Pharmacological analyses of learning and memory in zebrafish (Danio rerio)

Pharmacology Biochemistry and Behavior

Volumn 139, Issue , 2015, Pages 103-111

  Bailey, Jordan M ^a   Oliveri, Anthony N ^a   Levin, Edward D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Learning; Memory; Pharmacology; Zebrafish

Indexed keywords

ALCOHOL; CENTRAL STIMULANT AGENT; COCAINE; DIZOCILPINE; FLUOXETINE; NICOTINE; OLANZAPINE; OPIATE; PSYCHEDELIC AGENT; PSYCHOTROPIC AGENT; SCOPOLAMINE; SULPIRIDE;

ANIMAL BEHAVIOR; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIORAL PHARMACOLOGY; CONDITIONING; DRUG ABUSE; DRUG EFFECT; EXECUTIVE FUNCTION; HABITUATION; IMMERSION; IMPULSIVENESS; INTERVAL TIMING; LEARNING; LONG TERM MEMORY; MEMORY; MOTOR PERFORMANCE; NEUROBIOLOGY; NONHUMAN; PASSIVE AVOIDANCE; PHARMACOLOGY; PLACE PREFERENCE; PRIORITY JOURNAL; SALVIA; SELF CONTROL; SPATIAL DISCRIMINATION; STATE DEPENDENT LEARNING; SUBSTANCE ABUSE; VISUAL DISCRIMINATION; ZEBRA FISH; ANIMAL; ANIMAL MODEL; COGNITION; DRUG EFFECTS; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; COGNITION; EXECUTIVE FUNCTION; LEARNING; MEMORY; MODELS, ANIMAL; PSYCHOTROPIC DRUGS; ZEBRAFISH;

EID: 84949536842     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2015.03.006     Document Type: Review

References (82)

1. S. Ali, D.L. Champagne, H.P. Spaink, and M.K. Richardson Zebrafish embryos and larvae: a new generation of disease models and drug screens Birth Defects Res C Embryo Today 93 2 2011 115 133 10.1002/bdrc.20206
2. M. Antunes, and G. Biala The novel object recognition memory: neurobiology, test procedure, and its modifications Cogn Process 13 2 2012 93 110 10.1007/s10339-011-0430-z [May, Epub 2011 Dec 9]
3. D. Arthur, and E.D. Levin Spatial and non-spatial discrimination learning in zebrafish (Danio rerio) Anim Cogn 4 2001 125 131
4. J.M. Bailey, J.E. Johnson, and M.C. Newland Mechanisms and performance measures in mastery-based incremental repeated acquisition: behavioral and pharmacological analyses Psychopharmacology (Berl) 209 4 2010 331 341 10.1007/s00213-010-1801-3 [May]
5. J. Bailey, A. Oliveri, and E.D. Levin Zebrafish model systems for developmental neurobehavioral toxicology Birth Defects Res C Embryo Today 99 2013 14 23
6. J.M. Bailey, A.N. Oliveri, C. Zhang, J.M. Frazier, S. Mackinnon, G.J. Cole, and et al. Long-term behavioral impairment following acute embryonic ethanol exposure in zebrafish Neurotoxicol Teratol 48C 2015 1 8 10.1016/j.ntt.2015.01.005 [Jan 16, Epub ahead of print]
7. M.T. Bardo, and R.A. Bevins Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology (Berl) 153 1 2000 31 43 10.1007/s002130000569
8. M. Blank, L.D. Guerim, R.F. Cordeiro, and M.R. Vianna A one-trial inhibitory avoidance task to zebrafish: rapid acquisition of an NMDA-dependent long-term memory Neurobiol Learn Mem 92 4 2009 529 534 10.1016/j.nlm.2009.07.001
9. D. Braida, V. Limonta, S. Pegorini, A. Zani, C. Guerini-Rocco, E. Gori, and et al. Hallucinatory and rewarding effect of salvinorin A in zebrafish: kappa-opioid and CB1-cannabinoid receptor involvement Psychopharmacology (Berl) 190 4 2007 441 448 10.1007/s00213-006-0639-1
10. D. Braida, L. Ponzoni, R. Martucci, and M. Sala A new model to study visual attention in zebrafish Prog Neuropsychopharmacol Biol Psychiatry 55 2014 80 86 10.1016/j.pnpbp.2014.03.010
11. D. Braida, L. Ponzoni, R. Martucci, F. Sparatore, C. Gotti, and M. Sala Role of neuronal nicotinic acetylcholine receptors (nAChRs) on learning and memory in zebrafish Psychopharmacology (Berl) 231 9 2014 1975 1985 10.1007/s00213-013-3340-1
12. C. Castellano, C., V., and A. Ciamei NMDA receptors and learning and memory processes Curr Drug Targets 2 3 2001 273 283
13. A.C. Catania Learning 3rd ed. 1992 Prentice Hall Englewood Cliffs, NJ
14. D.T. Cerutti, J. Jozefowiez, and J.E. Staddon Rapid, accurate time estimation in zebrafish (Danio rerio) Behav Processes 99 2013 21 25 10.1016/j.beproc.2013.06.007
15. D.M. Chacon, and A.C. Luchiari A dose for the wiser is enough: the alcohol benefits for associative learning in zebrafish Prog Neuropsychopharmacol Biol Psychiatry 53 2014 109 115 10.1016/j.pnpbp.2014.03.009
16. L.P. Cofiel, and R. Mattiolo l-Histidine enhances learning in stressed zebrafish Braz J Med Biol Res 42 1 2009 128 134
17. G.P. Cognato, J.W. Bortolotto, A.R. Blazina, R.R. Christoff, D.R. Lara, M.R. Vianna, and et al. Y-maze memory task in zebrafish (Danio rerio): the role of glutamatergic and cholinergic systems on the acquisition and consolidation periods Neurobiol Learn Mem 98 4 2012 321 328 10.1016/j.nlm.2012.09.008
18. G.J. Cole, C. Zhang, P. Ojiaku, V. Bell, S. Devkota, and S. Mukhopadhyay Effects of ethanol exposure on nervous system development in zebrafish Int Rev Cell Mol Biol 299 2012 255 315 10.1016/B978-0-12-394310-1.00007-2
19. 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 5-6 2013 375 383 10.1097/FBP.0b013e328363d14a
20. R.M. Colwill, M.P. Raymond, L. Ferreira, and H. Escudero Visual discrimination learning in zebrafish (Danio rerio) Behav Processes 70 1 2005 19 31 10.1016/j.beproc.2005.03.001
21. T. Darland, and J.E. Dowling Behavioral screening for cocaine sensitivity in mutagenized zebrafish Proc Natl Acad Sci U S A 98 20 2001 11691 11696 10.1073/pnas.191380698
22. T. Darland, J.T. Mauch, E.M. Meier, S.J. Hagan, J.E. Dowling, and D.C. Darland Sulpiride, but not SCH23390, modifies cocaine-induced conditioned place preference and expression of tyrosine hydroxylase and elongation factor 1alpha in zebrafish Pharmacol Biochem Behav 103 2 2012 157 167 10.1016/j.pbb.2012.07.017
23. F. Del Bene, and C. Wyart Optogenetics: a new enlightenment age for zebrafish neurobiology Dev Neurobiol 72 3 2012 404 414 10.1002/dneu.20914 [Mar]
24. D.J. Echevarria, D.J. Jouandot, and C.N. Toms Assessing attention in the zebrafish: are we there yet? Prog Neuropsychopharmacol Biol Psychiatry 35 6 2011 1416 1420 10.1016/j.pnpbp.2011.01.020
25. D. Eddins, A. Petro, P. Williams, D.T. Cerutti, and E.D. Levin Nicotine effects on learning in zebrafish: the role of dopaminergic systems Psychopharmacology (Berl) 202 1-3 2009 103 109 10.1007/s00213-008-1287-4
26. D. Eddins, D. Cerutti, P. Williams, E. Linney, and E.D. Levin 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 1 2010 99 108 10.1016/j.ntt.2009.02.005
27. C.E. Feierstein, R. Portugues, and M.B. Orger Seeing the whole picture: a comprehensive imaging approach to functional mapping of circuits in behaving zebrafish Neuroscience 2014 10.1016/j.neuroscience.2014.11.046 [Nov 27. pii: S0306-4522(14)01014-8]
28. Y. Fernandes, and R. Gerlai Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish Alcohol Clin Exp Res 33 4 2009 601 609 10.1111/j.1530-0277.2008.00874.x [Apr, Epub 2009 Jan 12]
29. Y. Fernandes, S. Tran, E. Abraham, and R. Gerlai Embryonic alcohol exposure impairs associative learning performance in adult zebrafish Behav Brain Res 265 2014 181 187 10.1016/j.bbr.2014.02.035 [May 15, Epub 2014 Mar 2]
30. R. Gerlai Associative learning in zebrafish (Danio rerio) Methods Cell Biol 101 2011 249 270 10.1016/B978-0-12-387036-0.00012-8
31. L.M. Gomez-Laplaza, and R. Gerlai Latent learning in zebrafish (Danio rerio) Behav Brain Res 208 2 2010 509 515 10.1016/j.bbr.2009.12.031
32. L. Grossman, E. Utterback, A. Stewart, S. Gaikwad, K.M. Chung, C. Suciu, and et al. Characterization of behavioral and endocrine effects of LSD on zebrafish Behav Brain Res 214 2 2010 277 284 10.1016/j.bbr.2010.05.039
33. L. Grossman, A. Stewart, S. Gaikwad, E. Utterback, N. Wu, J. Dileo, and et al. Effects of piracetam on behavior and memory in adult zebrafish Brain Res Bull 85 1-2 2011 58 63 10.1016/j.brainresbull.2011.02.008
34. P. Iturriaga-Vasquez, F. Osorio, S. Riquelme, S. Catro, and R. Herzog Zebrafish: a model for behavioral pharmacology Rev Farmacol Chile 5 1 2012 27 32
35. S. Jesuthasan Fear, anxiety, and control in the zebrafish Dev Neurobiol 72 3 2012 395 403 10.1002/dneu.20873
36. J. Jia, Y. Fernandes, and R. Gerlai Short-term memory in zebrafish (Danio rerio) Behav Brain Res 270 2014 29 36 10.1016/j.bbr.2014.04.046
37. A.V. Kalueff, A.M. Stewart, and R. Gerlai Zebrafish as an emerging model for studying complex brain disorders Trends Pharmacol Sci 35 2 2014 63 75 10.1016/j.tips.2013.12.002
38. X. Kedikian, M.P. Faillace, and R. Bernabeu Behavioral and molecular analysis of nicotine-conditioned place preference in zebrafish PLoS One 8 7 2013 e69453 10.1371/journal.pone.0069453
39. Y.H. Kim, Y. Lee, D. Kim, M.W. Jung, and C.J. Lee Scopolamine-induced learning impairment reversed by physostigmine in zebrafish Neurosci Res 67 2 2010 156 161 10.1016/j.neures.2010.03.003
40. P. Kulkarni, G.H. Chaudhari, V. Sripuram, R.K. Banote, K.T. Kirla, R. Sultana, and et al. Oral dosing in adult zebrafish: proof-of-concept using pharmacokinetics and pharmacological evaluation of carbamazepine Pharmacol Rep 66 1 2014 179 183 10.1016/j.pharep.2013.06.012
41. B. Lau, S. Bretaud, Y. Huang, E. Lin, and S. Guo Dissociation of food and opiate preference by a genetic mutation in zebrafish Genes Brain Behav 5 7 2006 497 505 10.1111/j.1601-183X.2005.00185.x
42. E.D. Levin Complex relationships of nicotinic receptor actions and cognitive functions Biochem Pharmacol 86 8 2013 1145 1152 10.1016/j.bcp.2013.07.021
43. E.D. Levin, and E. Chen Nicotinic involvement in memory function in zebrafish Neurotoxicol Teratol 26 6 2004 731 735 10.1016/j.ntt.2004.06.010
44. E.D. Levin, and A.H. Rezvani Nicotinic treatment for cognitive dysfunction Curr Drug Targets CNS Neurol Disord 1 4 2002 423 431
45. E.D. Levin, J. Limpuangthip, T. Rachakonda, and M. Peterson Timing of nicotine effects on learning in zebrafish Psychopharmacology (Berl) 184 3-4 2006 547 552 10.1007/s00213-005-0162-9
46. E.D. Levin, D. Sledge, S. Roach, A. Petro, S. Donerly, and E. Linney Persistent behavioral impairment caused by embryonic methylphenidate exposure in zebrafish Neurotoxicol Teratol 33 6 2011 668 673 10.1016/j.ntt.2011.06.004
47. Y.C. Liu, I. Bailey, and M.E. Hale Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio) J Comp Physiol A Neuroethol Sens Neural Behav Physiol 198 1 2012 11 24 10.1007/s00359-011-0682-1
48. T. Lucon-Xiccato, and M. Dadda Assessing memory in zebrafish using the one-trial test Behav Processes 106 2014 1 4 10.1016/j.beproc.2014.03.010
49. K.D. Mann, H., C., S. Feldman, L. Blunt, A. Raymond, and P.S. Page-McCaw Cardiac response to startle stimuli in larval zebrafish: sympathetic and parasympathetic components Am J Physiol Regul Integr Comp Physiol 298 5 2010 R1288 R1297 10.1152/ajpregu.00302.2009.-Central
50. P. Mathur, B. Lau, and S. Guo Conditioned place preference behavior in zebrafish Nat Protoc 6 3 2011 338 345 10.1038/nprot.2010.201
51. H. Merchant, M. Luciana, C. Hooper, S. Majestic, and P. Tuite Interval timing and Parkinson's disease: heterogeneity in temporal performance Exp Brain Res 184 2 2008 233 248 10.1007/s00221-007-1097-7
52. J.A. Nevin, Randolph, S. Holland, and A.P. McLean Variable-ratio versus variable-interval schedules: response rate, resistance to change, and preference J Exp Anal Behav 76 1 2001 43 74 [Jul]
53. M.C. Ng, C.P. Hsu, Y.J. Wu, S.Y. Wu, Y.L. Yang, and K.T. Lu Effect of MK-801-induced impairment of inhibitory avoidance learning in zebrafish via inactivation of extracellular signal-regulated kinase (ERK) in telencephalon Fish Physiol Biochem 38 4 2012 1099 1106 10.1007/s10695-011-9595-8
54. J. Ninkovic, and L. Bally-Cuif The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse Methods 39 3 2006 262 274 10.1016/j.ymeth.2005.12.007
55. W. Norton, and L. Bally-Cuif Adult zebrafish as a model organism for behavioural genetics BMC Neurosci 11 2010 90 10.1186/1471-2202-11-90
56. P. Panula, V. Sallinen, M. Sundvik, J. Kolehmainen, V. Torkko, A. Tiittula, and et al. Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases Zebrafish 3 2 2006 235 247
57. P. Panula, Y.-C. Chen, M. Priyadarshini, H. Kudo, S. Semenova, M. Sundvik, and V. Sallinen The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases Neurobiology of Disease 40 2010 2010 46 57
58. M.O. Parker, M.E. Millington, F.J. Combe, and C.H. Brennan Development and implementation of a three-choice serial reaction time task for zebrafish (Danio rerio) Behav Brain Res 227 1 2012 73 80 10.1016/j.bbr.2011.10.037
59. M.O. Parker, A.M. Evans, A.J. Brock, F.J. Combe, M.T. Teh, and C.H. Brennan Moderate alcohol exposure during early brain development increases stimulus-response habits in adulthood Addict Biol 2014 10.1111/adb.12176 (Epub ahead of print)
60. M.G. Paule, W.H. Meck, D.E. McMillan, G.Y. McClure, M. Bateson, E.J. Popke, and et al. The use of timing behaviors in animals and humans to detect drug and/or toxicant effects Neurotoxicol Teratol 21 5 1999 491 502 [Sep-Oct]
61. J.T. Pittman, and C.S. Lott Startle response memory and hippocampal changes in adult zebrafish pharmacologically-induced to exhibit anxiety/depression-like behaviors Physiol Behav 123 2014 174 179 10.1016/j.physbeh.2013.10.023
62. C.M. Powers, E.D. Levin, F.J. Seidler, and T.A. Slotkin Silver exposure in developing zebrafish produces persistent synaptic and behavioral changes Neurotoxicol Teratol 33 2 2011 329 332 10.1016/j.ntt.2010.10.006
63. C.H. Rankin, T. Abrams, R.J. Barry, S. Bhatnagar, D.F. Clayton, J. Colombo, and et al. Habituation revisited: an updated and revised description of the behavioral characteristics of habituation Neurobiol Learn Mem 92 2009 135 138 10.1016/j.nlm.2008.09.012
64. S.K. Richetti, M. Blank, K.M. Capiotti, A.L. Piato, M.R. Bogo, M.R. Vianna, and et al. Quercetin and rutin prevent scopolamine-induced memory impairment in zebrafish Behav Brain Res 217 1 2011 10 15 10.1016/j.bbr.2010.09.027
65. E.P. Rico, D.B. Rosemberg, K.J. Seibt, K.M. Capiotti, R.S. Da Silva, and C.D. Bonan Zebrafish neurotransmitter systems as potential pharmacological and toxicological targets Neurotoxicol Teratol 33 6 2011 608 617 10.1016/j.ntt.2011.07.007
66. T. Ruhl, N. Prinz, N. Oellers, N.I. Seidel, A. Jonas, O. Albayram, and et al. Acute administration of THC impairs spatial but not associative memory function in zebrafish Psychopharmacology (Berl) 231 19 2014 3829 3842 10.1007/s00213-014-3522-5
67. K.J. Seibt, A.L. Piato, R. da Luz Oliveira, K.M. Capiotti, M.R. Vianna, and C.D. Bonan Antipsychotic drugs reverse MK-801-induced cognitive and social interaction deficits in zebrafish (Danio rerio) Behav Brain Res 224 1 2011 135 139 10.1016/j.bbr.2011.05.034
68. M. Sison, and R. Gerlai Associative learning performance is impaired in zebrafish (Danio rerio) by the NMDA-R antagonist MK-801 Neurobiol Learn Mem 96 2 2011 230 237 10.1016/j.nlm.2011.04.016
69. L. Stevens, A. Verdejo-García, A.E. Goudriaan, H. Roeyers, G. Dom, and W. Vanderplasschen Impulsivity as a vulnerability factor for poor addiction treatment outcomes: a review of neurocognitive findings among individuals with substance use disorders J Subst Abuse Treat 47 1 2014 58 72 10.1016/j.jsat.2014.01.008 [Jul, Epub 2014 Feb 10]
70. H.A. Swain, C. Sigstad, and F.M. Scalzo Effects of dizocilpine (MK-801) on circling behavior, swimming activity, and place preference in zebrafish (Danio rerio) Neurotoxicol Teratol 26 6 2004 725 729 10.1016/j.ntt.2004.06.009
71. R.F. Thompson, and W.A. Spencer Habituation: a model phenomenon for the study of neuronal substrates of behavior Psychol Rev 73 1966 16 43 10.1037/h0022681
72. E.C. Tolman, and C.H. Honzik Introduction and removal of reward, and maze performance in rats Univ Calif Publ Psychol 4 1930 257 275
73. L. Truong, D. Mandrell, R. Mandrell, M. Simonich, and R.L. Tanguay A rapid throughput approach identifies cognitive deficits in adult zebrafish from developmental exposure to polybrominated flame retardants Neurotoxicology 43 2014 134 142 10.1016/j.neuro.2014.03.005
74. F.J. van der Staay, E.T. Gieling, N.E. Pinzon, R.E. Nordquist, and F. Ohl The appetitively motivated "cognitive" holeboard: a family of complex spatial discrimination tasks for assessing learning and memory Neurosci Biobehav Rev 36 1 2012 379 403 10.1016/j.neubiorev.2011.07.008
75. D.M. Warburton Nicotine as a cognitive enhancer Prog Neuropsychopharmacol Biol Psychiatry 16 2 1992 181 191
76. K.J. Webb, W.H. Norton, D. Trumbach, A.H. Meijer, J. Ninkovic, S. Topp, and et al. Zebrafish reward mutants reveal novel transcripts mediating the behavioral effects of amphetamine Genome Biol 10 7 2009 R81 10.1186/gb-2009-10-7-r81
77. B. Weiss The whole animal as an assay system. Environmental pollutants T.Y. Toribara, J.R. Coleman, B.E. Dahneke, J. Feldman, 1978 Plenum New York 53 66
78. B. Weiss, and D.A. Cory-Slechta Assessment of behavioral toxicity A.W. Hayes, Principles and methods of toxicology 3rd ed. 1994 Raven Press New York 1091 1155
79. G. Winger, J.H. Woods, C.M. Galuska, and T. Wade-Galuska Behavioral perspectives on the neuroscience of drug addiction J Exp Anal Behav 84 3 2005 667 681 10.1901/jeab. 2005.101-04
80. C.A. Winstanley, P. Olausson, J.R. Taylor, and J.D. Jentsch Insight into the relationship between impulsivity and substance abuse from studies using animal models Alcohol Clin Exp Res 34 8 2010 1306 1318 10.1111/j.1530-0277.2010.01215.x [Aug, Epub 2010 May 14]
81. C. Zhang, P. Ojiaku, and G.J. Cole Forebrain and hindbrain development in zebrafish is sensitive to ethanol exposure involving agrin, Fgf, and sonic hedgehog function Birth Defects Res A Clin Mol Teratol 97 1 2013 8 27 10.1002/bdra.23099 [Jan, Epub 2012 Nov 27]
82. C. Zhang, J.M. Frazier, H. Chen, Y. Liu, J.A. Lee, and G.J. Cole Molecular and morphological changes in zebrafish following transient ethanol exposure during defined developmental stages Neurotoxicol Teratol 44 2014 70 80 10.1016/j.ntt.2014.06.001 [Jul-Aug, Epub 2014 Jun 11]