Studying social behavior in zebrafish (Danio rerioo) in the tests of social interaction, social preference, behavior in the shoaling and aggression tasks

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Abstract

Social interactions between conspecifics are an important factor in normal development of an individual in a community, and their deficits correlate with multiple psychiatric disorders. Several methods for assessing social behavior and its deficits have been described for zebrafish (Danio rerio), and include tests for social preference and social interaction. These tests are commonly used to model a wide range of social phenotypes that are potentially relevant to studying depression, pathological aggression, schizophrenia, autism, and other brain diseases. An important and widely used method for determining social behavior is the shoaling test, based on the innate, genetically fixed feature of zebrafish to form shoals/schools, the density of which depends on many factors, such as the presence of a predator, the effect of pharmacological drugs, etc. Aggression, along with shoaling, is an important manifestation of social behavior, which is also a core symptoms of multiple brain diseases, such as control disorder and conduct disorder. Here, we discuss various methods for assessing aggressive behavior in zebrafish (e.g., the mirror reflection tests), and their shoaling agonistic behaviors.

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About the authors

David S. Galstyan

Saint Petersburg State University; A.M. Granov Russian Research Center for Radiology and Surgical Technologies; Almazov National Medical Research Centre

Email: david_sam@mail.ru

Research Associate

Russian Federation, Saint Petersburg; Saint Petersburg; Saint Petersburg

Tatyana O. Kolesnikova

Sirius University of Science and Technology

Email: philimontani@yandex.ru
ORCID iD: 0000-0002-5561-8583
SPIN-code: 8558-7887

Research Associate

Russian Federation, Sochi

Yurii M. Kositsyn

Saint Petersburg State University

Email: ikosicin53@gmail.com
ORCID iD: 0000-0002-4266-808X

Research Associate

Russian Federation, Saint Petersburg

Konstantin N. Zabegalov

Sirius University of Science and Technology

Email: hatokiri@mail.ru
ORCID iD: 0000-0002-9748-0324
SPIN-code: 5993-6315

Research Associate

Russian Federation, Sochi

Mariya A. Gubaidullina

Sirius University of Science and Technology

Email: mariangub@gmail.com

Research Associate

Russian Federation, Sochi

Gleb O. Maslov

Sirius University of Science and Technology; Ural Federal University

Email: maslovog6@gmail.com

Research Associate

Russian Federation, Sochi; Yekaterinburg

Konstantin A. Demin

Saint Petersburg State University; Sirius University of Science and Technology; Almazov National Medical Research Centre

Email: deminkasci@gmail.com
SPIN-code: 3830-1853

Cand. Sci. (Biol.), Senior Research Associate

Russian Federation, Saint Petersburg; Sochi; Saint Petersburg

Allan V. Kalueff

Saint Petersburg State University; A.M. Granov Russian Research Center for Radiology and Surgical Technologies; Sirius University of Science and Technology; Almazov National Medical Research Centre; Ural Federal University; Novosibirsk State University; Research Institute of Neuroscience and Medicine; Moscow Institute of Physics and Technology

Author for correspondence.
Email: avkalueff@gmail.com
ORCID iD: 0000-0002-7525-1950
SPIN-code: 4134-0515

Dr. Sci. (Biol.), Professor

Russian Federation, Saint Petersburg; Saint Petersburg; Sochi; Saint Petersburg; Yekaterinburg; Novosibirsk; Novosibirsk; Moscow

References

  1. House JS, Landis KR, Umberson D. Social relationships and health. Science. 1988;241(4865):540–545. doi: 10.1126/science.3399889
  2. Engeszer RE, Ryan MJ, Parichy DM. Learned social preference in zebrafish. Curr Biol. 2004;14(10):881–884. doi: 10.1016/j.cub.2004.04.042
  3. Semenova AA, Lopatina OL, Salmina AB. Autism models and assessment techniquesfor autistic-like behavior in animals. I.P. Pavlov Journal of Higher Nervous Activity. 2020;70(2):147–162. (In Russ.) doi: 10.31857/S0044467720020112
  4. Stednitz SJ. The Social Brain of Zebrafish: [dissertation]. University of Oregon, 2019. 84 p.
  5. Stewart AM, Nguyen M, Wong K, et al. Developing zebrafish models of autism spectrum disorder (ASD). Prog Neuropsychopharmacol Biol Psychiatry. 2014;50:27–36. doi: 10.1016/j.pnpbp.2013.11.014
  6. Stednitz SJ, McDermott EM, Ncube D, et al. Forebrain control of behaviorally driven social orienting in zebrafish. Curr Biol. 2018;28(15):2445–2451.e3. doi: 10.1016/j.cub.2018.06.016
  7. Orger MB, de Polavieja GG. Zebrafish behavior: opportunities and challenges. Ann Rev Neurosci. 2017;40:125–147. doi: 10.1146/annurev-neuro-071714-033857
  8. Saverino C, Gerlai R. The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behav Brain Res. 2008;191(1):77–87. doi: 10.1016/j.bbr.2008.03.013
  9. Kalueff AV, Stewart AM. Zebrafish protocols for neurobehavioral research. New York: Humana Press, 2012. 357 p. doi: 10.1007/978-1-61779-597-8
  10. Grossman L, Stewart A, Gaikwad S, et al. Effects of piracetam on behavior and memory in adult zebrafish. Brain Res Bull. 2011; 85(1–2):58–63. doi: 10.1016/j.brainresbull.2011.02.008
  11. Veness C, Prior M, Bavin E, et al. Early indicators of autism spectrum disorders at 12 and 24 months of age: A prospective, longitudinal comparative study. Autism. 2012;16(2):163–177. doi: 10.1177/1362361311399936
  12. Figueira ML, Brissos S. Measuring psychosocial outcomes in schizophrenia patients. Curr Opin Psychiatry. 2011;24(2):91–99. doi: 10.1097/YCO.0b013e3283438119
  13. Kasumyan AO, Pavlov DS. Stainoe povedenie ryb. Moscow: Tovarishchestvo nauchnykh izdanii KMK, 2018. 274 p. (In Russ.)
  14. Miller N, Gerlai R. Quantification of shoaling behaviour in zebrafish (Danio rerio). Behav Brain Res. 2007;184(2):157–166. doi: 10.1016/j.bbr.2007.07.007
  15. Green J, Collins C, Kyzar EJ, et al. Automated high-throughput neurophenotyping of zebrafish social behavior. J Neurosci methods. 2012;210(2):266–271. doi: 10.1016/j.jneumeth.2012.07.017
  16. Cachat J, Kyzar EJ, Collins C, 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. 2013;236:258–269. doi: 10.1016/j.bbr.2012.08.041
  17. Kyzar EJ, Collins C, Gaikwad S, et al. Effects of hallucinogenic agents mescaline and phencyclidine on zebrafish behavior and physiology. Prog Neuropsychopharmacol Biol Psychiatry. 2012;37(1): 194–202. doi: 10.1016/j.pnpbp.2012.01.003
  18. Schaefer IC, Siebel AM, Piato AL, et al. The side-by-side exploratory test: a simple automated protocol for the evaluation of adult zebrafish behavior simultaneously with social interaction. Behav Pharmacol. 2015;26(7):691–696. doi: 10.1097/FBP.0000000000000145
  19. Buske C, Gerlai R. Early embryonic ethanol exposure impairs shoaling and the dopaminergic and serotoninergic systems in adult zebrafish. Neurotoxicol Teratol. 2011;33(6):698–707. doi: 10.1016/j.ntt.2011.05.0009
  20. Riehl R, Kyzar E, Allain A, et al. Behavioral and physiological effects of acute ketamine exposure in adult zebrafish. Neurotoxicol Teratol. 2011;33(6):658–667. doi: 10.1016/j.ntt.2011.05.011
  21. Speedie N, Gerlai R. Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav Brain Res. 2008;188(1): 168–177. doi: 10.1016/j.bbr.2007.10.031
  22. Kurta A, Palestis BG. Effects of ethanol on the shoaling behavior of zebrafish (Danio rerio). Dose-Response. 2010;8(4): dose-response.10–008.Palestis. doi: 10.2203/dose-response.10-008.Palestis
  23. Lindeyer CM, Langen EM, Swaney WT, Reader SM. Nonapeptide influences on social behaviour: effects of vasotocin and isotocin on shoaling and interaction in zebrafish. Behaviour. 2015;152(7–8): 897–915. doi: 10.1163/1568539X-00003261
  24. Delaney M, Follet C, Ryan N, et al. Social interaction and distribution of female zebrafish (Danio rerio) in a large aquarium. Biol Bull. 2002;203(20):240–241. doi: 10.2307/1543418
  25. Liu C-x, Li C-y, Hu C-c, et al. CRISPR/Cas9-induced shank3b mutant zebrafish display autism-like behaviors. Mol Autism. 2018;9:23. doi: 10.1186/s13229-018-0204-x
  26. Peper JS, de Reus MA, van den Heuvel MP, Schutter DJ. Short fused? Associations between white matter connections, sex steroids, and aggression across adolescence. Hum Brain Map. 2015;36: 1043–1052. doi: 10.1002/hbm.22684
  27. Wrangham RW. Two types of aggression in human evolution. PNAS USA. 2018;115(2):245–253. doi: 10.1073/pnas.1713611115
  28. American Psychiatric Association. Diagnostic and Statistical Manual of mental disorders. 5th ed. DSM-V. USA: American Psychiatric Publishing, 2013. 947 p.
  29. de Almeida RMM, Cabral JCC, Narvaes R. Behavioural, hormonal and neurobiological mechanisms of aggressive behaviour in human and nonhuman primates. Physiol Behav. 2015;143:121–135. doi: 10.1016/j.physbeh.2015.02.053
  30. Liu J, Zhong R, Xiong W, et al. Melatonin increases reactive aggression in humans. Psychopharmacology. 2017;234(19):2971–2978. doi: 10.1007/s00213-017-4693-7
  31. Lischinsky JE, Lin D. Neural mechanisms of aggression across species. Nat Neurosci. 2020;23(11):1317–1328. doi: 10.1038/s41593-020-00715-2
  32. Kolla NJ, Mishra A. The endocannabinoid system, aggression, and the violence of synthetic cannabinoid use, borderline personality disorder, antisocial personality disorder, and other psychiatric disorders. Front Behav Neurosci. 2018;12:41. doi: 10.3389/fnbeh.2018.00041
  33. Kudryavtseva NN, Smagin DA, Kovalenko IL, et al. Serotonergic genes in the development of anxiety/depression-like state and pathology of aggressive behavior in male mice: RNA-SEQ data. Molekulyarnaya biologiya. 2017;51(2):288–300. (In Russ.) doi: 10.7868/S0026898417020136
  34. O’Leary A, Laas K, Vaht M, et al. Nitric oxide synthase genotype interacts with stressful life events to increase aggression in male subjects in a population-representative sample. Eur Neuropsychopharmacol. 2020;30:56–65. doi: 10.1016/j.euroneuro.2019.07.241
  35. Suzuki H, Lucas LR. Neurochemical correlates of accumbal dopamine D2 and amygdaloid 5-HT 1B receptor densities on observational learning of aggression. Cogn Affect Behav Neurosci. 2015;15(2):460–474. doi: 10.3758/s13415-015-0337-8
  36. Oliveira RF, Silva JF, Simões JM. Fighting zebrafish: characterization of aggressive behavior and winner-loser effects. Zebrafish. 2011;8(2):73–81. doi: 10.1089/zeb.2011.0690
  37. Lumley LA, Charles RF, Charles RC, et al. Effects of social defeat and of diazepam on behavior in a resident–intruder test in male DBA/2 mice. Pharmacol Biochem Behav. 2000;67(3):433–447. doi: 10.1016/s0091-3057(00)00382-8
  38. Jones LJ, Norton WHJ. Using zebrafish to uncover the genetic and neural basis of aggression, a frequent comorbid symptom of psychiatric disorders. Behav Brain Res. 2015;276:171–180. doi: 10.1016/j.bbr.2014.05.055
  39. Norton W, Bally-Cuif L. Adult zebrafish as a model organism for behavioural genetics. BMC Neuroscience. 2010;11:90. doi: 10.1186/1471-2202-11-90
  40. Pham M, Raymond J, Hester J, et al. Assessing social behavior phenotypes in adult zebrafish: shoaling, social preference, and mirror biting tests. In: Kalueff AV, Stewart AM, editors. Zebrafish protocols for neurobehavioral research. Totowa, NJ: Humana Press, 2012. P. 231–246. doi: 10.1007/978-1-61779-597-8_17
  41. Zabegalov KN, Kolesnikova TO, Khatsko SL, et al. Understanding zebrafish aggressive behavior. Behav Processes. 2019;158:200–210. doi: 10.1016/j.beproc.2018.11.010
  42. Sterling ME, Karatayev O, Chang G-Q, et al. Model of voluntary ethanol intake in zebrafish: Effect on behavior and hypothalamic orexigenic peptides. Behav Brain Res. 2015;278:29–39. doi: 10.1016/j.bbr.2014.09.024
  43. Echevarria DJ, Toms CN, Jouandot DJ. Alcohol-induced behavior change in zebrafish models. Rev Neurosci. 2011;22(1):85–93. doi: 10.1515/RNS.2011.010
  44. Parker MO, Annan LV, Kanellopoulos AH, et al. The utility of zebrafish to study the mechanisms by which ethanol affects social behavior and anxiety during early brain development. Prog Neuropsychopharmacol Biol Psychiatry. 2014;55:94–100. doi: 10.1016/j.pnpbp.2014.03.011
  45. Fontana BD, Meinerz DL, Rosa LV, et al. Modulatory action of taurine on ethanol-induced aggressive behavior in zebrafish. Pharmacol Biochem Behav. 2016;141:18–27. doi: 10.1016/j.pbb.2015.11.011
  46. Giacomini ACVV, Abreu MS, Giacomini LV, et al. Fluoxetine and diazepam acutely modulate stress induced-behavior. Behav Brain Res. 2016;296:301–310. doi: 10.1016/j.bbr.2015.09.027
  47. Theodoridi A, Tsalafouta A, Pavlidis M. Acute exposure to fluoxetine alters aggressive behavior of zebrafish and expression of genes involved in serotonergic system regulation. Front Neurosci. 2017;11:223. doi: 10.3389/fnins.2017.00223
  48. Michelotti P, Quadros VA, Pereira ME, Rosemberg DB. Ketamine modulates aggressive behavior in adult zebrafish. Neurosci Lett. 2018;684:164–168. doi: 10.1016/j.neulet.2018.08.009
  49. Colman JR, Baldwin D, Johnson LL, Scholz NL. Effects of the synthetic estrogen, 17α-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol. 2009;91(4):346–354. doi: 10.1016/j.aquatox.2008.12.001
  50. Filby AL, Paull GC, Searle F, et al. Environmental estrogen-induced alterations of male aggression and dominance hierarchies in fish: A mechanistic analysis. Environ Sci Technol. 2012;46(6): 3472–3479. doi: 10.1021/es204023d
  51. Norton WHJ, Stumpenhorst K, Faus-Kessler T, et al. Modulation of Fgfr1a signaling in zebrafish reveals a genetic basis for the aggression-boldness syndrome. J Neurosci. 2011;31(39): 13796–13807. doi: 10.1523/JNEUROSCI.2892-11.2011
  52. Aliczki M, Varga ZK, Balogh Z, Haller J. Involvement of 2-arachidonoylglycerol signaling in social challenge responding of male CD1 mice. Psychopharmacology. 2015;232:2157–2167. doi: 10.1007/s00213-014-3846-1
  53. Krug RG II, Lee HB, El Khoury LY, et al. The endocannabinoid gene faah2a modulates stress-associated behavior in zebrafish. PloS one. 2018;13(1):e0190897-e. doi: 10.1371/journal.pone.0190897
  54. Carreño Gutiérrez H, O’Leary A, Freudenberg F, et al. Nitric oxide interacts with monoamine oxidase to modulate aggression and anxiety-like behavior. Eur Neuropsychopharmacol. 2020;30:30–43. doi: 10.1016/j.euroneuro.2017.09.004

Copyright (c) 2022 Galstyan D.S., Kolesnikova T.O., Kositsyn Y.M., Zabegalov K.N., Gubaidullina M.A., Maslov G.O., Demin K.A., Kalueff A.V.

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