Role of serotonin in zebrafish (Danio rerio) anxiety: Relationship with serotonin levels and effect of buspirone, WAY 100635, SB 224289, fluoxetine and para-chlorophenylalanine (pCPA) in two behavioral models

Neuropharmacology

Volumn 71, Issue , 2013, Pages 83-97

  Maximino, Caio ^a,b   Puty, Bruna ^a   Benzecry, Rancés ^a   Araújo, Juliana ^a   Lima, Monica Gomes ^a   De Jesus Oliveira Batista, Evander ^a   Renata De Matos Oliveira, Karen ^a   Crespo Lopez, Maria Elena ^a   Herculano, Anderson Manoel ^a,b  

^a FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^b Zebrafish Neuroscience Research Consortium   (Brazil)

Author keywords

Anxiety; Fear; Geotaxis; Scototaxis; Serotonin; Zebrafish

Indexed keywords

2,3,6,7 TETRAHYDRO 1' METHYL 5 [[2' METHYL 4' (5 METHYL 1,2,4 OXADIAZOL 3 YL) 4 BIPHENYLYL]CARBONYL]SPIRO[FURO[2,3 F]INDOLE 3,4' PIPERIDINE]; BUSPIRONE; FENCLONINE; FLUOXETINE; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; SEROTONIN;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ANXIOGENIC ACTIVITY; ARTICLE; BRAIN LEVEL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; DOSE RESPONSE; DRUG ACTIVITY; DRUG MEGADOSE; EXPERIMENTAL TEST; EXTRACELLULAR FLUID; GEOTAXIS TEST; LIGHT DARK TEST; LOW DRUG DOSE; NONHUMAN; NOVEL TANK TEST; PRIORITY JOURNAL; SCOTOTAXIS TEST; TRANQUILIZING ACTIVITY; ZEBRA FISH;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; BUSPIRONE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR FLUID; FENCLONINE; FLUOXETINE; HYPERKINESIS; NERVE TISSUE PROTEINS; NEURONS; PIPERAZINES; PIPERIDONES; PROTEIN ISOFORMS; PYRIDINES; SEROTONIN; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SEROTONIN 5-HT1 RECEPTOR ANTAGONISTS; SEROTONIN UPTAKE INHIBITORS; SPIRO COMPOUNDS; ZEBRAFISH;

EID: 84878120195     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.03.006     Document Type: Article

References (97)

1. 1B receptor agonist Neuropsychopharmacology 27 2002 171 181
2. 1B/D receptor agonist, alcohol, and aggression in male mice Psychopharmacology (Berl) 157 2001 131 141
3. G. Badgy, M. Graf, Z.E. Anheuer, E.A. Modos, and S. Kantor Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C angatonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635 Int. J. Neuropsychopharmacol. 4 2001 399 408
4. D.S. Baldwin, and M. Garner How effective are current drug treatments for anxiety disorders, and how could they be improved? R.J. Blanchard, D.C. Blanchard, G. Griebel, D. Nutt, Handbook of Anxiety and Fear 2008 Academic Press Amsterdam 395 411
5. P.A. Barba-Escobedo, and G.G. Gould Visual social preferences of lone zebrafish in a novel environment: strain and anxiolytic effects Genes Brain Behav. 11 2012 366 373
6. A. Barbosa Jr., F.B. Alves, A.S.F. Pereira, L.M. Ide, and A. Hoffmann Behavioral characterization of the alarm reaction and anxiolytic-like effect of acute treatment with fluoxetine in piauçu fish Physiol. Behav. 105 2012 784 790
7. N.M. Barnes, B. Costall, J. Ge, M.E. Kelly, and R.J. Naylor The interaction of R(+)- and S(-)-zacopride with PCPA to modify rodent aversive behaviour Eur. J. Pharmacol. 218 1992 15 25
8. M. Barros, E.L. Mello, R.S. Maior, C.P. Muller, M.A. de Souza Silva, R.J. Carey, J.P. Huston, and C. Tomaz Anxiolytic-like effects of the selective 5-HT1A receptor antagonist WAY 100635 in non-human primates Eur. J. Pharmacol. 482 2003 197 203
9. V. Beijamini, and R. Andreatini Effects of Hypericum perforatum and paroxetine on rat performance in the elevated T-maze Pharmacol. Res. 48 2003 199 207
10. G. Bellipanni, E. Rink, and L. Bally-Cuif Cloning of two tryptophan hydroxylase genes expressed in the diencephalon of the developing zebrafish brain Mech. Develop. 119 2002 S215 S250
11. Z. Bencan, D. Sledge, and E.D. Levin Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety Pharmacol. Biochem. Behav. 94 2009 75 80
12. D.C. Blanchard, G. Griebel, and R.J. Blanchard Mouse defense behaviors: pharmacological and behavioral assays for anxiety and panic Neurosci. Biobehav. Rev. 25 2001 205 218
13. D.C. Blanchard, G. Griebel, and R.J. Blanchard Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion Prog. Neuropsychopharmacol. Biol. Psychiatry 27 2003 1177 1185
14. 1 receptor agonists and p-chloroamphetamine Synapse 5 1990 120 133
15. 1A receptors in the dorsal raphe and the hippocampus: II. Effects of pertussis and cholera toxins J. Pharmacol. Exp. Therapeut. 265 1993 16 23
16. N.S. Burghardt, G.M. Sullivan, B.S. McEwen, J.M. Gorman, and J.E. LeDoux The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine Biol. Psychiatry 55 2004 1171 1178
17. N.S. Burghardt, D.E.A. Bush, B.S. McEwen, and J. LeDoux Acute selective serotonin reuptake inhibitors increase conditioned fear expression: blockade with a 5-HT2C receptor antagonist Biol. Psychiatry 62 2007 1111 1118
18. J. Cachat, A. Stewart, L. Grossman, S. Gaikwad, F. Kadri, K.M. Chung, N. Wu, K. Wong, S. Roy, C. Suciu, J. Goodspeed, M. Elegante, B. Bartels, S. Elkhayat, D. Tien, J. Tan, A. Denmark, T. Gilder, E. Kyzar, J. DiLeo, K. Frank, K. Chang, E. Utterback, P. Hart, and A.V. Kalueff Measuring behavioral and endocrine responses to novelty stress in adult zebrafish Nat. Protocols 5 2010 1786 1799
19. B.J. Cao, and R.J. Rodgers Anxiolytic-like profile of p-MPPI, a novel 5HT1A receptor antagonist, in the murine elevated plus-maze Psychopharmacology (Berl) 129 1997 365 371
20. B.J. Cao, and R.J. Rodgers Influence of 5-HT1A receptor antagonism on plus-maze behaviour in mice. I. Pindolol enantiomers and pindobind 5-HT1A Pharmacol. Biochem. Behav. 58 1997 583 591
21. B.J. Cao, and R.J. Rodgers Influence of 5-HT1A receptor antagonism on plus-maze behaviour in mice. II. WAY 100635, SDZ 216-525 and NAN-190 Pharmacol. Biochem. Behav. 58 1997 593 603
22. B.J. Cao, and R.J. Rodgers Comparative effects of novel 5-HT1A receptor ligands, LY293284, LY315712 and LY297996, on plus-maze anxiety in mice Psychopharmacology (Berl) 139 1998 185 194
23. P.L. Carlton, and C. Advokat Attenuated habituation due to parachlorophenylalanine Pharmacol. Biochem. Behav. 1 1973 657 663
24. J.M. Casanovas, and F. Artigas Differential effects of ipsapirone on 5-hydroxytryptamine release in the dorsal and median raphe neuronal pathways J. Neurochem. 67 1996 1945 1952
25. 1A agonists alnespirone (S-20499) and 8-OH-DPEAT on extracellular 5-hydroxytryptamine in different regions of rat brain Br. J. Pharmacol. 122 1997 733 741
26. 1A receptor agonist BAYx3702 on serotonergic cell firing and release Naunyn-Schmiedeberg's Arch. Pharmacol. 362 2000 248 254
27. 1B receptors induces conditioned place aversion and facilitates cocaine place conditioning in rats Psychopharmacology (Berl) 163 2002 145 150
28. J.W.F. Deakin, and F.G. Graeff 5-HT and mechanisms of defence J. Psychopharmacol. 5 1991 305 315
29. 1A receptor ligand, S15535, displays anxiolytic-like effects in the social interaction and Vogel models and suppresses dialysate levels of 5-HT in the dorsal hippocampus of freely-moving rats Psychopharmacology (Berl) 152 2000 55 66
30. R.J. Egan, C.L. Bergner, P.C. Hart, J.M. Cachat, P.R. Canavello, M.F. Elegante, S.I. Elkhayat, B.K. Bartels, A.K. Tien, D.H. Tien, S. Mohnot, E. Beeson, E. Glasgow, H. Amri, Z. Zukowska, and A.V. Kalueff Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish Behav. Brain Res. 205 2009 38 44
31. 1B agonist CP-94,253 Psychopharmacology (Berl) 146 1999 391 399
32. P. Gaspar, and C. Lillesaar Probing the diversity of serotonin neurons Philos. Trans. Roy. Soc. B 367 2012 2382 2394
33. D.L. Gebauer, N. Pagnussat, A.L. Piato, I.C. Schaefer, C.D. Bonan, and D.R. Lara Effects of anxiolytics in zebrafish: similarities and differences between benzodiazepines, buspirone and ethanol Pharmacol. Biochem. Behav. 99 2011 480 486
34. I. Geller, and K. Blum The effects of 5-HTP on para-chlorophenylalanine (p-CPA) attenuation of "conflict" behavior Eur. J. Pharmacol. 9 1970 319 324
35. F.G. Graeff, M.B. Viana, and P.O. Mora Dual role of 5-HT in defense and anxiety Neurosci. Biobehav. Rev. 21 1997 791 799
36. G. Griebel, D.C. Blanchard, and R.J. Blanchard Predator elicited flight responses in the Swiss Webster mice: an experimental model of panic attacks Prog. Neuropsychopharmacol. Biol. Psychiatry 20 1996 185 205
37. G. Griebel, R.J. Rodgers, G. Perrault, and D.J. Sanger Behavioural profiles in the mouse defence test battery suggest anxiolytic potential of 5-HT(1A) receptor antagonists Psychopharmacology (Berl) 144 1999 121 130
38. G. Griebel, R.J. Rodgers, G. Perrault, and D.J. Sanger The effects of compounds varying in selectivity as 5-HT(1A) receptor antagonists in three rat models of anxiety Neuropharmacology 39 2000 1848 1857
39. F.S. Guimarães, A.P. Carobrez, and F.G. Graeff Modulation of anxiety behaviors by 5-HT-interacting drugs R.J. Blanchard, D.C. Blanchard, G. Griebel, D. Nutt, Handbook of Anxiety and Fear 2008 Academic Press Amsterdam
40. F.S. Guimarães, H. Zangrossi Jr., C.M. Del Ben, and F.G. Graeff Serotonin in panic and anxiety disorders C. Müller, B. Jacobs, Handbook of Behavioral Neurobiology of Serotonin 2010 Academic Press San Diego, USA 667 685
41. 1B receptor compounds on ventral tegmental area intracranial self-stimulation thresholds in rats Eur. J. Pharmacol. 604 2009 74 78
42. A. Jahanshaji, L.W. Lim, H.W.M. Steinbusch, V. Visser-Vandewalle, and Y. Temel Buspirone-induced changes in the serotonergic and non-serotonergic cells in the dorsal raphe nucleus of rats Neurosci. Lett. 473 2010 136 140
43. A. Jahn-Eimermacher, I. Lasarzik, and J. Raber Statistical analysis of latency outcomes in behavioral experiments Behav. Brain Res. 221 2011 271 275
44. 1A receptor agonists and in their inhibitory effects on the firing of serotonergic neurons in the rat? J. Pharmacol. Exp. Therapeut. 272 1995 920 929
45. A.V. Kalueff, and D.L. Murphy The importance of cognitive phenotypes in experimental modeling of animal anxiety and depression Neural Plasticity 2007 2007 Article ID 52087
46. A.V. Kalueff, S. Gaikwad, A.M. Stewart, J. Green, E. Kyzar, A. Roth, and I. Zapolsky The Zebrafish Neurophenome Project, 2010-2011 2010-2011
47. F. Kassay, and I. Gyertyán Shock priming enhances the efficacy of SSRIs in the foot shock-induced ultrasonic vocalization test Prog. Neuropsychopharmacol. Biol. Psychiatry 36 2012 128 135
48. R.S. Kiser Jr., and R.M. Lebovitz Monoaminergic mechanisms in aversive brain stimulation Physiol. Behav. 15 1975 47 53
49. R.S. Kiser Jr., R.M. Lebovitz, and D.C. German Anatomic and pharmacologic differences between two types of aversive midbrain stimulation Brain Res. 155 1978 331 342
50. D. Kshama, H.J. Hrishikeshavan, R. Shanbhoge, and U.S. Munonyedi Modulation of baseline behavior in rats by putative serotonergic agents in three ethoexperimental paradigms Behav. Neural Biol. 54 1990 234 253
51. E. Kyzar, I. Zapolsky, J. Green, S. Gaikwad, M. Pham, A. Roth, A.M. Stewart, C. Collins, P. Saint-Pierre, B. Hirons, and A.V. Kalueff The Zebrafish Neurophenome Database (ZND): a dynamic open-access resource for zebrafish neurophenotypic data Zebrafish 9 2012 8 14
52. B.Y. Lau, P. Mathur, G.G. Gould, and S. Guo Identification of a brain center whose activity discriminates a choice behavior in zebrafish Proc. Natl. Acad. Sci. U.S.A. 108 2011 2581 2586
53. M.D. Lee, and P.G. Clifton Role of the serotonergic system in appetite and ingestion control C. Müller, B. Jacobs, Handbook of Behavioral Neurobiology of Serotonin 2010 Academic Press San Diego, USA 331 345
54. 1A receptor sensitivity in depression and anxiety disorders: molecular mechanisms of neuroadaption Clin. Neuropharmacol. 15 1992 208A 209A
55. C. Lillesaar The serotonergic system in fish J. Chem. Neuroanat. 41 2011 294 298
56. C. Lillesaar, C. Stigloher, B. Tannhäuser, M.F. Wullimann, and L. Bally-Cuif Axonal projections originating from raphe serotonergic neurons in the developing and adult zebrafish, Danio rerio, using transgenics to visualize raphe-specific pet1 expression J. Comp. Neurol. 512 2009 158 182
57. C.A. Lowry, and M.W. Hale Serotonin and the neurobiology of anxious states C. Müller, B. Jacobs, Handbook of Behavioral Neurobiology of Serotonin 2010 Academic Press San Diego, USA 379 397
58. G. Malleret, R. Hen, J.-L. Guillou, L. Segu, and M.-C.- Buhot 5-HT1B receptor knockout mice exhibit increased exploratory activity and enhanced spatial memory performance in the Morris water maze J. Neurosci. 19 1999 6157 6168
59. C. Maximino Serotonin and Anxiety - Neuroanatomical, Pharmacological, and Functional Aspects 2012 Springer New York
60. C. Maximino, and A.M. Herculano A review of monoaminergic neuropsychopharmacology in zebrafish Zebrafish 7 2010 359 378
61. C. Maximino, T.M. Brito, C.A.G.D.M. Dias, A. Gouveia Jr., and S. Morato Scototaxis as anxiety-like behavior in fish Nat. Protocols 5 2010 209 216
62. C. Maximino, A.W.B. Silva, A. Gouveia Jr., and A.M. Herculano Pharmacological analysis of zebrafish (Danio rerio) scototaxis Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 624 631
63. C. Maximino, R. Benzecry, K.R.M. Oliveira, E. d. J.O. Batista, A.M. Herculano, D.B. Rosemberg, D.L. Oliveira, and R. Blaser A comparison of the light/dark and novel tank tests in zebrafish Behaviour 149 2012 1099 1123
64. Maximino, C., Lima, M.G., Araújo, J., Oliveira, K.R.M., Herculano, A.M., Stewart, A.M., Kyzar, E.J., Cachat, J., Kalueff, A.V. The serotonergic system of zebrafish: genomics, neuroanatomy and neuropharmacology. In: Hall, S., (Ed), Serotonin: Biosynthesis, Regulation and Health Implications. Nova Science, New York, in press.
65. 1A agonists Mol. Pharmacol. 37 1990 231 237
66. 1B agonist apirtoline Psychopharmacology (Berl) 157 2001 421 429
67. 2A receptors suppresses the induction of locomotor activity by 5-HT reuptake inhibitors, citalopram and fluvoxamine, in NMRI mice exposed to a novel environment: a comparison to other 5-HT receptor subtypes Psychopharmacology (Berl) 168 2003 397 409
68. W.H.J. Norton, A. Folchert, and L. Bally-Cuif Comparative analysis of serotonin receptor (HTR1A/HTR1B families) and transporter (slc6a4a/b) gene expression in the zebrafish brain J. Comp. Neurol. 511 2008 521 542
69. S.H. Pinheiro, H. Zangrossi Jr., C.M. Del Ben, and F.G. Graeff Elevated mazes as animal models of anxiety: effects of serotonergic agents Anais Acad. Brasil. Ciências 79 2007 71 85
70. G. Pinna In a mouse model relevant for PTSD, selective brain steroidogenic stimulants (SBSSs) improve behavioral deficits by normalizing allopreganolone biosynthesis Behav. Pharmacol. 21 2010 438 450
71. S.C. Poltronieri, H. Zangrossi Jr., and M.B. Viana Antipanic-like effect of serotonin reuptake inhibitors in the elevated T-maze Behav. Brain Res. 147 2003 185 192
72. S. Ravinder, A.G. Pillai, and S. Chattarji Cellular correlates of enhanced anxiety caused by acute treatment with the selective serotonin reuptake inhibitor fluoxetine in rats Frontiers Behav. Neurosci. 5 2011 Article 88
73. A. Rex, J.P. Voigt, and H. Fink Anxiety but not arousal increases 5-hydroxytryptamine release in the rat ventral hippocampus in vivo Eur. J. Neurosci. 22 2005 1185 1189
74. T.W. Robbins, and M.J. Crockett Role of central serotonin in impulsivity and compulsivity: comparative studies in experimental animals and humans C. Müller, B. Jacobs, Handbook of Behavioral Neurobiology of Serotonin 2010 Academic Press San Diego, USA 415 427
75. J. Sackerman, J.J. Donegan, C.S. Cunningham, N.N. Nguyen, K. Lawless, A. Long, R.H. Benno, and G.G. Gould 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
76. P. Salchner, and N. Singewald Neuroanatomical substrates involved in the anxiogenic-like effect of acute fluoxetine treatment Neuropharmacology 43 2002 1238 1248
77. P. Salchner, and N. Singewald 5-HT receptor subtypes involved in the anxiogenic-like action and associated Fos response of acute fluoxetine treatment in rats Psychopharmacology (Berl) 185 2006 282 288
78. R.C. Silva, and M.L. Brandão Acute and chronic effects of gepirone and fluoxetine in rats tested in the elevated plus-maze: an ethological analysis Pharmacol. Biochem. Behav. 65 2000 209 216
79. 1 receptor Eur. J. Pharmacol. 167 1988 173 181
80. B. Söderpalm, and J.A. Engel Does PCPA induced anticonflict effect involve activation of the GABAA/benzodiazepine chloride ionophore receptor complex? J. Neural Transm. 76 1989 145 153
81. 1A receptor agonist ipsapirone in the rat: neurobiological correlates Eur. J. Pharmacol. 240 1993 29 37
82. P.J. Steenbergen, M.K. Richardson, and D.L. Champagne Patterns of avoidance behaviours in the light/dark preference test in young juvenile zebrafish: a pharmacological study Behav. Brain Res. 222 2011 15 25
83. J.F. Stephenson, K.E. Whitlock, and J.C. Partridge Zebrafish preference for light or dark is dependent on ambient light levels and olfactory stimulation Zebrafish 8 2011 17 22
84. A.M. Stewart, J. Cachat, K. Wong, S. Gaikwad, T. Gilder, J. DiLeo, K. Chang, E. Utterback, and A.V. Kalueff Homebase behavior of zebrafish in novelty-based paradigms Behav. Process. 85 2010 198 203
85. A.M. Stewart, N. Wu, J. Cachat, P. Hart, S. Gaikwad, K. Wong, E. Utterback, T. Gilder, E. Kyzar, A. Newman, D. Carlos, K. Chang, M. Hook, C. Rhymes, M. Caffery, M. Greenberg, J. Zadina, and A.V. Kalueff Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models Prog. Neuropsychopharmacol. Biol. Psychiatry 35 2011 1421 1431
86. A.M. Stewart, J. Cahcat, J. Green, S. Gaikwad, E. Kyzar, A. Roth, A. Davis, C. Collins, M. El-Ounsi, M. Pham, and A.V. Kalueff Constructing the habituome for phenotype-driven zebrafish research Behav. Brain Res. 236 2013 110 117
87. K. Strimmer A unified approach to false discovery rate estimation BMC Bioinformatics 9 2008 303
88. 1A receptor knockout mouse as a genetic model of anxiety Eur. J. Pharmacol. 463 2003 177 184
89. D. Treit, A. Robinson, S. Rotzinger, and C. Pesold Anxiolytic effects of serotonergic interventions in the shock-probe burying test and the elevated plus-maze test Behav. Brain Res. 54 1993 23 34
90. N.C. Tye, B.J. Everitt, and S.D. Iversen 5-Hydroxytryptamine and punishment Nature 268 1977 741 742
91. M.B. Viana, C. Tomaz, and F.G. Graeff The elevated T-maze: a new animal model of anxiety and memory Pharmacol. Biochem. Behav. 49 1994 549 554
92. Y. Wang, R. Takai, H. Yoshioka, and K. Shirabe Characterization and expression of serotonin transporter genes in zebrafish Tohoku J. Exp. Med. 208 2006 267 274
93. C.J. Watson, B.J. Venton, and R.T. Kennedy In vivo measurements of neurotransmitters by microdialysis sampling Anal. Chem. 78 2006 1391 1399
94. K. Wolf Physiological salines for freshwater teleosts Prog. Fish-Cult. 25 1963 135 140
95. K. Wong, M. Elegante, B. Bartels, S. Elkhayat, D. Tien, S. Roy, J. Goodspeed, C. Suciu, J.L. Tan, C. Grimes, A. Chung, M. Rosenberg, S. Gaikwad, A. Denmark, A. Jackson, F. Kadri, K.M. Chung, A. Stewart, T. Gilder, E. Beeson, I. Zapolsky, N.D. Wu, J. Cachat, and A.V. Kalueff Analyzing habituation responses to novelty in zebrafish (Danio rerio) Behav. Brain Res. 208 2010 450 457
96. F.D. Yocca, L. Iben, and E. Meller Lack of apparent receptor reserve at postsynaptic 5-hydroxytryptamine 1A receptors negatively coupled to adenylyl cyclase activity in rat hippocampal membranes Mol. Pharmacol. 41 1992 1066 1072
97. T. Zor, and Z. Selinger Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies Anal. Biochem. 236 1996 302 308