Collective Emotional Contagion in Zebrafish.

Daniel Alberto Burbano Lombana, Simone Macrì, Maurizio Porfiri
Author Information
  1. Daniel Alberto Burbano Lombana: Department of Mechanical and Aerospace Engineering, Tandon School of Engineering, New York University, Brooklyn, NY, United States.
  2. Simone Macrì: Centre for Behavioural Sciences and Mental Health, Istituto Superiore di Sanità, Viale Regina Elena, Rome, Italy.
  3. Maurizio Porfiri: Department of Mechanical and Aerospace Engineering, Tandon School of Engineering, New York University, Brooklyn, NY, United States.

Abstract

Seeking to match our emotional state with one of those around us is known as emotional contagion-a fundamental biological process that underlies social behavior across several species and taxa. While emotional contagion has been traditionally considered to be a prerogative of mammals and birds, recent findings are demonstrating otherwise. Here, we investigate emotional contagion in groups of zebrafish, a freshwater model species which is gaining momentum in preclinical studies. Zebrafish have high genetic homology to humans, and they exhibit a complex behavioral repertoire amenable to study social behavior. To investigate whether individual emotional states can be transmitted to group members, we pharmacologically modulated anxiety-related behaviors of a single fish through Citalopram administration and we assessed whether the altered emotional state spread to a group of four untreated conspecifics. By capitalizing upon our in-house developed tracking algorithm, we successfully preserved the identity of all the subjects and thoroughly described their individual and social behavioral phenotypes. In accordance with our predictions, we observed that Citalopram administration consistently reduced behavioral anxiety of the treated individual, in the form of reduced geotaxis, and that such a behavioral pattern readily generalized to the untreated subjects. A transfer entropy analysis of causal interactions within the group revealed that emotional contagion was directional, whereby the treated individual influenced untreated subjects, but not vice-versa. This study offers additional evidence that emotional contagion is biologically preserved in simpler living organisms amenable to preclinical investigations.

Keywords

References

  1. Exp Neurol. 2018 Jan;299(Pt A):157-171 [PMID: 28987462]
  2. Prog Neuropsychopharmacol Biol Psychiatry. 2021 Jun 8;108:110172 [PMID: 33188831]
  3. BMC Neurosci. 2010 Aug 02;11:90 [PMID: 20678210]
  4. J Theor Biol. 2015 Sep 7;380:480-8 [PMID: 26113192]
  5. Philos Trans R Soc Lond B Biol Sci. 2018 May 19;373(1746): [PMID: 29581390]
  6. J R Soc Interface. 2020 Mar;17(164):20190563 [PMID: 32183638]
  7. Biol Bull. 2002 Jun;202(3):296-305 [PMID: 12087003]
  8. BMC Biol. 2018 Apr 25;16(1):45 [PMID: 29690872]
  9. Br J Psychiatry. 2009 Jun;194(6):535-40 [PMID: 19478294]
  10. Behav Brain Res. 2014 Apr 15;263:16-21 [PMID: 24480421]
  11. Exp Mol Med. 2021 Mar;53(3):310-317 [PMID: 33649498]
  12. Behav Brain Res. 2020 Jan 27;378:112256 [PMID: 31614187]
  13. Science. 2006 Jun 30;312(5782):1967-70 [PMID: 16809545]
  14. Nature. 2013 Apr 25;496(7446):498-503 [PMID: 23594743]
  15. Behav Brain Res. 2010 Apr 2;208(2):450-7 [PMID: 20035794]
  16. J Vis Exp. 2012 Nov 18;(69):e4196 [PMID: 23183629]
  17. Aquat Toxicol. 2016 Jan;170:297-309 [PMID: 26372090]
  18. Neurosci Biobehav Rev. 2020 Apr;111:149-165 [PMID: 31972204]
  19. Trends Neurosci. 2014 May;37(5):264-78 [PMID: 24726051]
  20. J Theor Biol. 2017 Dec 21;435:145-156 [PMID: 28916452]
  21. PeerJ. 2017 Sep 4;5:e3739 [PMID: 28890851]
  22. Zebrafish. 2013 Mar;10(1):70-86 [PMID: 23590400]
  23. Am J Psychiatry. 1989 Jan;146(1):10-9 [PMID: 2643353]
  24. Eur J Neurosci. 2003 Apr;17(8):1703-14 [PMID: 12752388]
  25. Int J Comp Psychol. 2010 Jan 1;23(1):43-61 [PMID: 20523756]
  26. Zebrafish. 2019 Jun;16(3):223-232 [PMID: 30625048]
  27. Neurobiol Dis. 2010 Oct;40(1):46-57 [PMID: 20472064]
  28. R Soc Open Sci. 2015 Dec 23;2(12):150505 [PMID: 27019737]
  29. J Am Psychoanal Assoc. 1958 Jul;6(3):433-41 [PMID: 13575267]
  30. Wiley Interdiscip Rev Cogn Sci. 2021 May 5;:e1560 [PMID: 33951303]
  31. Prog Neuropsychopharmacol Biol Psychiatry. 2020 Aug 30;102:109957 [PMID: 32360787]
  32. PLoS One. 2012;7(11):e48865 [PMID: 23166599]
  33. Proc Natl Acad Sci U S A. 2019 Jun 4;116(23):11547-11552 [PMID: 31110007]
  34. PeerJ. 2019 Oct 16;7:e7893 [PMID: 31637136]
  35. PLoS One. 2013 Oct 16;8(10):e76123 [PMID: 24146825]
  36. Trends Cogn Sci. 2012 Mar;16(3):143-4 [PMID: 22206750]
  37. Phys Rev E. 2016 Apr;93:042411 [PMID: 27176333]
  38. Neuropharmacology. 2018 Dec;143:250-267 [PMID: 30213592]
  39. J Neurosci Res. 2016 Jun;94(6):445-62 [PMID: 26833658]
  40. Sci Rep. 2017 May 16;7(1):1962 [PMID: 28512334]
  41. Philos Trans R Soc Lond B Biol Sci. 2018 May 19;373(1746): [PMID: 29581391]
  42. Lab Anim. 2020 Jun;54(3):213-224 [PMID: 31510859]

Grants

  1. R21 DA042558/NIDA NIH HHS

Word Cloud

Created with Highcharts 10.0.0emotionalcontagionbehavioralindividualsocialbehaviorgroupCitalopramuntreatedsubjectsstatespeciesinvestigatepreclinicalZebrafishamenablestudywhetheradministrationpreservedreducedtreatedgeotaxistransferentropySeekingmatchonearoundusknowncontagion-afundamentalbiologicalprocessunderliesacrossseveraltaxatraditionallyconsideredprerogativemammalsbirdsrecentfindingsdemonstratingotherwisegroupszebrafishfreshwatermodelgainingmomentumstudieshighgenetichomologyhumansexhibitcomplexrepertoirestatescantransmittedmemberspharmacologicallymodulatedanxiety-relatedbehaviorssinglefishassessedalteredspreadfourconspecificscapitalizinguponin-housedevelopedtrackingalgorithmsuccessfullyidentitythoroughlydescribedphenotypesaccordancepredictionsobservedconsistentlyanxietyformpatternreadilygeneralizedanalysiscausalinteractionswithinrevealeddirectionalwherebyinfluencedvice-versaoffersadditionalevidencebiologicallysimplerlivingorganismsinvestigationsCollectiveEmotionalContagionempathy

Similar Articles

Cited By