Learning and memory in zebrafish (Danio rerio)

Methods in Cell Biology

Volumn 134, Issue , 2016, Pages 551-586

  Gerlai, R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Appetitive conditioning; Associative learning; Aversive conditioning; Behavioral phenotyping; Conditioning; High throughput screening; Memory; Memory consolidation; Motivation; Relational learning; Spatial learning

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; CENTRAL NERVOUS SYSTEM; COGNITIVE DEFECT; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; LEARNING; MEMORY; NEUROBIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; ZEBRA FISH;

ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; LEARNING; MEMORY; NEUROBIOLOGY; ZEBRAFISH;

EID: 84959471363     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.mcb.2016.02.005     Document Type: Article

References (102)

1. Ahmed T.S., Fernandes Y., Gerlai R. Effects of animated images of sympatric predators and abstract shapes on fear responses in zebrafish. Behaviour 2012, 149:1125-1153.
2. Aizenberg M., Schuman E.M. Cerebellar-dependent learning in larval zebrafish. Journal of Neuroscience 2011, 31:8708-8712.
3. Al-Imari L., Gerlai R. Conspecifics as reward in associative learning tasks for zebrafish (Danio rerio). Behavioural Brain Research 2008, 189:216-219.
4. Andersson M.Å., Ek F., Olsson R. Using visual lateralization to model learning and memory in zebrafish larvae. Scientific Reports 2015, 5:8667. 10.1038/srep08667.
5. Aoki R., Tsuboi T., Okamoto H. Y-maze avoidance: an automated and rapid associative learning paradigm in zebrafish. Neurosciences Research 2015, 91:69-72.
6. Babinet C., Morello D., Renard J.P. Transgenic mice. Genome 1989, 31:938-949.
7. Bass S.L.S., Gerlai R. Zebrafish (Danio rerio) responds differentially to stimulus fish: the effects of sympatric and allopatric predators and harmless fish. Behavioural Brain Research 2008, 186:107-117.
8. Berridge K.C. Food reward: brain substrates of wanting and liking. Neuroscience and Biobehavioral Reviews 1996, 20:1-25.
9. Best J.D., Berghmans S., Hunt J.J., Clarke S.C., Fleming A., Goldsmith P., Roach A.G. Non-associative learning in larval zebrafish. Neuropsychopharmacology 2008, 33:1206-1215.
10. Bilotta J., Risner M.L., Davis E.C., Haggbloom S.J. Assessing appetitive choice discrimination learning in zebrafish. Zebrafish 2005, 2:259-268.
11. Blackburn P.R., Campbell J.M., Clark K.J., Ekker S.C. The CRISPR system-keeping zebrafish gene targeting fresh. Zebrafish 2013, 10:116-118.
12. Blank M., Guerim L.D., Cordeiro R.F., Vianna M.R. A one-trial inhibitory avoidance task to zebrafish: rapid acquisition of an NMDA-dependent long-term memory. Neurobiology of Learning and Memory 2009, 92:529-534.
13. Blaser R.E., Chadwick L., McGinnis G.C. Behavioral measures of anxiety in zebrafish (Danio rerio). Behavioural Brain Research 2010, 208:56-62.
14. Blaser R., Gerlai R. Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods. Behavior Research Methods 2006, 38:456-469.
15. Braubach O.R., Wood H.D., Gadbois S., Fine A., Croll R.P. Olfactory conditioning in the zebrafish (Danio rerio). Behavioural Brain Research 2009, 198:190-198.
16. Capiotti K.M., De Moraes D.A., Menezes F.P., Kist L.W., Bogo M.R., Da Silva R.S. Hyperglycemia induces memory impairment linked to increased acetylcholinesterase activity in zebrafish (Danio rerio). Behavioural Brain Research 2014, 274:319-325.
17. Chakraborty C., Hsu C.H., Wen Z.H., Lin C.S., Agoramoorthy G. Zebrafish: a complete animal model for in vivo drug discovery and development. Current Drug Metabolism 2009, 10:116-124.
18. Clark K.J., Voytas D.F., Ekker S.C. A TALE of two nucleases: gene targeting for the masses?. Zebrafish 2011, 8:147-149.
19. Colwill R.M., Raymond M.P., Ferreira L., Escudero H. Visual discrimination learning in zebrafish (Danio rerio). Behavioural Processes 2005, 70:19-31.
20. Crusio W.E., van Abeelen J.H. The genetic architecture of behavioural responses to novelty in mice. Heredity 1986, 56:55-63.
21. Díaz E. From microarrays to mechanisms of brain development and function. Biochemical and Biophysical Research 2009, 385:129-131.
22. Dickerson B.C., Eichenbaum H. The episodic memory system: neurocircuitry and disorders. Neuropsychopharmacology 2010, 35:86-104.
23. Eddins D., Petro A., Williams P., Cerutti D.T., Levin E.D. Nicotine effects on learning in zebrafish: the role of dopaminergic systems. Psychopharmacology 2009, 202:103-109.
24. Eichenbaum H. Remembering: functional organization of the declarative memory system. Current Biology 2006, 16:R643-R645.
25. Endeman D., Klaassen L.J., Kamermans M. Action spectra of zebrafish cone photoreceptors. PLoS One 2013, 8:e68540. 10.1371/journal.pone.0068540.
26. Engeszer R.E., Barbiano L.A., Ryan M.J., Parichy D.M. Timing and plasticity of shoaling behaviour in the zebrafish, Danio rerio. Animal Behaviour 2007, 74:1269-1275.
27. Engeszer R.E., Patterson L.B., Rao A.A., Parichy D.M. Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 2007, 4:21-40.
28. Fadool J.M., Dowling J.E. Zebrafish: a model system for the study of eye genetics. Progress in Retinal and Eye Research 2008, 27:89-110.
29. Fernandes Y., Gerlai R. Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcoholism: Clinical and Experimental Research 2009, 33:601-609.
30. Fernandes Y., Talpos A., Gerlai R. Towards the characterization of short-term memory of zebrafish: effect of fixed versus random reward location. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2015, 56:189-195.
31. Fritzsch B. Of mice and genes: evolution of vertebrate brain development. Brain Behavior and Evolution 1998, 52:207-217.
32. Ganz J., Kaslin J., Freudenreich D., Machate A., Geffarth M., Brand M. Subdivisions of the adult zebrafish subpallium by molecular marker analysis. Journal of Comparative Neurology 2012, 520:633-655.
33. Gerlai R. Contextual learning and cue association in fear conditioning in mice: a strain comparison and a lesion study. Behavioural Brain Research 1998, 95:191-203.
34. Gerlai R. Behavioral tests of hippocampal function: simple paradigms, complex problems. Behavioural Brain Research 2001, 125:269-277.
35. Gerlai R. Phenomics: fiction or the future?. Trends in Neurosciences 2002, 25:506-509.
36. Gerlai R. High-throughput behavioral screens: the first step towards finding genes involved in vertebrate brain function using zebrafish. Molecules 2010, 15:2609-2622.
37. Gerlai R. Zebrafish phenomics: behavioral screens and phenotyping of mutagenized fish. Current Opinion in Behavioral Sciences 2014, 2:21-27.
38. Gerlai R. Fish in behavior research: unique tools with a great promise!. Journal of Neuroscience Methods 2014, 234:54-58.
39. Gerlai R., Chatterjee D., Pereira T., Sawashima T., Krishnannair R. Acute and chronic alcohol dose: population differences in behavior and neurochemistry of zebrafish. Genes, Brain and Behavior 2009, 8:586-599.
40. Gerlai R., Clayton N.S. Analysing hippocampal function in transgenic mice: an ethological perspective. Trends in Neurosciences 1999, 22:47-51.
41. Gerlai R., Crusio W.E., Csányi V. Inheritance of species specific behaviors in the paradise fish (Macropodus opercularis): a diallel study. Behavior Genetics 1990, 20:487-498.
42. Gerlai R., Fernandes Y., Pereira T. Zebrafish (Danio rerio) responds to the animated image of a predator: towards the development of an automated aversive task. Behavioural Brain Research 2009, 201:318-324.
43. Gerlai R., Hogan J.A. Learning to find the opponent: an ethological analysis of the behavior of paradise fish (Macropodus opercularis, Anabantidae) in intra- and inter-specific encounters. Journal of Comparative Psychology 1992, 106:306-315.
44. Gerlai R., McNamara A., Choi-Lundberg D., Powel-Braxton L., Phillips H.S. Impaired learning performance without altered dopaminergic function in mice heterozygous for the GDNF mutation. European Journal of Neuroscience 2001, 14:1153-1163.
45. Gómez-Laplaza L.M., Gerlai R. Latent learning in zebrafish (Danio rerio). Behavioural Brain Research 2010, 208:509-515.
46. Guo S. Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish?. Genes, Brain and Behavior 2004, 3:63-74.
47. Haffter P., Nüsslein-Volhard C. Large scale genetics in a small vertebrate, the zebrafish. International Journal of Developmental Biology 1996, 40:221-227.
48. Hall D., Suboski M.D. Visual and olfactory stimuli in learned release of alarm reactions by zebra danio fish (Brachydanio rerio). Neurobiology of Learning and Memory 1995, 63:229-240.
49. Hicks C., Sorocco D., Levin M. Automated analysis of behavior: a computer-controlled system for drug screening and the investigation of learning. Journal of Neurobiology 2006, 66:977-990.
50. Hinz F.I., Aizenberg M., Tushev G., Schuman E.M. Protein synthesis-dependent associative long-term memory in larval zebrafish. Journal of Neuroscience 2013, 33:15382-15387.
51. Hisano Y., Ota S., Kawahara A. Genome editing using artificial site-specific nucleases in zebrafish. Development Growth and Differentiation 2014, 56:26-33.
52. Howard M.W., Eichenbaum H. Time and space in the hippocampus. Brain Research 2015, 1621:345-354.
53. Jesuthasan S.J., Mathuru A.S. The alarm response in zebrafish: innate fear in a vertebrate genetic model. Journal of Neurogenetics 2008, 22:211-228.
54. Jia J., Fernandes Y., Gerlai R. Short-term memory in zebrafish (Danio rerio). Behavioural Brain Research 2014, 270:29-36.
55. Kalueff A.V., Gebhardt M., Stewart A.M., Cachat J.M., Brimmer M., Chawla J.S., the Zebrafish Neuroscience Research Consortium Towards a comprehensive catalog of zebrafish behavior 1.0, and beyond. Zebrafish 2013, 10:70-86.
56. Kalueff A.V., Stewart A.M., Gerlai R. Zebrafish as an emerging model for studying complex brain disorders. Trends in Pharmacological Sciences 2014, 35:63-75.
57. Karnik I., Gerlai R. Can zebrafish learn spatial tasks? an empirical analysis of place and single CS-US associative learning. Behavioural Brain Research 2012, 233:415-421.
58. Luca R., Gerlai R. Animated bird silhouette above the tank: acute alcohol diminishes fear responses in zebrafish. Behavioural Brain Research 2012, 229(15):194-201.
59. Luca R., Gerlai R. In search of optimal fear inducing stimuli: differential behavioral responses to computer animated images in zebrafish. Behavioural Brain Research 2012, 226:66-76.
60. Lucon-Xiccato T., Dadda M. Assessing memory in zebrafish using the one-trial test. Behavioural Processes 2014, 106:1-4.
61. Manabe K., Dooling R.J., Takaku S. Differential reinforcement of an approach response in zebrafish (Danio rerio). Behavioural Processes 2013, 98:106-111.
62. Manabe K., Dooling R.J., Takaku S. An automated device for appetitive conditioning in zebrafish (Danio rerio). Zebrafish 2013, 10:518-523.
63. Manuel R., Zethof J., Flik G., van den Bos R. Providing a food reward reduces inhibitory avoidance learning in zebrafish. Behavioural Processes 2015, 120:69-72.
64. May Z., Morrill A., Holcombe A., Johnston T., Gallup J., Fouad K., Hamilton T.J. Object recognition memory in zebrafish. Behavioural Brain Research 2015, 296:199-210.
65. Miller N., Gerlai R. Quantification of shoaling behaviour in zebrafish (Danio rerio). Behavioural Brain Research 2007, 184:157-166.
66. Miller N., Gerlai R. Redefining membership in animal groups. Behavior Research Methods 2011, 43:364-371.
67. Miller N., Gerlai R. From schooling to shoaling: patterns of collective motion in zebrafish (Danio rerio). PLoS One 2012, 7(11):e48865. 10.1371/journal.pone.0048865.
68. Mueller T., Dong Z., Berberoglu M.A., Guo S. The dorsal pallium in zebrafish, Danio rerio (Cyprinidae, Teleostei). Brain Research 2011, 1381:95-105.
69. Mueller K.P., Neuhauss S.C. Automated visual choice discrimination learning in zebrafish (Danio rerio). Journal of Integrative Neuroscience 2012, 11:73-85.
70. Mueller T., Wullimann M.F. An evolutionary interpretation of teleostean forebrain anatomy. Brain Behavior and Evolution 2009, 74:30-42.
71. Nam R.H., Kim W., Lee C.J. NMDA receptor-dependent long-term potentiation in the telencephalon of the zebrafish. Neuroscience Letters 2004, 370:248-251.
72. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Clarendon Press, Oxford.
73. O'Neale A., Ellis J., Creton R., Colwill R.M. Single stimulus learning in zebrafish larvae. Neurobiology of Learning and Memory 2014, 108:145-154.
74. Pan Y., Mo K., Razak Z., Westwood J.T., Gerlai R. Chronic alcohol exposure induced gene expression changes in the zebrafish brain. Behavioural Brain Research 2011, 216:66-76.
75. Parra K.V., Adrian J.C., Gerlai R. The synthetic substance hypoxanthine 3-N-oxide elicits alarm reactions in zebrafish (Danio rerio). Behavioural Brain Research 2009, 205:336-341.
76. Pather S., Gerlai R. Shuttle box learning in zebrafish. Behavioural Brain Research 2009, 196:323-327.
77. Patton E.E., Zon L.I. The art and design of genetic screens: zebrafish. Nature Reviews Genetics 2001, 2:956-966.
78. Phillips R.G., LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning and Memory 1994, 1:34-44.
79. Pradel G., Schachner M., Schmidt R. Inhibition of memory consolidation by antibodies against cell adhesion molecules after active avoidance conditioning in zebrafish. Journal of Neurobiology 1999, 39:197-206.
80. Qin M., Wong A., Seguin D., Gerlai R. Induction of social behaviour in zebrafish: live versus computer animated fish as stimuli. Zebrafish 2014, 11:185-197.
81. Rajan K.E., Ganesh A., Dharaneedharan S., Radhakrishnan K. Spatial learning-induced egr-1 expression in telencephalon of gold fish Carassius auratus. Fish Physiology and Biochemistry 2011, 37:153-159.
82. Reijmers L.G., Coats J.K., Pletcher M.T., Wiltshire T., Tarantino L.M., Mayford M. A mutant mouse with a highly specific contextual fear-conditioning deficit found in an N-ethyl-N-nitrosourea (ENU) mutagenesis screen. Learning and Memory 2006, 13:143-149.
83. Reimers M.J., Hahn M.E., Tanguay R.L. Two zebrafish alcohol dehydrogenases share common ancestry with mammalian class I, II, IV, and V alcohol dehydrogenase genes but have distinct functional characteristics. Journal of Biological Chemistry 2004, 279:38303-38312.
84. Renier C., Faraco J.H., Bourgin P., Motley T., Bonaventure P., Rosa F., Mignot E. Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenetics and Genomics 2007, 17:237-253.
85. Roberts A.C., Bill B.R., Glanzman D.L. Learning and memory in zebrafish larvae. Frontiers in Neural Circuits 2013, 7:126. 10.3389/fncir.2013.00126.
86. Salas C., Broglio C., Durán E., Gómez A., Ocaña F.M., Jiménez-Moya F., Rodríguez F. Neuropsychology of learning and memory in teleost fish. Zebrafish 2006, 3:157-171.
87. Saverino C., Gerlai R. The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behavioural Brain Research 2008, 191:77-87.
88. Shapiro M.L., Eichenbaum H. Hippocampus as a memory map: synaptic plasticity and memory encoding by hippocampal neurons. Hippocampus 1999, 9:365-384.
89. Sison M., Cawker J., Buske C., Gerlai R. Fishing for genes of vertebrate behavior: zebra fish as an upcoming model system. Laboratory Animals 2006, 35:33-39.
90. Speedie N., Gerlai R. Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behavioural Brain Research 2008, 188:168-177.
91. Sison M., Gerlai R. Associative learning in zebrafish (Danio rerio) in the plus maze. Behavioural Brain Research 2010, 207:99-104.
92. Sison M., Gerlai R. Associative learning performance is impaired in zebrafish (Danio rerio) by the NMDA-R antagonist MK-801. Neurobiology of Learning and Memory 2011, 96:230-237.
93. Sison M., Gerlai R. Behavioral performance altering effects of MK-801 in zebrafish (Danio rerio). Behavioural Brain Research 2011, 220:331-337.
94. Squire L.R. Memory systems of the brain: a brief history and current perspective. Neurobiology of Learning and Memory 2004, 82:171-177.
95. Stewart A.M., Ullmann J.F.P., Norton W.H., Brennan C.H., Parker M.O., Gerlai R., Kalueff A.W. Molecular psychiatry of zebrafish. Molecular Psychiatry 2014, 20:2-17.
96. Sweatt D. Mechanisms of memory 2010, 343. Elsevier, Amsterdam. 2nd ed.
97. von Trotha J.W., Vernier P., Bally-Cuif L. Emotions and motivated behavior converge on an amygdala-like structure in the zebrafish. European Journal of Neuroscience 2014, 40:3302-3315.
98. Tulving E. Multiple memory systems and consciousness. Human Neurobiology 1987, 6:67-80.
99. Valente A., Huang K.H., Portugues R., Engert F. Ontogeny of classical and operant learning behaviors in zebrafish. Learning and Memory 2012, 19:170-177.
100. Vargas R., Thorsteinsson H., Karlsson K.A. Spontaneous neural activity of the anterodorsal lobe and entopeduncular nucleus in adult zebrafish: a putative homologue of hippocampal sharp waves. Behavioural Brain Research 2012, 229:10-20.
101. Woodard W.T., Bitterman M.E. Pavlovian analysis of avoidance conditioning in the goldfish (Carassius auratus). Journal of Comparative and Physiological Psychology 1973, 82:123-129.
102. Xu X., Scott-Scheiern T., Kempker L., Simons K. Active avoidance conditioning in zebrafish (Danio rerio). Neurobiology of Learning and Memory 2007, 87:72-77.