Zebrafish as an emerging model for studying complex brain disorders

Trends in Pharmacological Sciences

Volumn 35, Issue 2, 2014, Pages 63-75

  Kalueff, Allan V ^a   Stewart, Adam Michael ^a,b   Gerlai, Robert ^c  

^a The International Zebrafish Neuroscience Research Consortium (ZNRC)   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

behavioral tests; brain disorders; translational research; zebrafish

Indexed keywords

BEHAVIORAL TESTS; BRAIN DISORDERS; TRANSLATIONAL RESEARCH; ZEBRAFISH;

ANIMALS; BRAIN DISEASES; DISEASE MODELS, ANIMAL; ZEBRAFISH;

EID: 84895076713     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2013.12.002     Document Type: Review

References (196)

1. T. Lopes da Fonseca et al. The zebrafish homologue of Parkinson's disease ATP13A2 is essential for embryonic survival Brain Res. Bull. 90 2013 118 126
2. M.F. Suen et al. Assessments of the effects of nicotine and ketamine using tyrosine hydroxylase-green fluorescent protein transgenic zebrafish as biosensors Biosens. Bioelectron. 42 2013 177 185
3. R. Gerlai A small fish with a big future: zebrafish in behavioral neuroscience Rev. Neurosci. 22 2011 3 4
4. R. Gerlai Zebrafish antipredatory responses: a future for translational research? Behav. Brain Res. 207 2010 223 231
5. R. Gerlai High-throughput behavioral screens: the first step towards finding genes involved in vertebrate brain function using zebrafish Molecules 15 2010 2609 2622
6. K. Howe et al. The zebrafish reference genome sequence and its relationship to the human genome Nature 496 2013 498 503
7. C. Laggner et al. Chemical informatics and target identification in a zebrafish phenotypic screen Nat. Chem. Biol. 8 2012 144 146
8. D. Kokel, and R.T. Peterson Using the zebrafish photomotor response for psychotropic drug screening Methods Cell Biol. 105 2011 517 524
9. D. Kokel, and R.T. Peterson Chemobehavioural phenomics and behaviour-based psychiatric drug discovery in the zebrafish Brief. Funct. Genomic Proteomic 7 2008 483 490
10. S. Ali et al. Behavioral profiling of zebrafish embryos exposed to a panel of 60 water-soluble compounds Behav. Brain Res. 228 2012 272 283
11. R.C. Kessler et al. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication Arch. Gen. Psychiatry 62 2005 593 602
12. L. Ziv et al. An affective disorder in zebrafish with mutation of the glucocorticoid receptor Mol. Psychiatry 18 2013 681 691
13. B.B. Griffiths et al. A zebrafish model of glucocorticoid resistance shows serotonergic modulation of the stress response Front. Behav. Neurosci. 6 2012 68
14. C.O. Bondi et al. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment Neuropsychopharmacology 33 2008 320 331
15. A.L. Piato et al. Unpredictable chronic stress model in zebrafish (Danio rerio): behavioral and physiological responses Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 561 567
16. S. Chakravarty et al. Chronic unpredictable stress (CUS)-induced anxiety and related mood disorders in a zebrafish model: altered brain proteome profile implicates mitochondrial dysfunction PLoS ONE 8 2013 e63302
17. E. Kyzar et al. Behavioral effects of bidirectional modulators of brain monoamines reserpine and d-amphetamine in zebrafish Brain Res. 1527 2013 108 116
18. J. Gerlai, and R. Gerlai Autism: a large unmet medical need and a complex research problem Physiol. Behav. 79 2003 461 470
19. D.I. Zafeiriou et al. Autism spectrum disorders: the quest for genetic syndromes Am. J. Med. Genet. B: Neuropsychiatr. Genet. 162B 2013 327 366
20. A.M. Stewart et al. Developing zebrafish models of autism spectrum disorder (ASD) Prog. Neuropsychopharmacol. Biol. Psychiatry 50 2014 27 36
21. A. Blaker-Lee et al. Zebrafish homologs of genes within 16p11.2, a genomic region associated with brain disorders, are active during brain development, and include two deletion dosage sensor genes Dis. Model Mech. 5 2012 834 851
22. J.D. Rudie et al. Autism-associated promoter variant in MET impacts functional and structural brain networks Neuron 75 2012 904 915
23. X. Zhou et al. Replication of the association of a MET variant with autism in a Chinese Han population PLoS ONE 6 2011 e27428
24. G.E. Elsen et al. The autism susceptibility gene met regulates zebrafish cerebellar development and facial motor neuron migration Dev. Biol. 335 2009 78 92
25. W.H. Norton Toward developmental models of psychiatric disorders in zebrafish Front. Neural Circuits 7 2013 79
26. V. Tropepe, and H.L. Sive Can zebrafish be used as a model to study the neurodevelopmental causes of autism? Genes Brain Behav. 2 2003 268 281
27. N. Miller, and R. Gerlai From schooling to shoaling: patterns of collective motion in zebrafish (Danio rerio) PLoS ONE 7 2012 e48865
28. N.Y. Miller, and R. Gerlai Shoaling in zebrafish: what we don't know Rev. Neurosci. 22 2011 17 25
29. N. Miller, and R. Gerlai Quantification of shoaling behaviour in zebrafish (Danio rerio) Behav. Brain Res. 184 2007 157 166
30. H. Maaswinkel et al. Assessing social engagement in heterogeneous groups of zebrafish: a new paradigm for autism-like behavioral responses PLoS ONE 8 2013 e75955
31. C. Buske, and R. Gerlai Early embryonic ethanol exposure impairs shoaling and the dopaminergic and serotoninergic systems in adult zebrafish Neurotoxicol. Teratol. 33 2011 698 707
32. D. Wright, and J. Krause Repeated measures of shoaling tendency in zebrafish (Danio rerio) and other small teleost fishes Nat. Protoc. 1 2006 1828 1831
33. S. Mahabir et al. Maturation of shoaling in two zebrafish strains: a behavioral and neurochemical analysis Behav. Brain Res. 247 2013 1 8
34. M. Saif et al. Sight of conspecific images induces changes in neurochemistry in zebrafish Behav. Brain Res. 243 2013 294 299
35. C. Buske, and R. Gerlai Maturation of shoaling behavior is accompanied by changes in the dopaminergic and serotoninergic systems in zebrafish Dev. Psychobiol. 54 2012 28 35
36. C. Buske, and R. Gerlai Shoaling develops with age in Zebrafish (Danio rerio) Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 1409 1415
37. S.J. Schmidt et al. Social cognition as a mediator variable between neurocognition and functional outcome in schizophrenia: empirical review and new results by structural equation modeling Schizophr. Bull. 37 Suppl. 2 2011 S41 S54
38. J.L. Hames et al. Interpersonal processes in depression Annu. Rev. Clin. Psychol. 9 2013 355 377
39. D.V. Iosifescu The relation between mood, cognition and psychosocial functioning in psychiatric disorders Eur. Neuropsychopharmacol. 22 Suppl. 3 2012 S499 S504
40. T. Burne et al. Big ideas for small brains: what can psychiatry learn from worms, flies, bees and fish? Mol. Psychiatry 16 2011 7 16
41. A. Stewart et al. Zebrafish models to study drug abuse-related phenotypes Rev. Neurosci. 22 2011 95 105
42. J. Cachat et al. Modeling withdrawal syndrome in zebrafish Behav. Brain Res. 208 2010 371 376
43. S. Tran, and R. Gerlai Time-course of behavioural changes induced by ethanol in zebrafish (Danio rerio) Behav. Brain Res. 252 2013 204 213
44. R. Gerlai et al. Acute and chronic alcohol dose: population differences in behavior and neurochemistry of zebrafish Genes Brain Behav. 8 2009 586 599
45. R. Gerlai et al. Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects Pharmacol. Biochem. Behav. 67 2000 773 782
46. R. Gerlai et al. Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio) Pharmacol. Biochem. Behav. 85 2006 752 761
47. Y. Pan et al. Chronic alcohol exposure induced gene expression changes in the zebrafish brain Behav. Brain Res. 216 2011 66 76
48. P. Thoma et al. Empathy and social problem solving in alcohol dependence, mood disorders and selected personality disorders Neurosci. Biobehav. Rev. 37 2013 448 470
49. N. Miller et al. Effects of nicotine and alcohol on zebrafish (Danio rerio) shoaling Behav. Brain Res. 240 2013 192 196
50. M.J. Carvan 3rd et al. Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis Neurotoxicol. Teratol. 26 2004 757 768
51. F.J. Arenzana et al. Teratogenic effects of ethanol exposure on zebrafish visual system development Neurotoxicol. Teratol. 28 2006 342 348
52. Y. Fernandes, and R. Gerlai Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish Alcohol. Clin. Exp. Res. 33 2009 601 609
53. H.A. Puttonen et al. Acute ethanol treatment upregulates th1, th2, and hdc in larval zebrafish in stable networks Front. Neural Circuits 7 2013 102
54. V. Vengeliene et al. Neuropharmacology of alcohol addiction Br. J. Pharmacol. 154 2008 299 315
55. E. Tupala, and J. Tiihonen Dopamine and alcoholism: neurobiological basis of ethanol abuse Prog. Neuropsychopharmacol. Biol. Psychiatry 28 2004 1221 1247
56. P.W. Kalivas, and J. Stewart Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity Brain Res. Brain Res. Rev. 16 1991 223 244
57. D. Chatterjee, and R. Gerlai High precision liquid chromatography analysis of dopaminergic and serotoninergic responses to acute alcohol exposure in zebrafish Behav. Brain Res. 200 2009 208 213
58. D. Chatterjee et al. Chronic and acute alcohol administration induced neurochemical changes in the brain: comparison of distinct zebrafish populations Amino Acids 2014 PMID: 24381007
59. Y.C. Chen et al. Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish Histochem. Cell Biol. 132 2009 375 381
60. O. Anichtchik et al. Distinct structure and activity of monoamine oxidase in the brain of zebrafish (Danio rerio) J. Comp. Neurol. 498 2006 593 610
61. B.K. Arslan, and D.E. Edmondson Expression of zebrafish (Danio rerio) monoamine oxidase (MAO) in Pichia pastoris: purification and comparison with human MAO A and MAO B Protein Expr. Purif. 70 2010 290 297
62. D.J. Nutt et al. Effects of Schedule I drug laws on neuroscience research and treatment innovation Nat. Rev. Neurosci. 14 2013 577 585
63. A.M. Stewart, and A.V. Kalueff Controlled substances and innovation of biomedicine Nat. Rev. Neurosci. 14 2013 877
64. M.A. Geyer Why study hallucinogenic drugs in animals? Heffer Rev. Psychedel. Res. 1 1998 33 38
65. N. Neelkantan et al. Perspectives on zebrafish models of hallucinogenic drugs and related psychotropic compounds ACS Chem. Neurosci. 4 2013 1137 1150
66. S.H. Lee et al. Cardiovascular risk assessment of atypical antipsychotic drugs in a zebrafish model J. Appl. Toxicol. 33 2013 466 470
67. J. Cachat et al. Unique and potent effects of acute ibogaine on zebrafish: the developing utility of novel aquatic models for hallucinogenic drug research Behav. Brain Res. 236 2013 258 269
68. S.M. Zakhary et al. A behavioral and molecular analysis of ketamine in zebrafish Synapse 65 2011 160 167
69. R. Riehl et al. Behavioral and physiological effects of acute ketamine exposure in adult zebrafish Neurotoxicol. Teratol. 33 2011 658 667
70. D. Braida et al. Hallucinatory and rewarding effect of salvinorin A in zebrafish: κ-opioid and CB1-cannabinoid receptor involvement Psychopharmacology (Berl.) 190 2007 441 448
71. K.J. Seibt et al. Antipsychotic drugs reverse MK-801-induced cognitive and social interaction deficits in zebrafish (Danio rerio) Behav. Brain Res. 224 2011 135 139
72. K.J. Seibt et al. Antipsychotic drugs prevent the motor hyperactivity induced by psychotomimetic MK-801 in zebrafish (Danio rerio) Behav. Brain Res. 214 2010 417 422
73. L.D. Ellis, and K.H. Soanes A larval zebrafish model of bipolar disorder as a screening platform for neuro-therapeutics Behav. Brain Res. 233 2012 450 457
74. J.W. Young et al. Animal models of schizophrenia Curr. Top. Behav. Neurosci. 4 2010 391 433
75. B. Moghaddam, and J.H. Krystal Capturing the angel in "angel dust": twenty years of translational neuroscience studies of NMDA receptor antagonists in animals and humans Schizophr. Bull. 38 2012 942 949
76. T. Rubino, and D. Parolaro Cannabis abuse in adolescence and the risk of psychosis: a brief review of the preclinical evidence Prog. Neuropsychopharmacol. Biol. Psychiatry 2013 10.1016/j.pnpbp.2013.07.020
77. J. Chen et al. The behavioral and pharmacological actions of NMDA receptor antagonism are conserved in zebrafish larvae Int. J. Comp. Psychol. 23 2010 82 90
78. A.V. Kalueff et al. Perspectives on genetic animal models of serotonin toxicity Neurochem. Int. 52 2008 649 658
79. A.M. Stewart et al. Perspectives on experimental models of serotonin syndrome in zebrafish Neurochem. Int. 62 2013 893 902
80. R. Haberzettl et al. Animal models of the serotonin syndrome: a systematic review Behav. Brain Res. 256C 2013 328 345
81. Cross-Disorder Group of the Psychiatric Genomics et al. Genetic relationship between five psychiatric disorders estimated from genome-wide SNPs Nat. Genet. 45 2013 984 994
82. A. Meyer-Lindenberg, and D.R. Weinberger Intermediate phenotypes and genetic mechanisms of psychiatric disorders Nat. Rev. Neurosci. 7 2006 818 827
83. S.D. Norrholm, and K.J. Ressler Genetics of anxiety and trauma-related disorders Neuroscience 164 2009 272 287
84. X. Li et al. Genes associated with autism spectrum disorder Brain Res. Bull. 88 2012 543 552
85. A.V. Kalueff et al. Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond Zebrafish 10 2013 70 86
86. Y. Shimada et al. A high-throughput fluorescence-based assay system for appetite-regulating gene and drug screening PLoS ONE 7 2012 e52549
87. T.W. Chen et al. Ultrasensitive fluorescent proteins for imaging neuronal activity Nature 499 2013 295 300
88. G. Polverino et al. Zebrafish response to robotic fish: preference experiments on isolated individuals and small shoals Bioinspir. Biomim. 7 2012 036019
89. N. Abaid et al. Zebrafish responds differentially to a robotic fish of varying aspect ratio, tail beat frequency, noise, and color Behav. Brain Res. 233 2012 545 553
90. C.A. Oomen et al. The touchscreen operant platform for testing working memory and pattern separation in rats and mice Nat. Protoc. 8 2013 2006 2021
91. A.C. Mar et al. The touchscreen operant platform for assessing executive function in rats and mice Nat. Protoc. 8 2013 1985 2005
92. T.J. Bussey et al. New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats Neuropharmacology 62 2012 1191 1203
93. M. Sison et al. Fishing for genes influencing vertebrate behavior: zebrafish making headway Lab Anim. (N.Y.) 35 2006 33 39
94. E.J. Nestler, and S.E. Hyman Animal models of neuropsychiatric disorders Nat. Neurosci. 13 2010 1161 1169
95. A.V. Kalueff et al. Domain interplay concept in animal models of neuropsychiatric disorders: a new strategy for high-throughput neurophenotyping research Behav. Brain Res. 188 2008 243 249
96. J.L. LaPorte et al. Qui non proficit, deficit: experimental models for 'integrative' research of affective disorders J. Affect. Disord. 121 2010 1 9
97. J.M. Goldstein et al. Validity: definitions and applications to psychiatric research M.T. Tsuang, Textbook in Psychiatric Epidemiology 2011 Wiley 99 116
98. M. Hosozawa et al. How children with specific language impairment view social situations: an eye tracking study Pediatrics 129 2012 e1453 e1460
99. S.J. Webb et al. ERP responses differentiate inverted but not upright face processing in adults with ASD Soc. Cogn. Affect. Neurosci. 7 2012 578 587
100. D.M. Riby et al. Brief report: faces cause less distraction in autism J. Autism Dev. Disord. 42 2012 634 639
101. M.O. Parker et al. Development and automation of a test of impulse control in zebrafish Front. Syst. Neurosci. 7 2013 65
102. M.O. Parker et al. Discrimination reversal and attentional sets in zebrafish (Danio rerio) Behav. Brain Res. 232 2012 264 268
103. M.O. Parker et al. Development and implementation of a three-choice serial reaction time task for zebrafish (Danio rerio) Behav. Brain Res. 227 2012 73 80
104. D.J. Echevarria et al. Assessing attention in the zebrafish: Are we there yet? Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 1416 1420
105. K.D. Mann et al. Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues Biol. Bull. 205 2003 224 225
106. C. Hinz et al. Olfactory imprinting is triggered by MHC peptide ligands Sci. Rep. 3 2013 2800
107. C. Hinz et al. Influence of kinship and MHC class II genotype on visual traits in zebrafish larvae (Danio rerio) PLoS ONE 7 2012 e51182
108. G. Gerlach et al. Kin recognition in zebrafish: a 24-hour window for olfactory imprinting Proc. Biol. Sci. 275 2008 2165 2170
109. M.C. Teles et al. Social modulation of brain monoamine levels in zebrafish Behav. Brain Res. 253 2013 17 24
110. R.F. Oliveira et al. Fighting zebrafish: characterization of aggressive behavior and winner-loser effects Zebrafish 8 2011 73 81
111. I.V. Zhdanova et al. Aging of the circadian system in zebrafish and the effects of melatonin on sleep and cognitive performance Brain Res. Bull. 75 2008 433 441
112. L. Yu et al. Cognitive aging in zebrafish PLoS ONE 1 2006 e14
113. A.M. Stewart, and A.V. Kalueff The developing utility of zebrafish models for cognitive enhancers research Curr. Neuropharmacol. 10 2012 263 271
114. M. Nguyen et al. Developing 'integrative' zebrafish models of behavioral and metabolic disorders Behav. Brain Res. 256 2013 172 187
115. A.D. Collier, and D.J. Echevarria The utility of the zebrafish model in conditioned place preference to assess the rewarding effects of drugs Behav. Pharmacol. 24 2013 375 383
116. S. Bretaud et al. A choice behavior for morphine reveals experience-dependent drug preference and underlying neural substrates in developing larval zebrafish Neuroscience 146 2007 1109 1116
117. B. Lau et al. Dissociation of food and opiate preference by a genetic mutation in zebrafish Genes Brain Behav. 5 2006 497 505
118. J. Ninkovic et al. Genetic identification of AChE as a positive modulator of addiction to the psychostimulant D-amphetamine in zebrafish J. Neurobiol. 66 2006 463 475
119. C.H. Brennan Zebrafish behavioural assays of translational relevance for the study of psychiatric disease Rev. Neurosci. 22 2011 37 48
120. L.J. Kily et al. Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways J. Exp. Biol. 211 2008 1623 1634
121. J. Sackerman et al. Zebrafish behavior in novel environments: effects of acute exposure to anxiolytic compounds and choice of Danio rerio line Int. J. Comp. Psychol. 23 2010 43 61
122. R.J. Egan et al. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish Behav. Brain Res. 205 2009 38 44
123. A.S. Mathuru, and S. Jesuthasan The medial habenula as a regulator of anxiety in adult zebrafish Front. Neural Circuits 7 2013 99
124. A. Stewart et al. Modeling anxiety using adult zebrafish: a conceptual review Neuropharmacology 62 2012 135 143
125. H. Okamoto et al. Genetic dissection of the zebrafish habenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety Dev. Neurobiol. 72 2012 386 394
126. R.E. Blaser, and D.B. Rosemberg Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test PLoS ONE 7 2012 e36931
127. H. Richendrfer et al. On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae Behav. Brain Res. 228 2012 99 106
128. W. Norton, and L. Bally-Cuif Adult zebrafish as a model organism for behavioural genetics BMC Neurosci. 2 2010 90
129. M.E. Oswald et al. The quantitative genetic architecture of the bold-shy continuum in zebrafish, Danio rerio PLoS ONE 8 2013 e68828
130. R.E. Drew et al. Brain transcriptome variation among behaviorally distinct strains of zebrafish (Danio rerio) BMC Genomics 13 2012 323
131. B.Y. Lau et al. Identification of a brain center whose activity discriminates a choice behavior in zebrafish Proc. Natl. Acad. Sci. U.S.A. 108 2011 2581 2586
132. A.V. Kalueff et al. What's wrong with my mouse model? Advances and strategies in animal modeling of anxiety and depression Behav. Brain Res. 179 2007 1 18
133. R.E. Engeszer et al. Zebrafish in the wild: a review of natural history and new notes from the field Zebrafish 4 2007 21 40
134. M. Arunachalam et al. Natural history of zebrafish (Danio rerio) in India Zebrafish 10 2013 1 14
135. R. Spence et al. The behaviour and ecology of the zebrafish, Danio rerio Biol. Rev. Camb. Philos. Soc. 83 2008 13 34
136. M.T. Akhtar et al. Developmental effects of cannabinoids on zebrafish larvae Zebrafish 10 2013 283 293
137. P.J. Steenbergen et al. The use of the zebrafish model in stress research Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 1432 1451
138. C.A. Beretta et al. Habenula circuit development: past, present, and future Front. Neurosci. 6 2012 51
139. L. Welberg Psychiatric disorders: Reining in the habenula? Nat. Rev. Neurosci. 14 2013 668 669
140. P. Panula et al. Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases Zebrafish 3 2006 235 247
141. J.B. Pippal et al. Characterization of the zebrafish (Danio rerio) mineralocorticoid receptor Mol. Cell. Endocrinol. 332 2011 58 66
142. S.C. Baraban et al. Drug screening in Scn1a zebrafish mutant identifies clemizole as a potential Dravet syndrome treatment Nat. Commun. 4 2013 2410
143. E.E. Patton, and L.I. Zon The art and design of genetic screens: zebrafish Nat. Rev. Genet. 2 2001 956 966
144. A. Amsterdam, and N. Hopkins Mutagenesis strategies in zebrafish for identifying genes involved in development and disease Trends Genet. 22 2006 473 478
145. S. Sivasubbu et al. Insertional mutagenesis strategies in zebrafish Genome Biol. 8 Suppl. 1 2007 S9
146. J. Heintze et al. A CRISPR CASe for high-throughput silencing Front. Genet. 4 2013 193
147. A. Hruscha et al. Efficient CRISPR/Cas9 genome editing with low off-target effects in zebrafish Development 140 2013 4982 4987
148. B.R. Bill et al. A primer for morpholino use in zebrafish Zebrafish 6 2009 69 77
149. C.B. Moens et al. Reverse genetics in zebrafish by TILLING Brief. Funct. Genomic Proteomic 7 2008 454 459
150. T. Cermak et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting Nucleic Acids Res. 39 2011 e82
151. K.J. Clark et al. A TALE of two nucleases: gene targeting for the masses? Zebrafish 8 2011 147 149
152. D. Wright et al. Epistatic regulation of behavioural and morphological traits in the zebrafish (Danio rerio) Behav. Genet. 36 2006 914 922
153. D. Wright et al. QTL analysis of behavioral and morphological differentiation between wild and laboratory zebrafish (Danio rerio) Behav. Genet. 36 2006 271 284
154. E. Chen, and S.C. Ekker Zebrafish as a genomics research model Curr. Pharm. Biotechnol. 5 2004 409 413
155. J. Cachat et al. Three-dimensional neurophenotyping of adult zebrafish behavior PLoS ONE 6 2011 e17597
156. K. Wong et al. Modeling seizure-related behavioral and endocrine phenotypes in adult zebrafish Brain Res. 1348 2010 209 215
157. L. Grossman et al. Characterization of behavioral and endocrine effects of LSD on zebrafish Behav. Brain Res. 214 2010 277 284
158. J. Green et al. Automated high-throughput neurophenotyping of zebrafish social behavior J. Neurosci. Methods 210 2012 266 271
159. S. Jesuthasan Fear, anxiety and control in the zebrafish Dev. Neurobiol. 72 2012 395 403
160. R.E. Blaser et al. Behavioral measures of anxiety in zebrafish (Danio rerio) Behav. Brain Res. 208 2010 56 62
161. C. Maximino et al. Measuring anxiety in zebrafish: a critical review Behav. Brain Res. 214 2010 157 171
162. C. Maximino et al. Parametric analyses of anxiety in zebrafish scototaxis Behav. Brain Res. 210 2010 1 7
163. A.M. Stewart et al. Constructing the habituome for phenotype-driven zebrafish research Behav. Brain Res. 236 2013 110 117
164. K. Wong et al. Analyzing habituation responses to novelty in zebrafish (Danio rerio) Behav. Brain Res. 208 2010 450 457
165. H.A. Burgess, and M. Granato Sensorimotor gating in larval zebrafish J. Neurosci. 27 2007 4984 4994
166. M. Lange et al. The ADHD-susceptibility gene lphn3.1 modulates dopaminergic neuron formation and locomotor activity during zebrafish development Mol. Psychiatry 17 2012 946 954
167. S. Gaikwad et al. Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: the utility of fish models to study stress-memory interplay Behav. Processes 87 2011 224 230
168. V. Gonzalez-Nunez, and R.E. Rodriguez The zebrafish: a model to study the endogenous mechanisms of pain ILAR J. 50 2009 373 386
169. L.U. Sneddon Pain perception in fish: indicators and endpoints ILAR J. 50 2009 338 342
170. F. Macho Sanchez-Simon, and R.E. Rodriguez Expression of the nociceptin receptor during zebrafish development: influence of morphine and nociceptin Int. J. Dev. Neurosci. 27 2009 315 320
171. A.M. Stewart et al. Perspectives of zebrafish models of epilepsy: what, how and where next? Brain Res. Bull. 87 2012 135 143
172. G.A. Hortopan, and S.C. Baraban Aberrant expression of genes necessary for neuronal development and notch signaling in an epileptic mind bomb zebrafish Dev. Dyn. 240 2011 1964 1976
173. G. Sallai Combined captopril treatment in severe and moderately severe hypertension resistant to therapy Acta Physiol. Hung. 72 Suppl. 1988 45 50
174. S.A. Budick, and D.M. O'Malley Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture J. Exp. Biol. 203 2000 2565 2579
175. I.V. Zhdanova Sleep and its regulation in zebrafish Rev. Neurosci. 22 2011 27 36
176. J. Rihel et al. Monitoring sleep and arousal in zebrafish Methods Cell Biol. 100 2010 281 294
177. L. Appelbaum et al. Sleep-wake regulation and hypocretin-melatonin interaction in zebrafish Proc. Natl. Acad. Sci. U.S.A. 106 2009 21942 21947
178. T. Yokogawa et al. Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants PLoS Biol. 5 2007 e277
179. R. Jones Let sleeping zebrafish lie: a new model for sleep studies PLoS Biol. 5 2007 e281
180. I.V. Zhdanova Sleep in zebrafish Zebrafish 3 2006 215 226
181. I.V. Zhdanova et al. Melatonin promotes sleep-like state in zebrafish Brain Res. 903 2001 263 268
182. K.S. Robinson et al. Psychopharmacological effects of acute exposure to kynurenic acid (KYNA) in zebrafish Pharmacol. Biochem. Behav. 108C 2013 54 60
183. A. Bisaga, and P. Popik In search of a new pharmacological treatment for drug and alcohol addiction: N-methyl-d-aspartate (NMDA) antagonists Drug Alcohol Depend. 59 2000 1 15
184. E.J. Kyzar et al. Effects of hallucinogenic agents mescaline and phencyclidine on zebrafish behavior and physiology Prog. Neuropsychopharmacol. Biol. Psychiatry 37 2012 194 202
185. W. Boehmler et al. D4 Dopamine receptor genes of zebrafish and effects of the antipsychotic clozapine on larval swimming behaviour Genes Brain Behav. 6 2007 155 166
186. A. Stewart et al. Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 1421 1431
187. Z. Bencan et al. Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety Pharmacol. Biochem. Behav. 94 2009 75 80
188. R.Y. Wong et al. Behavioral and neurogenomic transcriptome changes in wild-derived zebrafish with fluoxetine treatment BMC Genomics 14 2013 348
189. J. Cowden et al. Developmental exposure to valproate and ethanol alters locomotor activity and retino-tectal projection area in zebrafish embryos Reprod. Toxicol. 33 2012 165 173
190. J. Peng et al. Ethanol-modulated camouflage response screen in zebrafish uncovers a novel role for cAMP and extracellular signal-regulated kinase signaling in behavioral sensitivity to ethanol J. Neurosci. 29 2009 8408 8418
191. C.A. Dlugos, and R.A. Rabin Ethanol effects on three strains of zebrafish: model system for genetic investigations Pharmacol. Biochem. Behav. 74 2003 471 480
192. D.B. Rosemberg et al. Behavioral effects of taurine pretreatment in zebrafish acutely exposed to ethanol Neuropharmacology 63 2012 613 623
193. B.H. Mussulini et al. Seizures induced by pentylenetetrazole in the adult zebrafish: a detailed behavioral characterization PLoS ONE 8 2013 e54515
194. S. Sierra et al. Administration of docosahexaenoic acid before birth and until aging decreases kainate-induced seizures in adult zebrafish Brain Res. Bull. 88 2012 467 470
195. A.D. Correia et al. A novel behavioral fish model of nociception for testing analgesics Pharmaceuticals 4 2011 665 680
196. L. Grossman et al. Effects of piracetam on behavior and learning in adult zebrafish Brain Res. Bull. 85 2011 58 63