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Journal of Comparative Physiology A

, Volume 205, Issue 4, pp 567–582 | Cite as

The plus maze and scototaxis test are not valid behavioral assays for anxiety assessment in the South African clawed frog

  • R. Boone Coleman
  • Kelsey Aguirre
  • Hannah P. Spiegel
  • Celina Pecos
  • James A. Carr
  • Breanna N. HarrisEmail author
Original Paper

Abstract

There are no behavioral models for testing anxiety in amphibians, a group of animals widely used for developmental, ecotoxicological, and genetic research. We aimed to validate two common rodent paradigms, the plus maze and the scototaxis test, for use in the aquatic African clawed frog (Xenopus laevis). We predicted: (a) that frogs would prefer the dark, vs. light, portions of the testing arenas (face validity), (b) that this behavior could be altered with acute administration of anxio-selective drugs (construct validity), and (c) that time spent in the dark portions of the arenas would be positively correlated (predictive validity). Prior to testing, frogs were treated with fluoxetine (selective serotonin reuptake inhibitor [SSRI]), desipramine (serotonin- and norepinephrine-reuptake inhibitor), caffeine (methylxanthine, adenosine receptor antagonist, phosphodiesterase inhibitor), saline, or were left unmanipulated. Each drug was administered acutely (1 h prior to testing; caffeine) or subacutely (24, 3, and 1 h prior to testing; fluoxetine, desipramine) at one of three doses. Plus maze and scototaxis testing were separated by 1 week; each frog completed both behavioral tasks and was treated with the same drug regimen prior to testing. Overall, both tests showed face validity, however, data suggest these paradigms lack both construct and predictive validity.

Keywords

Ecotoxicology SSRI Amphibian Caffeine PPCP 

Abbreviations

PPCP

Pharmaceutical and personal care product

RDoC

Research Domain Criteria

SSRI

Selective serotonin reuptake inhibitor

TCA

Tricyclic antidepressant

Notes

Acknowledgements

We would like to thank Paul Duggan, Rebekah Salinas, Christian Thomas, and Dr. Kurt Caswell for their help on this project. We would also like to thank the Texas Tech Honors College (Undergraduate Research Scholar program) and the NSF-funded PRISM program (www.math.ttu.edu/outreach/prism) for supporting RBC. We especially thank the PRISM PIs (Drs. G. Brock Williams, Sophia Jang, Nancy McIntyre, Jaclyn Canas-Carrell, and Jerry Dwyer), Jessica Spott, Lori Lightfoot, and Jerylme Robins for their support. All applicable international, national, and Texas Tech University Institutional Animal Care and Use Committee (IACUC) guidelines were followed. Texas Tech University is Association for Assessment and Accreditation of Laboratory Animal Care accredited. We also thank two anonymous reviewers for their helpful and constructive comments on a previous version of this manuscript, their comments no doubt improved the final product.

Funding

This work was partially supported by the National Science Foundation under Grant Nos. 1035096 (PRISM) and 1656734 (IOS, awarded to JAC and BNH), and by the Texas Tech University (TTU) Center for Active Learning and Undergraduate Engagement (now TrUE). This project was conducted for the fulfillment of R. Boone Coleman’s Honor’s Thesis.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

359_2019_1351_MOESM1_ESM.pdf (222 kb)
Supplementary material 1 (PDF 222 kb)

References

  1. Adhikari A (2014) Distributed circuits underlying anxiety. Front Behav Neurosci 8:112CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anderzhanova E, Kirmeier T, Wotjak CT (2017) Animal models in psychiatric research: the RDoC system as a new framework for endophenotype-oriented translational neuroscience. Neurobiol Stress 7:47–56CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beaufour CC, Ballon N, Le Bihan C, Hamon M, Thiébot MH (1999) Effects of chronic antidepressants in an operant conflict procedure of anxiety in the rat. Pharmacol Biochem Behav 62(4):591–599CrossRefPubMedGoogle Scholar
  4. Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125(1–2):141–149CrossRefPubMedGoogle Scholar
  5. Belzung C, Lemoine M (2011) Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression. Biol Mood Anxiety Disord 1(1):9CrossRefPubMedPubMedCentralGoogle Scholar
  6. Benjamin DJ, Berger JO, Johannesson M, Nosek BA, Wagenmakers EJ, Berk R, Bollen KA, Brembs B, Brown L, Camerer C, Cesarini D, Chambers CD, Clyde M, Cook TD, De Boeck P, Dienes Z, Dreber A, Easwaran K, Efferson C, Fehr E, Fidler F, Field AP, Forster M, George EI, Gonzalez R, Goodman S, Green E, Green DP, Greenwald A, Hadfield JD, Hedges LV, Held L, Hau Ho T, Hoijtink H, Hruschka DJ, Imai K, Imbens G, Loannidis JPA, Jeon M, Holland Jones J, Kirchler M, Laibson D, List J, Little R, Lupia A, Machery E, Maxell SE, McCarthy M, Moore S, Morgan SL, Munafo M, Nakagawa S, Nyhan B, Parker TH, Pericchi L, Perugini M, Rouder J, Rousseau J, Savalei V, Schonbrodt FD, Sellke T, Sinclair B, Tingley D, Van Zandt T, Vazire S, Watts DJ, Winship C, Wolpert RL, Xie Y, Young C, Zinman J, Johnson VE (2018) Redefine statistical significance. Nat Hum Behav 2(1):6–10CrossRefGoogle Scholar
  7. Berg C, Backström T, Winberg S, Lindberg R, Brandt I (2013) Developmental exposure to fluoxetine modulates the serotonin system in hypothalamus. PLoS ONE 8(1):e55053CrossRefPubMedPubMedCentralGoogle Scholar
  8. Blanchard DC, Summers CH, Blanchard RJ (2013) The role of behavior in translational models for psychopathology: functionality and dysfunctional behaviors. Neurosci Biobehav Rev 37(8):1567–1577CrossRefPubMedPubMedCentralGoogle Scholar
  9. Blaser RE, Rosemberg DB (2012) Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test. PLoS ONE 7(5):e36931CrossRefPubMedPubMedCentralGoogle Scholar
  10. Blaser RE, Chadwick L, McGinnis GC (2010) Behavioral measures of anxiety in zebrafish (Danio rerio). BehavBrain Res 208(1):56–62Google Scholar
  11. Borsini F, Podhorna J, Marazziti D (2002) Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacol 163(2):121–141CrossRefGoogle Scholar
  12. Bourin M, Hascoët M (2003) The mouse light/dark box test. Eur J Pharmacol 463(1–3):55–65CrossRefPubMedGoogle Scholar
  13. Brodin T, Fick J, Jonsson M, Klaminder J (2013) Dilute concentrations of a psychiatric drug alter behavior of fish from natural populations. Science 339(6121):814–815CrossRefPubMedGoogle Scholar
  14. Brooks BW (2014) Fish on Prozac (and Zoloft): ten years later. Aquatic Toxicol 151:61–67CrossRefGoogle Scholar
  15. Carhart-Harris RL, Roseman L, Haijen E, Erritzoe D, Watts R, Branchi I, Kaelen M (2018) Psychedelics and the essential importance of context. J Psychopharmacol 32(7):725–731CrossRefPubMedGoogle Scholar
  16. Carobrez AP, Bertoglio LJ (2005) Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 29(8):1193–1205CrossRefPubMedGoogle Scholar
  17. Carr JA (2015) I’ll take the low road: the evolutionary underpinnings of visually triggered fear. Front Neurosci 9:414PubMedPubMedCentralGoogle Scholar
  18. Carr JA, Gentles A, Smith EE, Goleman WL, Urquidi LJ, Thuett K, Kendall RJ, Giesy JP, Gross TS, Solomon KR, Van Der Kraak G (2003) Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environ Toxicol Chem 22(2):396–405CrossRefPubMedGoogle Scholar
  19. Channing AC (2001) Amphibians of central and Southern Africa. Protea House, Pretoria, p 470Google Scholar
  20. Charney DS, Heninger GR, Sternberg DE (1984) Serotonin function and mechanism of action of antidepressant treatment: effects of amitriptyline and desipramine. Arch Gen Psychiatry 41(4):359–365CrossRefPubMedGoogle Scholar
  21. Clinchy M, Schulkin J, Zanette LY, Sheriff MJ, McGowan PO, Boonstra R (2011) The neurological ecology of fear: insights neuroscientists and ecologists have to offer one another. Front Behav Neurosci 5:21PubMedCentralGoogle Scholar
  22. Clinchy M, Sheriff MJ, Zanette LY (2013) Predator-induced stress and the ecology of fear. Funct Ecol 27(1):56–65CrossRefGoogle Scholar
  23. Correa M, Font L (2008) Is there a major role for adenosine A2A receptors in anxiety. Front Biosci 13:4058–4070CrossRefPubMedGoogle Scholar
  24. Craske MG, Stein MB, Eley TC, Milad MR, Holmes A, Rapee RM, Wittchen HU (2017) Anxiety disorders. Nat Rev Dis Primers 3:17100CrossRefPubMedGoogle Scholar
  25. Cregg R, Russo G, Gubbay A, Branford R, Sato H (2013) Pharmacogenetics of analgesic drugs. Br J Pain 7(4):189–208CrossRefPubMedPubMedCentralGoogle Scholar
  26. Cuthbert BN, Insel TR (2013) Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med 11(1):126CrossRefPubMedPubMedCentralGoogle Scholar
  27. Daly JW, Shi D, Nikodijevic O, Jacobson KA (1994) The role of adenosine receptors in the central action of caffeine. Pharmacopsychoecologia 7(2):201PubMedPubMedCentralGoogle Scholar
  28. Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51(1):68–80CrossRefPubMedGoogle Scholar
  29. Duggan PE, Prater C, Carr JA, Harris BN (2016) Predator presence decreases food consumption in juvenile Xenopus laevis. Behav Ecol Sociobio 70(12):2005–2015CrossRefGoogle Scholar
  30. Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF, Elkhayat SI, Bartels BK, Tien AK, Tien DH, Mohnot S (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205(1):38–44CrossRefPubMedGoogle Scholar
  31. Ennaceur A (2014) Tests of unconditioned anxiety—pitfalls and disappointments. Physiol Behav 135:55–71CrossRefPubMedGoogle Scholar
  32. File SE (1991) The biological basis of anxiety. In: Meltzer HY, Nerozzi D (eds) Current practices and future developments in the pharmacotherapy of mental disorders. Elsevier Publishing, Amsterdam, pp 159–165Google Scholar
  33. Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Delbecque JP, Cattaert D (2014) Anxiety-like behavior in crayfish is controlled by serotonin. Science 344(6189):1293–1297CrossRefPubMedGoogle Scholar
  34. Foxon GEH, Rowson KEK (1956) The fate of ‘Thorotrast’ (thorim dioxide) injected into the dorsal lymph sac of the frog, Rana temporaria. Q J Microscop Sci 3(37):47–57Google Scholar
  35. Gaetani S, Cuomo V, Piomelli D (2003) Anandamide hydrolysis: a new target for anti-anxiety drugs? Trends in Mol Medicine 9(11):474–478CrossRefGoogle Scholar
  36. Gendron A (2013) Amphibian ecotoxicology. In: Férard JF, Blaise C (eds) Encyclopedia of aquatic ecotoxicology. Springer, DordrechtGoogle Scholar
  37. Goswami S, Rodríguez-Sierra O, Cascardi M, Paré D (2013) Animal models of post-traumatic stress disorder: face validity. Front Neurosci 7:89CrossRefPubMedGoogle Scholar
  38. Griebel G (1995) 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30 years of research. Pharmacol Thers 65(3):319–395CrossRefGoogle Scholar
  39. Griebel G, Holmes A (2013) 50 years of hurdles and hope in anxiolytic drug discovery. Nat Rev Drug Dis 12(9):667–687CrossRefGoogle Scholar
  40. Harris BN, Carr JA (2016) The role of the hypothalamus-pituitary-adrenal/interrenal axis in mediating predator-avoidance trade-offs. Gen Comp Endocrinol 230:110–142CrossRefPubMedGoogle Scholar
  41. Harris BN, Hohman ZP, Campbell CM, King KS, Tucker CA (2019) FAAH genotype, CRFR1 genotype, and cortisol interact to predict anxiety in an aging, rural Hispanic population: a Project FRONTIER study. Neurobiol Stress 10:100154CrossRefPubMedGoogle Scholar
  42. Hoffman EJ, Mathew SJ (2008) Anxiety disorders: a comprehensive review of pharmacotherapies. Mount Sinai JJ Medicine: A J TranslPers Medicine 75(3):248–262CrossRefGoogle Scholar
  43. Hopkins WA (2007) Amphibians as models for studying environmental change. ILAR J 48(3):270–277CrossRefPubMedGoogle Scholar
  44. Hughes RN, Hancock NJ, Henwood GA, Rapley SA (2014) Evidence for anxiolytic effects of acute caffeine on anxiety-related behavior in male and female rats tested with and without bright light. Behav Brain Res 271:7–15CrossRefGoogle Scholar
  45. Insel TR (2014) The NIMH research domain criteria (RDoC) project: precision medicine for psychiatry. Am J Psychiatry 171(4):395–397CrossRefPubMedGoogle Scholar
  46. Jain N, Kemp N, Adeyemo O, Buchanan P, Stone TW (1995) Anxiolytic activity of adenosine receptor activation in mice. Br J Pharmacol 116(3):2127–2133CrossRefPubMedGoogle Scholar
  47. James JE (1997) Understanding caffeine: a biobehavioral analysis. Sage Publications, Beverley HillsGoogle Scholar
  48. Jesuthasan S (2012) Fear, anxiety, and control in the zebrafish. Devel Neurobiol 72(3):395–403CrossRefGoogle Scholar
  49. Kalueff AV, Stewart AM, Kyzar EJ, Cachat J, Gebhardt M, Landsman S (2012) International Zebrafish Neuroscience Research Consortium. Time to recognize zebrafish ‘affective’ behavior. Behaviour 149(10–12):1019–1036Google Scholar
  50. Kelleher SR, Silla AJ, Byrne PG (2018) Animal personality and behavioral syndromes in amphibians: a review of the evidence, experimental approaches, and implications for conservation. Behav Ecol Sociobiol 72(5):79CrossRefGoogle Scholar
  51. Kshama D, Hrishikeshavan HJ, Shanbhogue R, Munonyedi US (1990) Modulation of baseline behavior in rats by putative serotonergic agents in three ethoexperimental paradigms. Behav Neural Biol 54(3):234–253CrossRefPubMedGoogle Scholar
  52. Kumar V, Bhat ZA, Kumar D (2013) Animal models of anxiety: a comprehensive review. J Pharmacol Toxicol Methods 68(2):175–183CrossRefPubMedGoogle Scholar
  53. Kurt M, Arik AC, Celik S (2000) The effects of sertraline and fluoxetine on anxiety in the elevated plus-maze test. J Basic Clin Physiol Pharmacol 11(2):173–180CrossRefPubMedGoogle Scholar
  54. Lampis V, Maziade M, Battaglia M (2011) Animal models of human anxiety disorders: reappraisal from a developmental psychopathology vantage point. Pediatric Res 69(5 Pt 2):77R–84RCrossRefGoogle Scholar
  55. Lembke A, Papac J, Humphreys K (2018) Our other prescription drug problem. N Eng J Med 378(8):693–695CrossRefGoogle Scholar
  56. Lister RG (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46(3):321–340CrossRefPubMedGoogle Scholar
  57. Liu Z, Kariya MJ, Chute CD, Pribadi AK, Leinwand SG, Tong A, Curran KP, Bose N, Schroeder FC, Srinivasan J, Chalasani SH (2018) Predator-secreted sulfolipids induce defensive responses in C. elegans. Nat Commun 9(1):1128CrossRefPubMedGoogle Scholar
  58. Loonen AJ, Ivanova SA (2015) Circuits regulating pleasure and happiness: the evolution of reward-seeking and misery-fleeing behavioral mechanisms in vertebrates. Front Neurosci 9:394CrossRefPubMedGoogle Scholar
  59. Lowry CA, Johnson PL, Hay-Schmidt A, Mikkelsen J, Shekhar A (2005) Modulation of anxiety circuits by serotonergic systems. Stress 8(4):233–246CrossRefPubMedGoogle Scholar
  60. Mansouri MT, Soltani M, Naghizadeh B, Farbood Y, Mashak A, Sarkaki A (2014) A possible mechanism for the anxiolytic-like effect of gallic acid in the rat elevated plus maze. Pharmacol Biochem Behav 117:40–46CrossRefPubMedGoogle Scholar
  61. Matsuda K, Hagiwara Y, Shibata H, Sakashita A, Wada K (2013) Ovine corticotropin-releasing hormone (oCRH) exerts an anxiogenic-like action in the goldfish, Carassius auratus. Gen Comp Endocrinol 188:118–122CrossRefPubMedGoogle Scholar
  62. Maximino C, Marques T, Dias F, Cortes FV, Taccolini IB, Pereira PM, Colmanetti R, Lozano R, Gazolla RA, Tenoria R, Tavares de Lacerda RI, Rodrigues STK, de Oliveira Valéria, Coelho Lameirao S, Pontes AAA, Romao CF, Prado VM, Gouveia A (2007) A comparative analysis of the preference for dark environments in five teleosts. Int J Comp Psychol 20(4):351–367Google Scholar
  63. Maximino C, de Brito TM, da Silva Batista AW, Herculano AM, Morato S, Gouveia A (2010a) Measuring anxiety in zebrafish: a critical review. Behav Brain Res 214(2):157–171CrossRefPubMedGoogle Scholar
  64. Maximino C, de Brito TM, Colmanetti R, Pontes AAA, de Castro HM, de Lacerda RIT, Morato S, Gouveia A Jr (2010b) Parametric analyses of anxiety in zebrafish scototaxis. Behav Brain Res 210(1):1–7CrossRefPubMedGoogle Scholar
  65. Maximino C, de Brito TM, de Mattos Dias CAG, Gouveia A Jr, Morato S (2010c) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5(2):209CrossRefGoogle Scholar
  66. Maximino C, da Silva AWB, Gouveia A, Herculano AM (2011) Pharmacological analysis of zebrafish (Danio rerio) scototaxis. Prog Neuro-Psychopharmacol Biolo Psychiatry 35(2):624–631CrossRefGoogle Scholar
  67. Maximino C, Benzecry R, Oliveira KRM, de Batista OBE, Herculano AM, Rosemberg DB, de Oliveira DL, Blaser R (2012) A comparison of the light/dark and novel tank tests in zebrafish. Behaviour 149(10–12):1099–1123CrossRefGoogle Scholar
  68. McNaughton N, Zangrossi H (2008) Theoretical approaches to the modeling of anxiety in animals. In: Blanchard DC, Griebel G, Nutt DJ (eds) Handbook of anxiety and fear, vol 17. Elsevier Publishing, Amsterdam, pp 11–27CrossRefGoogle Scholar
  69. Measey GJ (1998) Diet of feral Xenopus laevis (Daudin) in South Wales, UK. J Zool 246(3):287–298CrossRefGoogle Scholar
  70. Morris A, Green M, Martin H, Crossland K, Swaney WT, Williamson SM, Rae R (2018) A nematode that can manipulate the behaviour of slugs. Behav Process 151:73–80CrossRefGoogle Scholar
  71. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13(10):1161CrossRefPubMedPubMedCentralGoogle Scholar
  72. O’Neill SJ, Williamso JE, Tosetto L, Brown C (2018) Effects of acclimatisation on behavioural repeatability in two behaviour assays of the guppy Poecilia reticulata. Behav Ecol Sociobiol 72(10):166CrossRefGoogle Scholar
  73. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167CrossRefGoogle Scholar
  74. Perusini JN, Fanselow MS (2015) Neurobehavioral perspectives on the distinction between fear and anxiety. Learn Mem 22(9):417–425CrossRefPubMedPubMedCentralGoogle Scholar
  75. Prater CM, Harris BN, Carr JA (2018) Tectal CRFR1 receptors modulate food intake and feeding behavior in the South African clawed frog Xenopus laevis. Horm Behav 105:86–94CrossRefPubMedGoogle Scholar
  76. Ramos A (2008) Animal models of anxiety: do I need multiple tests? Trends Pharmacol Sci 29(10):493–498CrossRefPubMedGoogle Scholar
  77. Ramos A, Berton O, Mormède P, Chaouloff F (1997) A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85(1):57–69CrossRefPubMedGoogle Scholar
  78. Ramos A, Mellerin Y, Mormede P, Chaouloff F (1998) A genetic and multifactorial analysis of anxiety-related behaviours in Lewis and SHR intercrosses. Behav Brain Res 96(1–2):195–205CrossRefPubMedGoogle Scholar
  79. Ramos A, Pereira E, Martins GC, Wehrmeister TD, Izídio GS (2008) Integrating the open field, elevated plus maze and light/dark box to assess different types of emotional behaviors in one single trial. Behav Brain Res 193(2):277–288CrossRefPubMedGoogle Scholar
  80. Ren J, Friedmann D, Xiong J, Liu CD, DeLoach KE, Ran C, Pu A, Sun Y, Weissbourd B, Neve RL, Horowtiz M, Luo L (2018) Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems. Cell 175(2):472–487.  https://doi.org/10.1016/j.cell.2018.07.043
  81. Ressler KJ, Mayberg HS (2007) Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci 10(9):1116CrossRefPubMedPubMedCentralGoogle Scholar
  82. Richendrfer H, Pelkowski SD, Colwill RM, Creton R (2012) On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behav Brain Res 228(1):99–106CrossRefPubMedGoogle Scholar
  83. Rodgers RJ, Cao BJ, Dalvi A, Holmes A (1997) Animal models of anxiety: an ethological perspective. Braz J Medical Bioll Res 30:289–304CrossRefGoogle Scholar
  84. Rosenthal R (1994) Parametric measures of effect size. In: Cooper H, Hedges LV (eds) The handbook of research synthesis. Russell Sage Foundation, New York, pp 231–244Google Scholar
  85. Rotzinger S, Lovejoy DA, Tan LA (2010) Behavioral effects of neuropeptides in rodent models of depression and anxiety. Peptides 31(4):736–756CrossRefPubMedGoogle Scholar
  86. Sackerman J, Donegan JJ, Cunningham CS, Nguyen NN, Lawless K, Long A, Benno RH, Gould GG (2010) Zebrafish behavior in novel environments: effects of acute exposure to anxiolytic compounds and choice of Danio rerio line. Int J Comp Psychol 23(1):43PubMedPubMedCentralGoogle Scholar
  87. Shin JT, Fishman MC (2002) From zebrafish to human: modular medical models. Ann Rev Genom Hum Genet 3(1):311–340CrossRefGoogle Scholar
  88. Silva LJ, Lino CM, Meisel LM, Pena A (2012) Selective serotonin re-uptake inhibitors (SSRIs) in the aquatic environment: an ecopharmacovigilance approach. Sci Total Environ 437:185–195CrossRefPubMedGoogle Scholar
  89. Simmons DBD, McCallum ES, Balshine S, Chandramouli B, Cosgrove J, Sherry JP (2017) Reduced anxiety is associated with the accumulation of six serotonin reuptake inhibitors in wastewater treatment effluent exposed goldfish Carassius auratus. Sci Rep 7(1):17001CrossRefPubMedPubMedCentralGoogle Scholar
  90. Simon P, Dupuis R, Costentin J (1994) Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 61(1):59–64CrossRefGoogle Scholar
  91. Smith A (2002) Effects of caffeine on human behavior. Food Chem Toxicol 40(9):1243–1255CrossRefPubMedGoogle Scholar
  92. Sokolowski K, Corbin JG (2012) Wired for behaviors: from development to function of innate limbic system circuitry. Front Mol Neurosci 5:55CrossRefPubMedPubMedCentralGoogle Scholar
  93. Sommi RW, Crismon ML, Bowden CL (1987) Fluoxetine: a serotonin-specific, second-generation antidepressant. Pharmacother J Hum Pharmacol Drug Ther 7(1):1–14CrossRefGoogle Scholar
  94. Steimer T (2011) Animal models of anxiety disorders in rats and mice: some conceptual issues. Dialog Clin Neurosci 13(4):495–506Google Scholar
  95. Stewart AM, Kalueff AV (2015) Developing better and more valid animal models of brain disorders. Behav Brain Res 276:28–31CrossRefPubMedGoogle Scholar
  96. Stewart A, Wu N, Cachat J, Hart P, Gaikwad S, Wong K, Utterback E, Gilder T, Kyzar E, Newman A, Carols D, Chang K, Hook M, Rhymes C, Caffery M, Greenberg M, Zadina J, Kalueff AV (2011a) Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models. Prog Neuro-Psychopharmacol Biol Psychiatry 35(6):1421–1431CrossRefGoogle Scholar
  97. Stewart A, Maximino C, De Brito TM, Herculano AM, Gouveia A, Morato S, Cachet JM, Gaikwad S, Elegante MF, Hart PC, Kalueff AV (2011b) Neurophenotyping of adult zebrafish using the light/dark box paradigm. In: Kalueff AV, Cachat J (eds) Zebrafish neurobehavioral protocols. Humana Press, Clifton, pp 157–167CrossRefGoogle Scholar
  98. Stewart A, Gaikwad S, Kyzar E, Green J, Roth A, Kalueff AV (2012) Modeling anxiety using adult zebrafish: a conceptual review. Neuropharmacol 62(1):135–143CrossRefGoogle Scholar
  99. Stewart AM, Braubach O, Spitsbergen J, Gerlai R, Kalueff AV (2014) Zebrafish models for translational neuroscience research: from tank to bedside. Trends Neurosci 37(5):264–278CrossRefPubMedPubMedCentralGoogle Scholar
  100. Tandon P, Conlon F, Furlow JD, Horb ME (2016) Expanding the genetic toolkit in Xenopus: approaches and opportunities for human disease modeling. Devel Biol 426(2):325–335CrossRefGoogle Scholar
  101. Tierney AJ (2018) Invertebrate serotonin receptors: a molecular perspective on classification and pharmacology. J Exp Biol 221(19):jeb184838CrossRefPubMedGoogle Scholar
  102. Tovote P, Fadok JP, Lüthi A (2015) Neuronal circuits for fear and anxiety. Nat Rev Neurosci 16(6):317–331CrossRefGoogle Scholar
  103. Treit D, Engin E, McEown K (2009) Animal models of anxiety and anxiolytic drug action. Behavioral neurobiology of anxiety and its treatment. Springer, Berlin, pp 121–160CrossRefGoogle Scholar
  104. Trullas R, Skolnick P (1993) Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacol 111(3):323–331CrossRefGoogle Scholar
  105. van der Staay FJ, Arndt SS, Nordquist RE (2009) Evaluation of animal models of neurobehavioral disorders. Behav Brain Funct 5(1):11CrossRefPubMedPubMedCentralGoogle Scholar
  106. Van Mier P, Joosten HWJ, Van Rheden R, Ten Donkelaar HJ (1986) The development of serotonergic raphespinal projections in Xenopus laevis. Int J Devel Neurosci 4(5):465–475CrossRefGoogle Scholar
  107. Varty GB, Morgan CA, Cohen-Williams ME, Coffin VL, Carey GJ (2002) The gerbil elevated plus-maze I: behavioral characterization and pharmacological validation. Neuropsychopharmacol 27(3):357–370CrossRefGoogle Scholar
  108. Vendruscolo LF, Takahashi RN, Brüske GR, Ramos A (2003) Evaluation of the anxiolytic-like effect of NKP608, a NK1-receptor antagonist, in two rat strains that differ in anxiety-related behaviors. Psychopharmacol 170(3):287–293CrossRefGoogle Scholar
  109. Vetulani J, Stawarz RJ, Dingell JV, Sulser F (1976) A possible common mechanism of action of antidepressant treatments. Naunyn-Schmiedeberg’s Archi Pharmacol 293(2):109–114CrossRefGoogle Scholar
  110. Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Prot 2(2):322CrossRefGoogle Scholar
  111. Williams TD (2008) Individual variation in endocrine systems: moving beyond the ‘tyranny of the Golden Mean’. Philos Trans R Soc Lond B Biol Sci 363(1497):1687–1698CrossRefPubMedGoogle Scholar
  112. Willner P (1984) The validity of animal models of depression. Psychopharmacol 83(1):1–16CrossRefGoogle Scholar
  113. Wong K, Elegante M, Bartels B, Elkhayat S, Tien D, Roy S, Goodspeed J, Suciu C, Tan J, Grimes C, Chung A, Rosenberg M, Gaikwad S, Denmark A, Jackson A, Kadri F, Chung KM, Stewart S, Glider T, Beeson E, Zapolsky I, Wu N, Cachat J, Kalueff AV (2010) Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav Brain Res 208(2):450–457CrossRefPubMedGoogle Scholar
  114. Zohar J, Westenberg HGM (2000) Anxiety disorders: a review of tricyclic antidepressants and selective serotonin reuptake inhibitors. Acta Psychiatr Scand 101(S403):39–49CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biological SciencesTexas Tech UniversityLubbockUSA
  2. 2.Honors CollegeTexas Tech UniversityLubbockUSA

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