol Toxicol Methods 69:30–38PubMedGoogle Scholar
  14. Peal DS, Mills RW, Lynch SN, Mosley JM, Lim E, Ellinor PT, January CT, Peterson RT, Milan DJ (2011a) Novel chemical suppressors of long QT syndrome identified by an in vivo functional screen. Circulation 123:23–30PubMedCentralPubMedGoogle Scholar
  15. Rana N, Moond M, Marthi A, Bapatla S, Sarvepalli T, Chatti K, Challa AK (2010) Caffeine-induced effects on heart rate in zebrafish embryos and possible mechanisms of action: an effective system for experiments in chemical biology. Zebrafish 7:69–81PubMedGoogle Scholar
  16. Sabeh MK, Kekhia H, Macrae CA (2012) Optical mapping in the developing zebrafish heart. Pediatr Cardiol 33:916–922PubMedGoogle Scholar
  17. Santoriello C, Zon LI (2012) Hooked! Modeling human disease in zebrafish. J Clin Invest 122:2337–2343PubMedCentralPubMedGoogle Scholar
  18. Yozzo KL, Isales GM, Raftery TD, Volz DC (2013a) High-content screening assay for identification of chemicals impacting cardiovascular function in zebrafish embryos. Environ Sci Technol 47:11302–11310PubMedGoogle Scholar

Circulation and Blood Vessel Formation

  1. Han L, Yuan Y, Zhao L, He Q, Li Y, Chen X, Liu X, Liu K (2012) Tracking antiangiogenic components from Glycyrrhiza uralensis Fisch. based on zebrafish assays using high-speed countercurrent chromatography. J Sep Sci 35:1167–1172PubMedGoogle Scholar
  2. Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307–318PubMedGoogle Scholar
  3. Leet JK, Lindberg CD, Bassett LA, Isales GM, Yozzo KL, Raftery TD, Volz DC (2014) High-content screening in zebrafish embryos identifies butafenacil as a potent inducer of anemia. PLoS One 9:e104190PubMedCentralPubMedGoogle Scholar
  4. Parker T, Libourel P-A, Hetheridge MJ, Cumming RI, Sutcliffe TP, Goonesinghe AC, Ball JS, Owen SF, Chomis Y, Winter MJ (2014b) A multi-endpoint in vivo larval zebrafish (Danio rerio) model for the assessment of integrated cardiovascular function. J Pharmacol Toxicol Methods 69:30–38PubMedGoogle Scholar
  5. Peterson RT, Shaw SY, Peterson TA, Milan DJ, Zhong TP, Schreiber SL, MacRae CA, Fishman MC (2004) Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat Biotechnol 22:595–599PubMedGoogle Scholar
  6. Tran TC, Sneed B, Haider J, Blavo D, White A, Aiyejorun T, Baranowski TC, Rubinstein AL, Doan TN, Dingledine R et al (2007b) Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish. Cancer Res 67:11386–11392PubMedGoogle Scholar
  7. Watkins SC, Maniar S, Mosher M, Roman BL, Tsang M, St Croix CM (2012) High resolution imaging of vascular function in zebrafish. PLoS One 7:e44018PubMedCentralPubMedGoogle Scholar
  8. Watson O, Novodvorsky P, Gray C, Rothman AMK, Lawrie A, Crossman DC, Haase A, McMahon K, Gering M, Van Eeden FJM et al (2013) Blood flow suppresses vascular Notch signalling via dll4 and is required for angiogenesis in response to hypoxic signalling. Cardiovasc Res 100:252–261PubMedCentralPubMedGoogle Scholar
  9. Weinstein BM, Stemple DL, Driever W, Fishman MC (1995) Gridlock, a localized heritable vascular patterning defect in the zebrafish. Nat Med 1:1143–1147PubMedGoogle Scholar
  10. Yozzo KL, Isales GM, Raftery TD, Volz DC (2013b) High-content screening assay for identification of chemicals impacting cardiovascular function in zebrafish embryos. Environ Sci Technol 47:11302–11310PubMedGoogle Scholar

Larval Electrocardiogram

  1. Arnaout R, Ferrer T, Huisken J, Spitzer K, Stainier DYR, Tristani-Firouzi M, Chi NC (2007a) Zebrafish model for human long QT syndrome. Proc Natl Acad Sci U S A 104:11316–11321PubMedCentralPubMedGoogle Scholar
  2. Dhillon SS, Dóró E, Magyary I, Egginton S, Sík A, Müller F (2013) Optimisation of embryonic and larval ECG measurement in zebrafish for quantifying the effect of QT prolonging drugs. PLoS One 8:e60552PubMedCentralPubMedGoogle Scholar
  3. Huttner IG, Trivedi G, Jacoby A, Mann SA, Vandenberg JI, Fatkin D (2013) A transgenic zebrafish model of a human cardiac sodium channel mutation exhibits bradycardia, conduction-system abnormalities and early death. J Mol Cell Cardiol 61:123–132PubMedGoogle Scholar
  4. Yu F, Huang J, Adlerz K, Jadvar H, Hamdan MH, Chi N, Chen J-N, Hsiai TK (2010a) Evolving cardiac conduction phenotypes in developing zebrafish larvae: implications to drug sensitivity. Zebrafish 7:325–331PubMedCentralPubMedGoogle Scholar

Adult Electrocardiogram

  1. Arnaout R, Ferrer T, Huisken J, Spitzer K, Stainier DYR, Tristani-Firouzi M, Chi NC (2007b) Zebrafish model for human long QT syndrome. Proc Natl Acad Sci U S A 104:11316–11321PubMedCentralPubMedGoogle Scholar
  2. Chaudhari GH, Chennubhotla KS, Chatti K, Kulkarni P (2013) Optimization of the adult zebrafish ECG method for assessment of drug-induced QTc prolongation. J Pharmacol Toxicol Methods 67:115–120PubMedGoogle Scholar
  3. Milan DJ, Jones IL, Ellinor PT, MacRae CA (2006) In vivo recording of adult zebrafish electrocardiogram and assessment of drug-induced QT prolongation. Am J Physiol Heart Circ Physiol 291:H269–H273PubMedGoogle Scholar
  4. Sun P, Zhang Y, Yu F, Parks E, Lyman A, Wu Q, Ai L, Hu C-H, Zhou Q, Shung K et al (2009) Micro-electrocardiograms to study post-ventricular amputation of zebrafish heart. Ann Biomed Eng 37:890–901PubMedGoogle Scholar
  5. Yu F, Li R, Parks E, Takabe W, Hsiai TK (2010b) Electrocardiogram signals to assess zebrafish heart regeneration: implication of long QT intervals. Ann Biomed Eng 38:2346–2357PubMedCentralPubMedGoogle Scholar

Action Potential Recording

  1. Alday A, Alonso H, Gallego M, Urrutia J, Letamendia A, Callol C, Casis O (2014) Ionic channels underlying the ventricular action potential in zebrafish embryo. Pharmacol Res 84:26–31PubMedGoogle Scholar
  2. Arnaout R, Ferrer T, Huisken J, Spitzer K, Stainier DYR, Tristani-Firouzi M, Chi NC (2007c) Zebrafish model for human long QT syndrome. Proc Natl Acad Sci U S A 104:11316–11321PubMedCentralPubMedGoogle Scholar
  3. Bazett H (1920) An analysis of the time-relations of electrocardiograms. Heart 7:353–370Google Scholar
  4. Brette F, Luxan G, Cros C, Dixey H, Wilson C, Shiels HA (2008) Characterization of isolated ventricular myocytes from adult zebrafish (Danio rerio). Biochem Biophys Res Commun 374:143–146PubMedCentralPubMedGoogle Scholar
  5. Jou CJ, Spitzer KW, Tristani-Firouzi M (2010) Blebbistatin effectively uncouples the excitation-contraction process in zebrafish embryonic heart. Cell Physiol Biochem 25:419–424PubMedCentralPubMedGoogle Scholar
  6. Kovács M, Tóth J, Hetényi C, Málnási-Csizmadia A, Sellers JR (2004a) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279:35557–35563PubMedGoogle Scholar
  7. Nemtsas P, Wettwer E, Christ T, Weidinger G, Ravens U (2010) Adult zebrafish heart as a model for human heart? An electrophysiological study. J Mol Cell Cardiol 48:161–171PubMedGoogle Scholar
  8. Tsai C-T, Wu C-K, Chiang F-T, Tseng C-D, Lee J-K, Yu C-C, Wang Y-C, Lai L-P, Lin J-L, Hwang J-J (2011) In-vitro recording of adult zebrafish heart electrocardiogram – a platform for pharmacological testing. Clin Chim Acta 412:1963–1967PubMedGoogle Scholar

Optical Mapping

  1. Kovács M, Tóth J, Hetényi C, Málnási-Csizmadia A, Sellers JR (2004b) Mechanism of blebbistatin inhibition of myosin II. J Biol Chem 279:35557–35563PubMedGoogle Scholar
  2. Lin E, Ribeiro A, Ding W, Hove-Madsen L, Sarunic MV, Beg MF, Tibbits GF (2014) Optical mapping of the electrical activity of isolated adult zebrafish hearts: acute effects of temperature. Am J Physiol Regul Integr Comp Physiol 306:R823–R836PubMedCentralPubMedGoogle Scholar
  3. Peal DS, Mills RW, Lynch SN, Mosley JM, Lim E, Ellinor PT, January CT, Peterson RT, Milan DJ (2011b) Novel chemical suppressors of long QT syndrome identified by an in vivo functional screen. Circulation 123:23–30PubMedCentralPubMedGoogle Scholar
  4. Samson SC, Ferrer T, Jou CJ, Sachse FB, Shankaran SS, Shaw RM, Chi NC, Tristani-Firouzi M, Yost HJ (2013) 3-OST-7 regulates BMP-dependent cardiac contraction. PLoS Biol 11:e1001727PubMedCentralPubMedGoogle Scholar
  5. Sedmera D, Reckova M, deAlmeida A, Sedmerova M, Biermann M, Volejnik J, Sarre A, Raddatz E, McCarthy RA, Gourdie RG et al (2003) Functional and morphological evidence for a ventricular conduction system in zebrafish and Xenopus hearts. Am J Physiol Heart Circ Physiol 284:H1152–H1160PubMedGoogle Scholar
  6. Tsutsui H, Higashijima S, Miyawaki A, Okamura Y (2010) Visualizing voltage dynamics in zebrafish heart. J Physiol 588:2017–2021PubMedCentralPubMedGoogle Scholar

Flow Cytometry of Red Blood Cells

  1. Brownlie A, Donovan A, Pratt SJ, Paw BH, Oates AC, Brugnara C, Witkowska HE, Sassa S, Zon LI (1998) Positional cloning of the zebrafish sauternes gene: a model for congenital sideroblastic anaemia. Nat Genet 20:244–250PubMedGoogle Scholar
  2. Danilova N, Sakamoto KM, Lin S (2008) Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoiesis through activation of p53 protein family. Blood 112:5228–5237PubMedGoogle Scholar
  3. Detrich HW, Kieran MW, Chan FY, Barone LM, Yee K, Rundstadler JA, Pratt S, Ransom D, Zon LI (1995) Intraembryonic hematopoietic cell migration during vertebrate development. Proc Natl Acad Sci 92:10713–10717PubMedCentralPubMedGoogle Scholar
  4. Dooley KA, Fraenkel PG, Langer NB, Schmid B, Davidson AJ, Weber G, Chiang K, Foott H, Dwyer C, Wingert RA et al (2008) Montalcino, a zebrafish model for variegate porphyria. Exp Hematol 36:1132–1142PubMedCentralPubMedGoogle Scholar
  5. Long Q, Meng A, Wang H, Jessen JR, Farrell MJ, Lin S (1997) GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene. Development 124:4105–4111PubMedGoogle Scholar
  6. Payne EM, Virgilio M, Narla A, Sun H, Levine M, Paw BH, Berliner N, Look AT, Ebert BL, Khanna-Gupta A (2012) L-Leucine improves the anemia and developmental defects associated with Diamond-Blackfan anemia and del(5q) MDS by activating the mTOR pathway. Blood 120:2214–2224PubMedCentralPubMedGoogle Scholar
  7. Shafizadeh E, Paw BH, Foott H, Liao EC, Barut BA, Cope JJ, Zon LI, Lin S (2002) Characterization of zebrafish merlot/chablis as non-mammalian vertebrate models for severe congenital anemia due to protein 4.1 deficiency. Development 129:4359–4370PubMedGoogle Scholar
  8. Shafizadeh E, Peterson RT, Lin S (2004) Induction of reversible hemolytic anemia in living zebrafish using a novel small molecule. Comp Biochem Physiol C Toxicol Pharmacol 138:245–249PubMedGoogle Scholar
  9. Taylor AM, Humphries JM, White RM, Murphey RD, Burns CE, Zon LI (2012b) Hematopoietic defects in rps29 mutant zebrafish depend upon p53 activation. Exp Hematol 40:228–237.e5PubMedCentralPubMedGoogle Scholar
  10. Uechi T, Nakajima Y, Chakraborty A, Torihara H, Higa S, Kenmochi N (2008) Deficiency of ribosomal protein S19 during early embryogenesis leads to reduction of erythrocytes in a zebrafish model of Diamond-Blackfan anemia. Hum Mol Genet 17:3204–3211PubMedGoogle Scholar
  11. Van Rooijen E, Voest EE, Logister I, Korving J, Schwerte T, Schulte-Merker S, Giles RH, van Eeden FJ (2009) Zebrafish mutants in the von Hippel-Lindau tumor suppressor display a hypoxic response and recapitulate key aspects of Chuvash polycythemia. Blood 113:6449–6460PubMedGoogle Scholar

Video Analysis of Gut Motility

  1. Berghmans S, Butler P, Goldsmith P, Waldron G, Gardner I, Golder Z, Richards FM, Kimber G, Roach A, Alderton W et al (2008b) Zebrafish based assays for the assessment of cardiac, visual and gut function–potential safety screens for early drug discovery. J Pharmacol Toxicol Methods 58:59–68PubMedGoogle Scholar
  2. Burzynski G, Shepherd IT, Enomoto H (2009) Genetic model system studies of the development of the enteric nervous system, gut motility and Hirschsprung’s disease. Neurogastroenterol Motil 21:113–127PubMedCentralPubMedGoogle Scholar
  3. Holmberg A, Schwerte T, Pelster B, Holmgren S (2004) Ontogeny of the gut motility control system in zebrafish Danio rerio embryos and larvae. J Exp Biol 207:4085–4094PubMedGoogle Scholar
  4. Holmberg A, Olsson C, Holmgren S (2006) The effects of endogenous and exogenous nitric oxide on gut motility in zebrafish Danio rerio embryos and larvae. J Exp Biol 209:2472–2479PubMedGoogle Scholar
  5. Holmberg A, Olsson C, Hennig GW (2007) TTX-sensitive and TTX-insensitive control of spontaneous gut motility in the developing zebrafish (Danio rerio) larvae. J Exp Biol 210:1084–1091PubMedGoogle Scholar
  6. Kuhlman J, Eisen JS (2007) Genetic screen for mutations affecting development and function of the enteric nervous system. Dev Dyn 236:118–127PubMedGoogle Scholar
  7. Rich A (2009) A new high-content model system for studies of gastrointestinal transit: the zebrafish. Neurogastroenterol Motil 21:225–228PubMedGoogle Scholar
  8. Rich A, Gordon S, Brown C, Gibbons SJ, Schaefer K, Hennig G, Farrugia G (2013) Kit signaling is required for development of coordinated motility patterns in zebrafish gastrointestinal tract. Zebrafish 10:154–160PubMedCentralPubMedGoogle Scholar
  9. Roach G, Heath Wallace R, Cameron A, Emrah Ozel R, Hongay CF, Baral R, Andreescu S, Wallace KN (2013) Loss of ascl1a prevents secretory cell differentiation within the zebrafish intestinal epithelium resulting in a loss of distal intestinal motility. Dev Biol 376:171–186PubMedCentralPubMedGoogle Scholar

Intestinal Transit Assay

  1. Abrams J, Davuluri G, Seiler C, Pack M (2012) Smooth muscle caldesmon modulates peristalsis in the wild type and non-innervated zebrafish intestine. Neurogastroenterol Motil 24:288–299PubMedCentralPubMedGoogle Scholar
  2. Cocchiaro JL, Rawls JF (2013) Microgavage of zebrafish larvae. J Vis Exp 72:e4434PubMedGoogle Scholar
  3. Davuluri G, Seiler C, Abrams J, Soriano AJ, Pack M (2010) Differential effects of thin and thick filament disruption on zebrafish smooth muscle regulatory proteins. Neurogastroenterol Motil 22:1100–e285PubMedCentralPubMedGoogle Scholar
  4. Field HA, Kelley KA, Martell L, Goldstein AM, Serluca FC (2009) Analysis of gastrointestinal physiology using a novel intestinal transit assay in zebrafish. Neurogastroenterol Motil 21:304–312PubMedGoogle Scholar
  5. Zhou J, Guo S-Y, Zhang Y, Li C-Q (2014) Human prokinetic drugs promote gastrointestinal motility in zebrafish. Neurogastroenterol Motil 26:589–595PubMedGoogle Scholar

Renal Function

  1. Cao Y, Semanchik N, Lee SH, Somlo S, Barbano PE, Coifman R, Sun Z (2009) Chemical modifier screen identifies HDAC inhibitors as suppressors of PKD models. Proc Natl Acad Sci U S A 106:21819–21824PubMedCentralPubMedGoogle Scholar
  2. Cianciolo Cosentino C, Roman BL, Drummond IA, Hukriede NA (2010) Intravenous microinjections of zebrafish larvae to study acute kidney injury. J Vis Exp 42. pii: 2079Google Scholar
  3. Drummond IA (2005) Kidney development and disease in the zebrafish. J Am Soc Nephrol 16:299–304PubMedGoogle Scholar
  4. Drummond IA, Majumdar A, Hentschel H, Elger M, Solnica-Krezel L, Schier AF, Neuhauss SC, Stemple DL, Zwartkruis F, Rangini Z et al (1998) Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125:4655–4667PubMedGoogle Scholar
  5. Hentschel DM, Bonventre JV (2005) Novel non-rodent models of kidney disease. Curr Mol Med 5:537–546PubMedGoogle Scholar
  6. Hentschel DM, Park KM, Cilenti L, Zervos AS, Drummond I, Bonventre JV (2005) Acute renal failure in zebrafish: a novel system to study a complex disease. Am J Physiol Renal Physiol 288:F923–F929PubMedGoogle Scholar
  7. Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF, Drummond IA (2005) Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer’s vesicle is required for normal organogenesis. Development 132:1907–1921PubMedGoogle Scholar
  8. Swanhart LM, Cosentino CC, Diep CQ, Davidson AJ, de Caestecker M, Hukriede NA (2011) Zebrafish kidney development: basic science to translational research. Birth Defects Res Part C Embryo Today Rev 93:141–156Google Scholar
  9. Tobin JL, Beales PL (2008) Restoration of renal function in zebrafish models of ciliopathies. Pediatr Nephrol 23:2095–2099PubMedGoogle Scholar

Models of Infection and Immunity

  1. Burgos JS, Ripoll-Gomez J, Alfaro JM, Sastre I, Valdivieso F (2008) Zebrafish as a new model for herpes simplex virus type 1 infection. Zebrafish 5:323–333PubMedGoogle Scholar
  2. Carvalho R, de Sonneville J, Stockhammer OW, Savage NDL, Veneman WJ, Ottenhoff THM, Dirks RP, Meijer AH, Spaink HP (2011) A high-throughput screen for tuberculosis progression. PLoS One 6:e16779PubMedCentralPubMedGoogle Scholar
  3. Clatworthy AE, Lee JS-W, Leibman M, Kostun Z, Davidson AJ, Hung DT (2009) Pseudomonas aeruginosa infection of zebrafish involves both host and pathogen determinants. Infect Immun 77:1293–1303PubMedCentralPubMedGoogle Scholar
  4. Ding C-B, Zhang J-P, Zhao Y, Peng Z-G, Song D-Q, Jiang J-D (2011) Zebrafish as a potential model organism for drug test against hepatitis C virus. PLoS One 6:e22921PubMedCentralPubMedGoogle Scholar
  5. Gabor KA, Goody MF, Mowel WK, Breitbach ME, Gratacap RL, Witten PE, Kim CH (2014) Influenza A virus infection in zebrafish recapitulates mammalian infection and sensitivity to anti-influenza drug treatment. Dis Model Mech 7:1227–1237PubMedCentralPubMedGoogle Scholar
  6. Goody MF, Sullivan C, Kim CH (2014) Studying the immune response to human viral infections using zebrafish. Dev Comp Immunol 46:84–95PubMedGoogle Scholar
  7. Hall CJ, Wicker SM, Chien A-T, Tromp A, Lawrence LM, Sun X, Krissansen GW, Crosier KE, Crosier PS (2014) Repositioning drugs for inflammatory disease – fishing for new anti-inflammatory agents. Dis Model Mech 7:1069–1081PubMedCentralPubMedGoogle Scholar
  8. Harriff MJ, Bermudez LE, Kent ML (2007) Experimental exposure of zebrafish, Danio rerio (Hamilton), to Mycobacterium marinum and Mycobacterium peregrinum reveals the gastrointestinal tract as the primary route of infection: a potential model for environmental mycobacterial infection. J Fish Dis 30:587–600PubMedGoogle Scholar
  9. Meijer AH, Spaink HP (2011) Host-pathogen interactions made transparent with the zebrafish model. Curr Drug Targets 12:1000–1017PubMedCentralPubMedGoogle Scholar
  10. Neely MN, Pfeifer JD, Caparon M (2002) Streptococcus-zebrafish model of bacterial pathogenesis. Infect Immun 70:3904–3914PubMedCentralPubMedGoogle Scholar
  11. Novoa B, Figueras A (2012) Current topics in innate immunity II. Springer New York, New YorkGoogle Scholar
  12. O’Toole R, Von Hofsten J, Rosqvist R, Olsson P-E, Wolf-Watz H (2004) Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum. Microb Pathog 37:41–46PubMedGoogle Scholar
  13. Palha N, Guivel-Benhassine F, Briolat V, Lutfalla G, Sourisseau M, Ellett F, Wang C-H, Lieschke GJ, Herbomel P, Schwartz O et al (2013) Real-time whole-body visualization of Chikungunya virus infection and host interferon response in zebrafish. PLoS Pathog 9:e1003619PubMedCentralPubMedGoogle Scholar
  14. Pressley ME, Phelan PE, Witten PE, Mellon MT, Kim CH (2005) Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev Comp Immunol 29:501–513PubMedGoogle Scholar
  15. Robertson AL, Holmes GR, Bojarczuk AN, Burgon J, Loynes CA, Chimen M, Sawtell AK, Hamza B, Willson J, Walmsley SR et al (2014) A zebrafish compound screen reveals modulation of neutrophil reverse migration as an anti-inflammatory mechanism. Sci Transl Med 6:225ra29PubMedCentralPubMedGoogle Scholar
  16. Sullivan C, Kim CH (2008) Zebrafish as a model for infectious disease and immune function. Fish Shellfish Immunol 25:341–350PubMedGoogle Scholar
  17. Van der Sar AM, Musters RJP, van Eeden FJM, Appelmelk BJ, Vandenbroucke-Grauls CMJE, Bitter W (2003) Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. Cell Microbiol 5:601–611PubMedGoogle Scholar
  18. Van der Sar AM, Appelmelk BJ, Vandenbroucke-Grauls CMJE, Bitter W (2004) A star with stripes: zebrafish as an infection model. Trends Microbiol 12:451–457PubMedGoogle Scholar
  19. Wang X, Robertson AL, Li J, Chai RJ, Haishan W, Sadiku P, Ogryzko NV, Everett M, Yoganathan K, Luo HR et al (2014) Inhibitors of neutrophil recruitment identified using transgenic zebrafish to screen a natural product library. Dis Model Mech 7:163–169PubMedCentralPubMedGoogle Scholar

The Photomotor Response (PMR)

  1. Fernandes AM, Fero K, Driever W, Burgess HA (2013) Enlightening the brain: linking deep brain photoreception with behavior and physiology. Bioessays 35:775–779PubMedCentralPubMedGoogle Scholar
  2. Huang Y-Y, Neuhauss SCF (2008) The optokinetic response in zebrafish and its applications. Front. Biosci. 13:1899–1916PubMedGoogle Scholar
  3. Kokel D, Bryan J, Laggner C, White R, Cheung CYJ, Mateus R, Healey D, Kim S, Werdich AA, Haggarty SJ et al (2010) Rapid behavior-based identification of neuroactive small molecules in the zebrafish. Nat Chem Biol 6:231–237PubMedCentralPubMedGoogle Scholar
  4. Kokel D, Dunn TW, Ahrens MB, Alshut R, Cheung CYJ, Saint-Amant L, Bruni G, Mateus R, van Ham TJ, Shiraki T et al (2013a) Identification of nonvisual photomotor response cells in the vertebrate hindbrain. J Neurosci 33:3834–3843PubMedCentralPubMedGoogle Scholar
  5. Kokel D, Cheung CYJ, Mills R, Coutinho-Budd J, Huang L, Setola V, Sprague J, Jin S, Jin YN, Huang X-P et al (2013b) Photochemical activation of TRPA1 channels in neurons and animals. Nat Chem Biol 9:257–263PubMedCentralPubMedGoogle Scholar
  6. Rihel J, Schier AF (2012a) Behavioral screening for neuroactive drugs in zebrafish. Dev Neurobiol 72:373–385PubMedGoogle Scholar

Visual Motor Response (Light and Dark Photokinesis)

  1. Akhtar MT, Ali S, Rashidi H, van der Kooy F, Verpoorte R, Richardson MK (2013) Developmental effects of cannabinoids on zebrafish larvae. Zebrafish 10:283–293PubMedGoogle Scholar
  2. Ali S, van Mil HGJ, Richardson MK (2011b) Large-scale assessment of the zebrafish embryo as a possible predictive model in toxicity testing. PLoS One 6:e21076PubMedCentralPubMedGoogle Scholar
  3. Ali S, Champagne DL, Richardson MK (2012) Behavioral profiling of zebrafish embryos exposed to a panel of 60 water-soluble compounds. Behav Brain Res 228:272–283PubMedGoogle Scholar
  4. Burgess HA, Granato M (2007a) Modulation of locomotor activity in larval zebrafish during light adaptation. J Exp Biol 210:2526–2539PubMedGoogle Scholar
  5. Deeti S, O’Farrell S, Kennedy BN (2014a) Early safety assessment of human oculotoxic drugs using the zebrafish visualmotor response. J Pharmacol Toxicol Methods 69:1–8PubMedGoogle Scholar
  6. Emran F, Rihel J, Adolph AR, Wong KY, Kraves S, Dowling JE (2007a) OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proc Natl Acad Sci U S A 104:19126–19131PubMedCentralPubMedGoogle Scholar
  7. Emran F, Rihel J, Dowling JE (2008). A behavioral assay to measure responsiveness of zebrafish to changes in light intensities. J Vis Exp 20. pii: 923Google Scholar
  8. Emran F, Rihel J, Adolph AR, Dowling JE (2010a) Zebrafish larvae lose vision at night. Proc Natl Acad Sci U S A 107:6034–6039PubMedCentralPubMedGoogle Scholar
  9. 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 22:2042–2047PubMedCentralPubMedGoogle Scholar
  10. Fadool JM, Dowling JE (2008) Zebrafish: a model system for the study of eye genetics. Prog Retin Eye Res 27:89–110PubMedCentralPubMedGoogle Scholar
  11. Gao Y, Chan RHM, Chow TWS, Zhang L, Bonilla S, Pang C-P, Zhang M, Leung YF (2014) A high-throughput zebrafish screening method for visual mutants by light-induced locomotor response. IEEE/ACM Trans Comput Biol Bioinform 11:693–701Google Scholar
  12. Long S-M, Liang F-Y, Wu Q, Lu X-L, Yao X-L, Li S-C, Li J, Su H, Pang J-Y, Pei Z (2014) Identification of marine neuroactive molecules in behaviour-based screens in the larval zebrafish. Mar Drugs 12:3307–3322PubMedCentralPubMedGoogle Scholar
  13. Spulber S, Kilian P, Wan Ibrahim WN, Onishchenko N, Ulhaq M, Norrgren L, Negri S, Di Tuccio M, Ceccatelli S (2014) PFOS induces behavioral alterations, including spontaneous hyperactivity that is corrected by dexamfetamine in zebrafish larvae. PLoS One 9:e94227PubMedCentralPubMedGoogle Scholar

Optomotor Reflex (OMR)

  1. Bilotta J, Saszik S, Givin CM, Hardesty HR, Sutherland SE (2002b) Effects of embryonic exposure to ethanol on zebrafish visual function. Neurotoxicol Teratol 24:759–766PubMedGoogle Scholar
  2. Orger MB, Smear MC, Anstis SM, Baier H (2000) Perception of Fourier and non-Fourier motion by larval zebrafish. Nat Neurosci 3:1128–1133PubMedGoogle Scholar
  3. Orger MB, Gahtan E, Muto A, Page-McCaw P, Smear MC, Baier H (2004) Behavioral screening assays in zebrafish. In: Westerfield M, Zon LI, Detrich WH (eds) Methods in cell biology, vol I. Academic, San Diego, pp 53–68Google Scholar
  4. Richards FM, Alderton WK, Kimber GM, Liu Z, Strang I, Redfern WS, Valentin J-P, Winter MJ, Hutchinson TH (2008a) Validation of the use of zebrafish larvae in visual safety assessment. J Pharmacol Toxicol Methods 58:50–58PubMedGoogle Scholar
  5. Zou SQ, Yin W, Zhang MJ, Hu CR, Huang YB, Hu B (2010) Using the optokinetic response to study visual function of zebrafish. J Vis Exp 36. pii: 1742Google Scholar
  6. Zou S, Tian C, Ge S, Hu B (2013) Neurogenesis of retinal ganglion cells is not essential to visual functional recovery after optic nerve injury in adult zebrafish. PLoS One 8:e57280PubMedCentralPubMedGoogle Scholar

Optokinetic Reflex (OKR)

  1. Bilotta J, Saszik S, Givin CM, Hardesty HR, Sutherland SE (2002c) Effects of embryonic exposure to ethanol on zebrafish visual function. Neurotoxicol Teratol 24:759–766PubMedGoogle Scholar
  2. Brockerhoff SE (2006) Measuring the optokinetic response of zebrafish larvae. Nat Protoc 1:2448–2451PubMedGoogle Scholar
  3. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE (1995a) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A 92:10545–10549PubMedCentralPubMedGoogle Scholar
  4. Cameron DJ, Rassamdana F, Tam P, Dang K, Yanez C, Ghaemmaghami S, Dehkordi MI (2013) The optokinetic response as a quantitative measure of visual acuity in zebrafish. J Vis Exp 80Google Scholar
  5. Deeti S, O’Farrell S, Kennedy BN (2014b) Early safety assessment of human oculotoxic drugs using the zebrafish visualmotor response. J Pharmacol Toxicol Methods 69:1–8PubMedGoogle Scholar
  6. Emran F, Rihel J, Adolph AR, Wong KY, Kraves S, Dowling JE (2007b) OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proc Natl Acad Sci U S A 104:19126–19131PubMedCentralPubMedGoogle Scholar
  7. Huber-Reggi SP, Mueller KP, Neuhauss SCF (2013) Analysis of optokinetic response in zebrafish by computer-based eye tracking. Methods Mol Biol Clifton NJ 935:139–160Google Scholar
  8. Mueller KP, Neuhauss SCF (2010) Quantitative measurements of the optokinetic response in adult fish. J Neurosci Methods 186:29–34PubMedGoogle Scholar
  9. Mueller KP, Schnaedelbach ODR, Russig HD, Neuhauss SCF (2011) VisioTracker, an innovative automated approach to oculomotor analysis. J Vis Exp 56. pii: 3556Google Scholar
  10. Neuhauss SC, Biehlmaier O, Seeliger MW, Das T, Kohler K, Harris WA, Baier H (1999) Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J Neurosci 19:8603–8615PubMedGoogle Scholar
  11. Richards FM, Alderton WK, Kimber GM, Liu Z, Strang I, Redfern WS, Valentin J-P, Winter MJ, Hutchinson TH (2008b) Validation of the use of zebrafish larvae in visual safety assessment. J Pharmacol Toxicol Methods 58:50–58PubMedGoogle Scholar
  12. Tappeiner C, Gerber S, Enzmann V, Balmer J, Jazwinska A, Tschopp M (2012) Visual acuity and contrast sensitivity of adult zebrafish. Front Zool 9:10PubMedCentralPubMedGoogle Scholar
  13. Zou SQ, Yin W, Zhang MJ, Hu CR, Huang YB, Hu B (2010) Using the optokinetic response to study visual function of zebrafish. J Vis Exp 36. pii: 1742Google Scholar

Electroretinogram (ERG)

  1. Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE (1995b) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci U S A 92:10545–10549PubMedCentralPubMedGoogle Scholar
  2. Emran F, Rihel J, Adolph AR, Wong KY, Kraves S, Dowling JE (2007c) OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proc Natl Acad Sci U S A 104:19126–19131PubMedCentralPubMedGoogle Scholar
  3. Emran F, Rihel J, Adolph AR, Dowling JE (2010b) Zebrafish larvae lose vision at night. Proc Natl Acad Sci U S A 107:6034–6039PubMedCentralPubMedGoogle Scholar
  4. Fleisch VC, Jametti T, Neuhauss SCF (2008) Electroretinogram (ERG) measurements in larval zebrafish. CSH Protoc 2008:pdb.prot4973PubMedGoogle Scholar
  5. Li L, Dowling JE (1997) A dominant form of inherited retinal degeneration caused by a non-photoreceptor cell-specific mutation. Proc Natl Acad Sci U S A 94:11645–11650PubMedCentralPubMedGoogle Scholar
  6. Seeliger MW, Rilk A, Neuhauss SCF (2002) Ganzfeld ERG in zebrafish larvae. Doc Ophthalmol 104:57–68PubMedGoogle Scholar
  7. Wong KY, Gray J, Hayward CJC, Adolph AR, Dowling JE (2004) Glutamatergic mechanisms in the outer retina of larval zebrafish: analysis of electroretinogram b- and d-waves using a novel preparation. Zebrafish 1:121–131PubMedGoogle Scholar

Acoustic Startle

  1. Bergeron SA, Carrier N, Li GH, Ahn S, Burgess HA (2014) Gsx1 expression defines neurons required for prepulse inhibition. Mol Psychiatry. doi:10.1038/mp.2014.106Google Scholar
  2. Best JD, Berghmans S, Hunt JJFG, Clarke SC, Fleming A, Goldsmith P, Roach AG (2008a) Non-associative learning in larval zebrafish. Neuropsychopharmacology 33:1206–1215PubMedGoogle Scholar
  3. Bhandiwad AA, Zeddies DG, Raible DW, Rubel EW, Sisneros JA (2013) Auditory sensitivity of larval zebrafish (Danio rerio) measured using a behavioral prepulse inhibition assay. J Exp Biol 216:3504–3513PubMedCentralPubMedGoogle Scholar
  4. Burgess HA, Granato M (2007b) Sensorimotor gating in larval zebrafish. J Neurosci 27:4984–4994PubMedGoogle Scholar
  5. Hedrick TL (2008) Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim 3:034001PubMedGoogle Scholar
  6. Preuss T, Faber DS (2003) Central cellular mechanisms underlying temperature-dependent changes in the goldfish startle-escape behavior. J Neurosci 23:5617–5626PubMedGoogle Scholar
  7. Roberts AC, Reichl J, Song MY, Dearinger AD, Moridzadeh N, Lu ED, Pearce K, Esdin J, Glanzman DL (2011a) Habituation of the C-start response in larval zebrafish exhibits several distinct phases and sensitivity to NMDA receptor blockade. PLoS One 6:e29132PubMedCentralPubMedGoogle Scholar
  8. Wolman MA, Jain RA, Liss L, Granato M (2011a) Chemical modulation of memory formation in larval zebrafish. Proc Natl Acad Sci U S A 108:15468–15473PubMedCentralPubMedGoogle Scholar

Olfactory Explants

  1. Blumhagen F, Zhu P, Shum J, Schärer Y-PZ, Yaksi E, Deisseroth K, Friedrich RW (2011) Neuronal filtering of multiplexed odour representations. Nature 479:493–498PubMedGoogle Scholar
  2. Bundschuh ST, Zhu P, Schärer Y-PZ, Friedrich RW (2012) Dopaminergic modulation of mitral cells and odor responses in the zebrafish olfactory bulb. J Neurosci 32:6830–6840PubMedGoogle Scholar
  3. Friedrich RW (2014) Calcium imaging in the intact olfactory system of zebrafish and mouse. Cold Spring Harb Protoc 2014:310–316PubMedGoogle Scholar
  4. Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737–752PubMedGoogle Scholar
  5. Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291:889–894PubMedGoogle Scholar
  6. Friedrich RW, Habermann CJ, Laurent G (2004) Multiplexing using synchrony in the zebrafish olfactory bulb. Nat Neurosci 7:862–871PubMedGoogle Scholar
  7. Mathieson WB, Maler L (1988) Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J Comp Physiol A 163:489–506PubMedGoogle Scholar
  8. Schärer Y-PZ, Shum J, Moressis A, Friedrich RW (2012) Dopaminergic modulation of synaptic transmission and neuronal activity patterns in the zebrafish homolog of olfactory cortex. Front Neural Circ 6:76Google Scholar
  9. Tabor R, Friedrich RW (2008) Pharmacological analysis of ionotropic glutamate receptor function in neuronal circuits of the zebrafish olfactory bulb. PLoS One 3:e1416PubMedCentralPubMedGoogle Scholar
  10. Tabor R, Yaksi E, Friedrich RW (2008) Multiple functions of GABA A and GABA B receptors during pattern processing in the zebrafish olfactory bulb. Eur J Neurosci 28:117–127PubMedGoogle Scholar
  11. Yaksi E, Friedrich RW (2006) Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nat Methods 3:377–383PubMedGoogle Scholar
  12. Yaksi E, von Saint Paul F, Niessing J, Bundschuh ST, Friedrich RW (2009) Transformation of odor representations in target areas of the olfactory bulb. Nat Neurosci 12:474–482PubMedGoogle Scholar
  13. Zhu P, Frank T, Friedrich RW (2013) Equalization of odor representations by a network of electrically coupled inhibitory interneurons. Nat Neurosci 16:1678–1686PubMedGoogle Scholar

Larval Short Term Tracking

  1. Bichara D, Calcaterra NB, Arranz S, Armas P, Simonetta SH (2014) Set-up of an infrared fast behavioral assay using zebrafish (Danio rerio) larvae, and its application in compound biotoxicity screening. J Appl Toxicol 34:214–219PubMedGoogle Scholar
  2. Duan J, Yu Y, Shi H, Tian L, Guo C, Huang P, Zhou X, Peng S, Sun Z (2013) Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS One 8:e74606PubMedCentralPubMedGoogle Scholar
  3. Grillner S, Manira AE (2015) The intrinsic operation of the networks that make us locomote. Curr Opin Neurobiol 31C:244–249Google Scholar
  4. Irons TD, MacPhail RC, Hunter DL, Padilla S (2010) Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol Teratol 32:84–90PubMedGoogle Scholar
  5. Irons TD, Kelly PE, Hunter DL, Macphail RC, Padilla S (2013) Acute administration of dopaminergic drugs has differential effects on locomotion in larval zebrafish. Pharmacol Biochem Behav 103:792–813PubMedCentralPubMedGoogle Scholar
  6. MacPhail RC, Brooks J, Hunter DL, Padnos B, Irons TD, Padilla S (2009) Locomotion in larval zebrafish: influence of time of day, lighting and ethanol. Neurotoxicology 30:52–58PubMedGoogle Scholar
  7. Mirat O, Sternberg JR, Severi KE, Wyart C (2013a) ZebraZoom: an automated program for high-throughput behavioral analysis and categorization. Front Neural Circ 7:107Google Scholar
  8. Renier C, Faraco JH, Bourgin P, Motley T, Bonaventure P, Rosa F, Mignot E (2007b) Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenet Genomics 17:237–253PubMedGoogle Scholar

Head Embedded, Tail Free Swimming

  1. Bianco IH, Kampff AR, Engert F (2011) Prey capture behavior evoked by simple visual stimuli in larval zebrafish. Front Syst Neurosci 5:101PubMedCentralPubMedGoogle Scholar
  2. Brustein E, Drapeau P (2005a) Serotoninergic modulation of chloride homeostasis during maturation of the locomotor network in zebrafish. J Neurosci 25:10607–10616PubMedGoogle Scholar
  3. Brustein E, Chong M, Holmqvist B, Drapeau P (2003a) Serotonin patterns locomotor network activity in the developing zebrafish by modulating quiescent periods. J Neurobiol 57:303–322PubMedGoogle Scholar
  4. Budick SA, O’Malley DM (2000) Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. J Exp Biol 203:2565–2579PubMedGoogle Scholar
  5. Mirat O, Sternberg JR, Severi KE, Wyart C (2013b) ZebraZoom: an automated program for high-throughput behavioral analysis and categorization. Front Neural Circ 7:107Google Scholar
  6. O’Malley DM, Sankrithi NS, Borla MA, Parker S, Banden S, Gahtan E, Detrich HW (2004) Optical physiology and locomotor behaviors of wild-type and nacre zebrafish. Methods Cell Biol 76:261–284PubMedGoogle Scholar
  7. Portugues R, Engert F (2011) Adaptive locomotor behavior in larval zebrafish. Front Syst Neurosci 5:72PubMedCentralPubMedGoogle Scholar
  8. Portugues R, Feierstein CE, Engert F, Orger MB (2014) Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior. Neuron 81:1328–1343PubMedCentralPubMedGoogle Scholar
  9. 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 83:692–707PubMedGoogle Scholar
  10. Wyart C, Bene FD, Warp E, Scott EK, Trauner D, Baier H, Isacoff EY (2009) Optogenetic dissection of a behavioral module in the vertebrate spinal cord. Nature 461:407–410PubMedCentralPubMedGoogle Scholar

Larval Fictive Swimming

  1. Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485:471–477PubMedCentralPubMedGoogle Scholar
  2. Brustein E, Drapeau P (2005b) Serotoninergic modulation of chloride homeostasis during maturation of the locomotor network in zebrafish. J Neurosci 25:10607–10616PubMedGoogle Scholar
  3. Brustein E, Chong M, Holmqvist B, Drapeau P (2003b) Serotonin patterns locomotor network activity in the developing zebrafish by modulating quiescent periods. J Neurobiol 57:303–322PubMedGoogle Scholar
  4. Buss RR, Drapeau P (2001) Synaptic drive to motoneurons during fictive swimming in the developing zebrafish. J Neurophysiol 86:197–210PubMedGoogle Scholar
  5. Drapeau P, Ali DW, Buss RR, Saint-Amant L (1999) In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish. J Neurosci Methods 88:1–13PubMedGoogle Scholar
  6. Knogler LD, Drapeau P (2014) Sensory gating of an embryonic zebrafish interneuron during spontaneous motor behaviors. Front Neural Circ 8:121Google Scholar
  7. Knogler LD, Liao M, Drapeau P (2010) Synaptic scaling and the development of a motor network. J Neurosci 30:8871–8881PubMedGoogle Scholar
  8. Knogler LD, Ryan J, Saint-Amant L, Drapeau P (2014) A hybrid electrical/chemical circuit in the spinal cord generates a transient embryonic motor behavior. J Neurosci 34:9644–9655PubMedGoogle Scholar
  9. Masino MA, Fetcho JR (2005) Fictive swimming motor patterns in wild type and mutant larval zebrafish. J Neurophysiol 93:3177–3188PubMedGoogle Scholar
  10. Trapani JG, Nicolson T (2010) Physiological recordings from zebrafish lateral-line hair cells and afferent neurons. Methods Cell Biol 100:219–231PubMedGoogle Scholar
  11. Vladimirov N, Mu Y, Kawashima T, Bennett DV, Yang C-T, Looger LL, Keller PJ, Freeman J, Ahrens MB (2014) Light-sheet functional imaging in fictively behaving zebrafish. Nat Methods 11:883–884PubMedGoogle Scholar

Long Term Tracking: Sleep

  1. Cahill GM, Hurd MW, Batchelor MM (1998) Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport 9:3445–3449PubMedGoogle Scholar
  2. Gandhi AV, Mosser EA, Oikonomou G, Prober DA (2015) Melatonin is required for the circadian regulation of sleep. Neuron 85:1193–1199PubMedGoogle Scholar
  3. Hurd MW, Cahill GM (2002) Entraining signals initiate behavioral circadian rhythmicity in larval zebrafish. J Biol Rhythms 17:307–314PubMedGoogle Scholar
  4. Prober DA, Rihel J, Onah AA, Sung R-J, Schier AF (2006) Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J Neurosci 26:13400–13410PubMedGoogle Scholar
  5. Rihel J, Schier AF (2012b) Behavioral screening for neuroactive drugs in zebrafish. Dev Neurobiol 72:373–385PubMedGoogle Scholar
  6. Rihel J, Prober DA, Schier AF (2010a) Monitoring sleep and arousal in zebrafish. Methods Cell Biol 100:281–294PubMedGoogle Scholar
  7. Rihel J, Prober DA, Arvanites A, Lam K, Zimmerman S, Jang S, Haggarty SJ, Kokel D, Rubin LL, Peterson RT et al (2010b) Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 327:348–351PubMedCentralPubMedGoogle Scholar
  8. Sigurgeirsson B, Thornorsteinsson H, Sigmundsdóttir S, Lieder R, Sveinsdóttir HS, Sigurjónsson ÓE, Halldórsson B, Karlsson K (2013) Sleep-wake dynamics under extended light and extended dark conditions in adult zebrafish. Behav Brain Res 256:377–390PubMedGoogle Scholar
  9. Yokogawa T, Marin W, Faraco J, Pézeron G, Appelbaum L, Zhang J, Rosa F, Mourrain P, Mignot E (2007) Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PLoS Biol 5:e277PubMedCentralPubMedGoogle Scholar
  10. Zhdanova IV, Wang SY, Leclair OU, Danilova NP (2001) Melatonin promotes sleep-like state in zebrafish. Brain Res 903:263–268PubMedGoogle Scholar

Novel Tank and Anxiety

  1. Ahmad F, Richardson MK (2013) Exploratory behaviour in the open field test adapted for larval zebrafish: impact of environmental complexity. Behav Processes 92:88–98PubMedGoogle Scholar
  2. Amir-Zilberstein L, Blechman J, Sztainberg Y, Norton WHJ, Reuveny A, Borodovsky N, Tahor M, Bonkowsky JL, Bally-Cuif L, Chen A, Levkowitz G (2012) Homeodomain protein otp and activity-dependent splicing modulate neuronal adaptation to stress. Neuron 73(2):279–291PubMedCentralPubMedGoogle Scholar
  3. Bencan Z, Sledge D, Levin ED (2009) Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. Pharmacol Biochem Behav 94(1):75–80PubMedCentralPubMedGoogle Scholar
  4. Blaser RE, Chadwick L, McGinnis GC (2010) Behavioral measures of anxiety in zebrafish (Danio rerio). Behav Brain Res 208(1):56–62PubMedGoogle Scholar
  5. Cachat J et al (2010) Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat Protoc 5(11):1786–1799PubMedGoogle Scholar
  6. Cachat J, Kyzar EJ, Collins C, Gaikwad S, Green J, Roth A, El-Ounsi M, Davis A, Pham M, Landsman S, Stewart AM, Kalueff AV (2013a) Unique and potent effects of acute ibogaine on zebrafish: the developing utility of novel aquatic models for hallucinogenic drug research. Behav Brain Res 236(1):258–269PubMedGoogle Scholar
  7. Grossman L, Utterback E, Stewart A, Gaikwad S, Chung KM, Suciu C, Wong K, Elegante M, Elkhayat S, Tan J et al (2010a) Characterization of behavioral and endocrine effects of LSD on zebrafish. Behav Brain Res 214:277–284PubMedGoogle Scholar
  8. Kyzar EJ, Collins C, Gaikwad S, Green J, Roth A, Monnig L, El-Ounsi M, Davis A, Freeman A, Capezio N, Stewart AM, Kalueff AV (2012b) Effects of hallucinogenic agents mescaline and phencyclidine on zebrafish behavior and physiology. Prog Neuropsychopharmacol Biol Psychiatry 37(1):194–202PubMedCentralPubMedGoogle Scholar
  9. Levin ED, Bencan Z, Cerutti DT (2007) Anxiolytic effects of nicotine in zebrafish. Physiol Behav 90(1):54–58PubMedGoogle Scholar
  10. Maximino C, de Brito TM, Colmanetti R, Pontes AAA, de Castro HM, de Lacerda RIT, Morato S, Gouveia A (2010a) Parametric analyses of anxiety in zebrafish scototaxis. Behav Brain Res 210(1):1–7PubMedGoogle Scholar
  11. Maximino C, Marques de Brito T, Dias CA, Gouveia G, Morato S (2010b) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5(2):209–216PubMedGoogle Scholar
  12. Schnörr SJ, Steenbergen PJ, Richardson MK, Champagne DL (2012) Measuring thigmotaxis in larval zebrafish. Behav Brain Res 228(2):367–374PubMedGoogle Scholar
  13. Ziv L, Muto A, Schoonheim PJ, Meijsing SH, Strasser D, Ingraham HA, Schaaf MJM, Yamamoto KR, Baier H (2013) An affective disorder in zebrafish with mutation of the glucocorticoid receptor. Mol Psychiatry 18(6):681–691PubMedCentralPubMedGoogle Scholar

Electrophysiology

  1. Afrikanova T, Serruys A-SK, Buenafe OEM, Clinckers R, Smolders I, de Witte PAM, Crawford AD, Esguerra CV (2013a) Validation of the zebrafish pentylenetetrazol seizure model: locomotor versus electrographic responses to antiepileptic drugs. PLoS One 8:e54166PubMedCentralPubMedGoogle Scholar
  2. Baraban SC, Taylor MR, Castro PA, Baier H (2005a) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131:759–768PubMedGoogle Scholar
  3. Baraban SC, Dinday MT, Castro PA, Chege S, Guyenet S, Taylor MR (2007) A large-scale mutagenesis screen to identify seizure-resistant zebrafish. Epilepsia 48:1151–1157PubMedCentralPubMedGoogle Scholar
  4. Baraban SC, Dinday MT, Hortopan GA (2013a) Drug screening in Scn1a zebrafish mutant identifies clemizole as a potential Dravet syndrome treatment. Nat Commun 4:2410PubMedCentralPubMedGoogle Scholar
  5. Grone BP, Baraban SC (2015a) Animal models in epilepsy research: legacies and new directions. Nat Neurosci 18:339–343PubMedGoogle Scholar
  6. Mahmood F, Mozere M, Zdebik AA, Stanescu HC, Tobin J, Beales PL, Kleta R, Bockenhauer D, Russell C (2013) Generation and validation of a zebrafish model of EAST (epilepsy, ataxia, sensorineural deafness and tubulopathy) syndrome. Dis Model Mech 6:652–660PubMedCentralPubMedGoogle Scholar
  7. Ramirez IB-R, Pietka G, Jones DR, Divecha N, Alia A, Baraban SC, Hurlstone AFL, Lowe M (2012) Impaired neural development in a zebrafish model for Lowe syndrome. Hum Mol Genet 21:1744–1759PubMedCentralPubMedGoogle Scholar
  8. Zdebik AA, Mahmood F, Stanescu HC, Kleta R, Bockenhauer D, Russell C (2013a) Epilepsy in kcnj10 morphant zebrafish assessed with a novel method for long-term EEG recordings. PLoS One 8:e79765PubMedCentralPubMedGoogle Scholar

Electroencephalogram

  1. Afrikanova T, Serruys A-SK, Buenafe OEM, Clinckers R, Smolders I, de Witte PAM, Crawford AD, Esguerra CV (2013b) Validation of the zebrafish pentylenetetrazol seizure model: locomotor versus electrographic responses to antiepileptic drugs. PLoS One 8:e54166PubMedCentralPubMedGoogle Scholar
  2. Zdebik AA, Mahmood F, Stanescu HC, Kleta R, Bockenhauer D, Russell C (2013b) Epilepsy in kcnj10 morphant zebrafish assessed with a novel method for long-term EEG recordings. PLoS One 8:e79765PubMedCentralPubMedGoogle Scholar

Seizure Behavior

  1. Afrikanova T, Serruys A-SK, Buenafe OEM, Clinckers R, Smolders I, de Witte PAM, Crawford AD, Esguerra CV (2013c) Validation of the zebrafish pentylenetetrazol seizure model: locomotor versus electrographic responses to antiepileptic drugs. PLoS One 8:e54166PubMedCentralPubMedGoogle Scholar
  2. Baraban SC, Taylor MR, Castro PA, Baier H (2005b) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131:759–768PubMedGoogle Scholar
  3. Baraban SC, Dinday MT, Hortopan GA (2013b) Drug screening in Scn1a zebrafish mutant identifies clemizole as a potential Dravet syndrome treatment. Nat Commun 4:2410PubMedCentralPubMedGoogle Scholar
  4. Baxendale S, Holdsworth CJ, Meza Santoscoy PL, Harrison MRM, Fox J, Parkin CA, Ingham PW, Cunliffe VT (2012) Identification of compounds with anti-convulsant properties in a zebrafish model of epileptic seizures. Dis Model Mech 5:773–784PubMedCentralPubMedGoogle Scholar
  5. Berghmans S, Hunt J, Roach A, Goldsmith P (2007) Zebrafish offer the potential for a primary screen to identify a wide variety of potential anticonvulsants. Epilepsy Res 75:18–28PubMedGoogle Scholar
  6. Grone BP, Baraban SC (2015b) Animal models in epilepsy research: legacies and new directions. Nat Neurosci 18:339–343PubMedGoogle Scholar
  7. Koseki N, Deguchi J, Yamashita A, Miyawaki I, Funabashi H (2014) Establishment of a novel experimental protocol for drug-induced seizure liability screening based on a locomotor activity assay in zebrafish. J Toxicol Sci 39:579–600PubMedGoogle Scholar
  8. Wong K, Stewart A, Gilder T, Wu N, Frank K, Gaikwad S, Suciu C, Dileo J, Utterback E, Chang K et al (2010a) Modeling seizure-related behavioral and endocrine phenotypes in adult zebrafish. Brain Res 1348:209–215PubMedGoogle Scholar

Nonassociative Learning

  1. Best JD, Berghmans S, Hunt JJFG, Clarke SC, Fleming A, Goldsmith P, Roach AG (2008b) Non-associative learning in larval zebrafish. Neuropsychopharmacology 33:1206–1215PubMedGoogle Scholar
  2. Blaser RE, Vira DG (2014a) Experiments on learning in zebrafish (Danio rerio): a promising model of neurocognitive function. Neurosci Biobehav Rev 42:224–231PubMedGoogle Scholar
  3. Burgess HA, Granato M (2007c) Sensorimotor gating in larval zebrafish. J Neurosci 27:4984–4994PubMedGoogle Scholar
  4. Burgess HA, Granato M (2007d) Modulation of locomotor activity in larval zebrafish during light adaptation. J Exp Biol 210:2526–2539PubMedGoogle Scholar
  5. Eddins D, Cerutti D, Williams P, Linney E, Levin ED (2010) Zebrafish provide a sensitive model of persisting neurobehavioral effects of developmental chlorpyrifos exposure: comparison with nicotine and pilocarpine effects and relationship to dopamine deficits. Neurotoxicol Teratol 32:99–108PubMedCentralPubMedGoogle Scholar
  6. Roberts AC, Reichl J, Song MY, Dearinger AD, Moridzadeh N, Lu ED, Pearce K, Esdin J, Glanzman DL (2011b) Habituation of the C-start response in larval zebrafish exhibits several distinct phases and sensitivity to NMDA receptor blockade. PLoS One 6:e29132PubMedCentralPubMedGoogle Scholar
  7. Roberts AC, Bill BR, Glanzman DL (2013) Learning and memory in zebrafish larvae. Front Neural Circ 7:126Google Scholar
  8. Wolman MA, Jain RA, Liss L, Granato M (2011b) Chemical modulation of memory formation in larval zebrafish. Proc Natl Acad Sci U S A 108:15468–15473PubMedCentralPubMedGoogle Scholar
  9. Wong K, Elegante M, Bartels B, Elkhayat S, Tien D, Roy S, Goodspeed J, Suciu C, Tan J, Grimes C et al (2010b) Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav Brain Res 208:450–457PubMedGoogle Scholar

Associative Learning-Classical Conditioning

  1. Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M, Sassa T, Amo R, Shiraki T, Kawakami K et al (2010) The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13:1354–1356PubMedGoogle Scholar
  2. Aizenberg M, Schuman EM (2011) Cerebellar-dependent learning in larval zebrafish. J Neurosci 31:8708–8712PubMedGoogle Scholar
  3. Blaser RE, Vira DG (2014b) Experiments on learning in zebrafish (Danio rerio): a promising model of neurocognitive function. Neurosci Biobehav Rev 42:224–231PubMedGoogle Scholar
  4. Braubach OR, Wood H-D, Gadbois S, Fine A, Croll RP (2009) Olfactory conditioning in the zebrafish (Danio rerio). Behav Brain Res 198:190–198PubMedGoogle Scholar
  5. Cerutti DT, Jozefowiez J, Staddon JER (2013) Rapid, accurate time estimation in zebrafish (Danio rerio). Behav Processes 99:21–25PubMedGoogle Scholar
  6. Darland T, Dowling JE (2001) Behavioral screening for cocaine sensitivity in mutagenized zebrafish. Proc Natl Acad Sci U S A 98:11691–11696PubMedCentralPubMedGoogle Scholar
  7. Hall D, Suboski MD (1995a) Visual and olfactory stimuli in learned release of alarm reactions by zebra danio fish (Brachydanio rerio). Neurobiol Learn Mem 63:229–240PubMedGoogle Scholar
  8. Hall D, Suboski MD (1995b) Sensory preconditioning and secord-order conditioning of alarm reactions in zebra danio fish (Brachydanio rerio). J Comp Psychol 109:76–84Google Scholar
  9. Kily LJM, Cowe YCM, Hussain O, Patel S, McElwaine S, Cotter FE, Brennan CH (2008) Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways. J Exp Biol 211:1623–1634PubMedGoogle Scholar
  10. Lau B, Bretaud S, Huang Y, Lin E, Guo S (2006) Dissociation of food and opiate preference by a genetic mutation in zebrafish. Genes Brain Behav 5:497–505PubMedGoogle Scholar
  11. Mathur P, Berberoglu MA, Guo S (2011) Preference for ethanol in zebrafish following a single exposure. Behav Brain Res 217:128–133PubMedCentralPubMedGoogle Scholar
  12. Ninkovic J, Bally-Cuif L (2006) The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse. Methods 39:262–274PubMedGoogle Scholar
  13. Valente A, Huang K-H, Portugues R, Engert F (2012a) Ontogeny of classical and operant learning behaviors in zebrafish. Learn Mem 19:170–177PubMedCentralPubMedGoogle Scholar
  14. Webb KJ, Norton WH, Trümbach D, Meijer AH, Ninkovic J, Topp S, Heck D, Marr C, Wurst W, Theis FJ et al (2009) Zebrafish reward mutants reveal novel transcripts mediating the behavioral effects of amphetamine. Genome Biol 10:R81PubMedCentralPubMedGoogle Scholar

Associative Learning: Operant Conditioning

  1. Al-Imari L, Gerlai R (2008) Sight of conspecifics as reward in associative learning in zebrafish (Danio rerio). Behav Brain Res 189:216–219PubMedGoogle Scholar
  2. Bilotta J, Saszik S, Givin CM, Hardesty HR, Sutherland SE (2002d) Effects of embryonic exposure to ethanol on zebrafish visual function. Neurotoxicol Teratol 24:759–766PubMedGoogle Scholar
  3. Blank M, Guerim LD, Cordeiro RF, Vianna MRM (2009) A one-trial inhibitory avoidance task to zebrafish: rapid acquisition of an NMDA-dependent long-term memory. Neurobiol Learn Mem 92:529–534PubMedGoogle Scholar
  4. Colwill RM, Raymond MP, Ferreira L, Escudero H (2005) Visual discrimination learning in zebrafish (Danio rerio). Behav Processes 70:19–31PubMedGoogle Scholar
  5. Gleason PE, Weber PG, Weber SP (1977) Effect of group size on avoidance learning in zebra fish, Brachydanio rerio (Pisces: Cyprinidae). Anim Learn Behav 5:213–216Google Scholar
  6. Karnik I, Gerlai R (2012) Can zebrafish learn spatial tasks? An empirical analysis of place and single CS-US associative learning. Behav Brain Res 233:415–421PubMedCentralPubMedGoogle Scholar
  7. Lee A, Mathuru AS, Teh C, Kibat C, Korzh V, Penney TB, Jesuthasan S (2010) The habenula prevents helpless behavior in larval zebrafish. Curr Biol 20:2211–2216PubMedGoogle Scholar
  8. Mueller KP, Neuhauss SCF (2012) Automated visual choice discrimination learning in zebrafish (Danio rerio). J Integr Neurosci 11:73–85PubMedGoogle Scholar
  9. Parker MO, Gaviria J, Haigh A, Millington ME, Brown VJ, Combe FJ, Brennan CH (2012) Discrimination reversal and attentional sets in zebrafish (Danio rerio). Behav Brain Res 232:264–268PubMedCentralPubMedGoogle Scholar
  10. Pather S, Gerlai R (2009) Shuttle box learning in zebrafish (Danio rerio). Behav Brain Res 196:323–327PubMedCentralPubMedGoogle Scholar
  11. Pradel G, Schachner M, Schmidt R (1999) Inhibition of memory consolidation by antibodies against cell adhesion molecules after active avoidance conditioning in zebrafish. J Neurobiol 39:197–206PubMedGoogle Scholar
  12. Valente A, Huang K-H, Portugues R, Engert F (2012b) Ontogeny of classical and operant learning behaviors in zebrafish. Learn Mem 19:170–177PubMedCentralPubMedGoogle Scholar
  13. Williams FE, White D, Messer WS (2002) A simple spatial alternation task for assessing memory function in zebrafish. Behav Processes 58:125–132PubMedGoogle Scholar
  14. Xu X, Scott-Scheiern T, Kempker L, Simons K (2007) Active avoidance conditioning in zebrafish (Danio rerio). Neurobiol Learn Mem 87:72–77PubMedGoogle Scholar
  15. Yang S, Kim W, Choi B, Koh H, Lee C (2003) Alcohol impairs learning of T-maze task but not active avoidance task in zebrafish. Korean J Biol Sci 7:303–307Google Scholar

Aggression: Mirror

  1. Cachat J, Kyzar EJ, Collins C, Gaikwad S, Green J, Roth A, El-Ounsi M, Davis A, Pham M, Landsman S et al (2013b) Unique and potent effects of acute ibogaine on zebrafish: the developing utility of novel aquatic models for hallucinogenic drug research. Behav Brain Res 236:258–269PubMedGoogle Scholar
  2. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6:744–747PubMedCentralPubMedGoogle Scholar
  3. Oliveira RF (2013) Mind the fish: zebrafish as a model in cognitive social neuroscience. Front Neural Circ 7:131Google Scholar
  4. Oliveira RF, Canário AVM (2011) Nemo through the looking-glass: a commentary on Desjardins & Fernald. Biol Lett 7:487–488PubMedCentralPubMedGoogle Scholar
  5. Oliveira RF, Carneiro LA, Canário AVM (2005) Behavioural endocrinology: no hormonal response in tied fights. Nature 437:207–208PubMedGoogle Scholar
  6. Paull GC, Filby AL, Giddins HG, Coe TS, Hamilton PB, Tyler CR (2010a) Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. Zebrafish 7:109–117PubMedGoogle Scholar
  7. Pham M, Raymond J, Hester J, Kyzar E, Gaikwad S, Bruce I, Fryar C, Chanin S, Enriquez J, Bagawandoss S, et al (2012) Assessing social behavior phenotypes in adult zebrafish: shoaling, social preference, and mirror biting tests. In Zebrafish Protocols for Neurobehavioral Research, (Humana Press), pp 231–246Google Scholar
  8. Teles MC, Dahlbom SJ, Winberg S, Oliveira RF (2013a) Social modulation of brain monoamine levels in zebrafish. Behav Brain Res 253:17–24PubMedGoogle Scholar
  9. Toms CN, Echevarria DJ (2014) Back to basics: searching for a comprehensive framework for exploring individual differences in zebrafish (Danio rerio) behavior. Zebrafish 11:325–340PubMedGoogle Scholar
  10. Way GP, Ruhl N, Snekser JL, Kiesel AL, McRobert SP (2015) A comparison of methodologies to test aggression in zebrafish. Zebrafish 12:144–151PubMedGoogle Scholar
  11. Weber DN, Ghorai JK (2013) Experimental design affects social behavior outcomes in adult zebrafish developmentally exposed to lead. Zebrafish 10:294–302PubMedGoogle Scholar

Conspecific Aggression

  1. Colman JR, Baldwin D, Johnson LL, Scholz NL (2009a) Effects of the synthetic estrogen, 17alpha-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol 91:346–354PubMedGoogle Scholar
  2. Larson ET, O’Malley DM, Melloni RH (2006) Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. Behav Brain Res 167:94–102PubMedGoogle Scholar
  3. Oliveira RF, Silva JF, Simões JM (2011) Fighting zebrafish: characterization of aggressive behavior and winner-loser effects. Zebrafish 8:73–81PubMedGoogle Scholar
  4. Teles MC, Dahlbom SJ, Winberg S, Oliveira RF (2013b) Social modulation of brain monoamine levels in zebrafish. Behav Brain Res 253:17–24PubMedGoogle Scholar

Competitive Spawning

  1. Coe TS, Hamilton PB, Hodgson D, Paull GC, Stevens JR, Sumner K, Tyler CR (2008) An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environ Sci Technol 42:5020–5025PubMedGoogle Scholar
  2. Coe TS, Hamilton PB, Hodgson D, Paull GC, Tyler CR (2009) Parentage outcomes in response to estrogen exposure are modified by social grouping in zebrafish. Environ Sci Technol 43:8400–8405PubMedGoogle Scholar
  3. Colman JR, Baldwin D, Johnson LL, Scholz NL (2009b) Effects of the synthetic estrogen, 17alpha-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol 91:346–354PubMedGoogle Scholar
  4. Danzmann RG (1997) PROBMAX: a computer program for assigning unknown parentage in pedigree analysis from known genotypic pools of parents and progeny. J Hered 88:333Google Scholar
  5. Delaney M, Follet C, Ryan N, Hanney N, Lusk-Yablick J, Gerlach G (2002) Social interaction and distribution of female zebrafish (Danio rerio) in a large aquarium. Biol Bull 203:240–241PubMedGoogle Scholar
  6. Filby AL, Paull GC, Searle F, Ortiz-Zarragoitia M, Tyler CR (2012) Environmental estrogen-induced alterations of male aggression and dominance hierarchies in fish: a mechanistic analysis. Environ Sci Technol 46:3472–3479PubMedGoogle Scholar
  7. Paull GC, Van Look KJW, Santos EM, Filby AL, Gray DM, Nash JP, Tyler CR (2008) Variability in measures of reproductive success in laboratory-kept colonies of zebrafish and implications for studies addressing population-level effects of environmental chemicals. Aquat Toxicol 87:115–126PubMedGoogle Scholar
  8. Paull GC, Filby AL, Giddins HG, Coe TS, Hamilton PB, Tyler CR (2010b) Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. Zebrafish 7:109–117PubMedGoogle Scholar
  9. Spence R (2006) Mating preference of female zebrafish, Danio rerio, in relation to male dominance. Behav Ecol 17:779–783Google Scholar
  10. Spence R, Smith C (2005) Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish. Anim Behav 69:1317–1323Google Scholar

Social Preference

  1. Abaid N, Bartolini T, Macrì S, Porfiri M (2012) Zebrafish responds differentially to a robotic fish of varying aspect ratio, tail beat frequency, noise, and color. Behav Brain Res 233:545–553PubMedGoogle Scholar
  2. Braida D, Donzelli A, Martucci R, Capurro V, Busnelli M, Chini B, Sala M (2012) Neurohypophyseal hormones manipulation modulate social and anxiety-related behavior in zebrafish. Psychopharmacology (Berl) 220:319–330Google Scholar
  3. Engeszer RE, Ryan MJ, Parichy DM (2004) Learned social preference in zebrafish. Curr Biol 14:881–884PubMedGoogle Scholar
  4. Fernandes Y, Gerlai R (2009b) Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcohol Clin Exp Res 33:601–609PubMedCentralPubMedGoogle Scholar
  5. Grossman L, Utterback E, Stewart A, Gaikwad S, Chung KM, Suciu C, Wong K, Elegante M, Elkhayat S, Tan J et al (2010b) Characterization of behavioral and endocrine effects of LSD on zebrafish. Behav Brain Res 214:277–284PubMedGoogle Scholar
  6. Moretz JA, Martins EP, Robison BD (2006) The effects of early and adult social environment on zebrafish (Danio rerio) behavior. Environ Biol Fishes 80:91–101Google Scholar
  7. Pitcher TJ (1993) Behaviour of teleost fishes. London, UK: Chapman and HallGoogle Scholar
  8. Riehl R, Kyzar E, Allain A, Green J, Hook M, Monnig L, Rhymes K, Roth A, Pham M, Razavi R et al (2011a) Behavioral and physiological effects of acute ketamine exposure in adult zebrafish. Neurotoxicol Teratol 33:658–667PubMedGoogle Scholar
  9. Saverino C, Gerlai R (2008) The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behav Brain Res 191:77–87PubMedCentralPubMedGoogle Scholar
  10. Savio LEB, Vuaden FC, Piato AL, Bonan CD, Wyse ATS (2012) Behavioral changes induced by long-term proline exposure are reversed by antipsychotics in zebrafish. Prog Neuropsychopharmacol Biol Psychiatry 36:258–263PubMedGoogle Scholar
  11. Seibt KJ, Piato AL, da Luz Oliveira R, Capiotti KM, Vianna MR, Bonan CD (2011) Antipsychotic drugs reverse MK-801-induced cognitive and social interaction deficits in zebrafish (Danio rerio). Behav Brain Res 224:135–139PubMedGoogle Scholar
  12. Sison M, Gerlai R (2011) Behavioral performance altering effects of MK-801 in zebrafish (Danio rerio). Behav Brain Res 220:331–337PubMedCentralPubMedGoogle Scholar
  13. Spence R, Smith C (2007) The role of early learning in determining shoaling preferences based on visual cues in the zebrafish, Danio rerio. Ethology 113:62–67Google Scholar
  14. Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin RK (2003) Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften 90:374–377PubMedGoogle Scholar
  15. Xia J, Niu C, Pei X (2010) Effects of chronic exposure to nonylphenol on locomotor activity and social behavior in zebrafish (Danio rerio). J Environ Sci (China) 22:1435–1440Google Scholar

Shoaling

  1. Buske C, Gerlai R (2011b) Early embryonic ethanol exposure impairs shoaling and the dopaminergic and serotoninergic systems in adult zebrafish. Neurotoxicol Teratol 33:698–707PubMedCentralPubMedGoogle Scholar
  2. Cachat J, Kyzar EJ, Collins C, Gaikwad S, Green J, Roth A, El-Ounsi M, Davis A, Pham M, Landsman S et al (2013c) Unique and potent effects of acute ibogaine on zebrafish: the developing utility of novel aquatic models for hallucinogenic drug research. Behav Brain Res 236:258–269PubMedGoogle Scholar
  3. Dolado R, Gimeno E, Beltran FS, Quera V, Pertusa JF (2014) A method for resolving occlusions when multitracking individuals in a shoal. Behav Res Methods, Oct 8Google Scholar
  4. Green J, Collins C, Kyzar EJ, Pham M, Roth A, Gaikwad S, Cachat J, Stewart AM, Landsman S, Grieco F et al (2012) Automated high-throughput neurophenotyping of zebrafish social behavior. J Neurosci Methods 210:266–271PubMedGoogle Scholar
  5. Grossman L, Utterback E, Stewart A, Gaikwad S, Chung KM, Suciu C, Wong K, Elegante M, Elkhayat S, Tan J et al (2010c) Characterization of behavioral and endocrine effects of LSD on zebrafish. Behav Brain Res 214:277–284PubMedGoogle Scholar
  6. Maaswinkel H, Zhu L, Weng W (2013a) Assessing social engagement in heterogeneous groups of zebrafish: a new paradigm for autism-like behavioral responses. PLoS One 8:e75955PubMedCentralPubMedGoogle Scholar
  7. Maaswinkel H, Le X, He L, Zhu L, Weng W (2013b) Dissociating the effects of habituation, black walls, buspirone and ethanol on anxiety-like behavioral responses in shoaling zebrafish. A 3D approach to social behavior. Pharmacol Biochem Behav 108:16–27PubMedGoogle Scholar
  8. Martineau PR, Mourrain P (2013) Tracking zebrafish larvae in group–status and perspectives. Methods 62:292–303PubMedCentralPubMedGoogle Scholar
  9. Miller N, Greene K, Dydinski A, Gerlai R (2013) Effects of nicotine and alcohol on zebrafish (Danio rerio) shoaling. Behav Brain Res 240:192–196PubMedGoogle Scholar
  10. Parker MO, Brock AJ, Millington ME, Brennan CH (2013) Behavioural phenotyping of casper mutant and 1-pheny-2-thiourea treated adult zebrafish. Zebrafish 10:466–471PubMedCentralPubMedGoogle Scholar
  11. Pérez-Escudero A, Vicente-Page J, Hinz RC, Arganda S, de Polavieja GG (2014) idTracker: tracking individuals in a group by automatic identification of unmarked animals. Nat Methods 11:743–748PubMedGoogle Scholar
  12. Riehl R, Kyzar E, Allain A, Green J, Hook M, Monnig L, Rhymes K, Roth A, Pham M, Razavi R et al (2011b) Behavioral and physiological effects of acute ketamine exposure in adult zebrafish. Neurotoxicol Teratol 33:658–667PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Cell and Developmental BiologyUniversity College LondonLondonUK

Personalised recommendations