Rapid olfactory discrimination learning in adult zebrafish.

Iori Namekawa, Nila R Moenig, Rainer W Friedrich
Author Information
  1. Iori Namekawa: Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058, Basel, Switzerland.
  2. Nila R Moenig: Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058, Basel, Switzerland.
  3. Rainer W Friedrich: Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058, Basel, Switzerland. Rainer.Friedrich@fmi.ch. ORCID

Abstract

The zebrafish is a model organism to study olfactory information processing, but efficient behavioral procedures to analyze olfactory discrimination and memory are lacking. We devised an automated odor discrimination task for adult zebrafish based on olfactory conditioning of feeding behavior. Presentation of a conditioned odor (CS+), but not a neutral odor (CS-) was followed by food delivery at a specific location. Fish developed differential behavioral responses to CS+ and CS- within a few trials. The behavioral response to the CS+ was complex and included components reminiscent of food search such as increased swimming speed and water surface sampling. Appetitive behavior was therefore quantified by a composite score that combined measurements of multiple behavioral parameters. Robust discrimination behavior was observed in different strains, even when odors were chemically similar, and learned preferences could overcome innate odor preferences. These results confirm that zebrafish can rapidly learn to make fine odor discriminations. The procedure is efficient and provides novel opportunities to dissect the neural mechanisms underlying olfactory discrimination and memory.

Keywords

References

  1. Nature. 2010 May 6;465(7294):47-52 [PMID: 20393466]
  2. Nat Neurosci. 2010 Nov;13(11):1354-6 [PMID: 20935642]
  3. Neuron. 2017 Mar 8;93(5):1198-1212.e5 [PMID: 28238548]
  4. Nat Neurosci. 2013 Nov;16(11):1678-86 [PMID: 24077563]
  5. Chem Senses. 1999 Dec;24(6):637-45 [PMID: 10587496]
  6. Nature. 2011 Nov 13;479(7374):493-8 [PMID: 22080956]
  7. Chem Senses. 2012 Jan;37(1):65-75 [PMID: 21778519]
  8. Nat Neurosci. 2011 Nov 20;15(1):155-61 [PMID: 22101640]
  9. Neuron. 2004 Dec 2;44(5):865-76 [PMID: 15572116]
  10. Nat Rev Drug Discov. 2015 Oct;14(10):721-31 [PMID: 26361349]
  11. Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11691-6 [PMID: 11553778]
  12. Zebrafish. 2013 Mar;10(1):70-86 [PMID: 23590400]
  13. Nat Neurosci. 2016 Jun;19(6):816-25 [PMID: 27089019]
  14. Neuron. 2006 Aug 3;51(3):351-8 [PMID: 16880129]
  15. Front Neural Circuits. 2013 Apr 23;7:71 [PMID: 23630467]
  16. Science. 2001 Feb 2;291(5505):889-94 [PMID: 11157170]
  17. Behav Brain Res. 2009 Mar 2;198(1):190-8 [PMID: 19056431]
  18. Neuron. 1997 May;18(5):737-52 [PMID: 9182799]
  19. Biomed Opt Express. 2016 Apr 04;7(5):1656-71 [PMID: 27231612]
  20. Behav Brain Res. 2010 Feb 11;207(1):99-104 [PMID: 19800919]
  21. Neurobiol Learn Mem. 2007 Jan;87(1):72-7 [PMID: 16861014]
  22. Front Neural Circuits. 2013 Apr 17;7:67 [PMID: 23641200]
  23. Learn Mem. 2012 Mar 20;19(4):170-7 [PMID: 22434824]
  24. Annu Rev Neurosci. 2013 Jul 8;36:383-402 [PMID: 23725002]
  25. Behav Neurosci. 2009 Apr;123(2):430-7 [PMID: 19331465]
  26. Cell. 2010 Apr 2;141(1):154-165 [PMID: 20303157]
  27. Behav Brain Res. 2017 Jan 15;317:444-452 [PMID: 27659557]
  28. Front Neural Circuits. 2014 Jul 30;8:91 [PMID: 25126059]
  29. Psychopharmacology (Berl). 2009 Jan;202(1-3):103-9 [PMID: 18716760]
  30. Neuron. 2013 Jun 5;78(5):881-94 [PMID: 23684786]
  31. Nat Neurosci. 1999 Nov;2(11):1003-9 [PMID: 10526340]
  32. Prog Neuropsychopharmacol Biol Psychiatry. 2011 Aug 1;35(6):1409-15 [PMID: 20837077]
  33. Neuron. 2016 Oct 5;92(1):174-186 [PMID: 27667005]
  34. Nat Protoc. 2012 Jun 28;7(7):1410-25 [PMID: 22743832]
  35. Curr Biol. 2018 Jan 8;28(1):1-14.e3 [PMID: 29249662]
  36. Dev Dyn. 2005 Sep;234(1):229-42 [PMID: 16086331]
  37. Science. 2008 Mar 28;319(5871):1842-5 [PMID: 18369149]
  38. J Integr Neurosci. 2012 Mar;11(1):73-85 [PMID: 22744784]
  39. Science. 2016 Apr 1;352(6281):87-90 [PMID: 27034372]
  40. Chem Senses. 2000 Feb;25(1):21-9 [PMID: 10667990]
  41. Nat Neurosci. 2009 Apr;12(4):474-82 [PMID: 19305401]
  42. Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20508-13 [PMID: 23197836]
  43. Genes Brain Behav. 2006 Oct;5(7):497-505 [PMID: 17010096]
  44. Curr Opin Neurobiol. 2013 Feb;23(1):119-26 [PMID: 23246238]
  45. J Comp Physiol A. 1995;177(2):191-9 [PMID: 7636767]
  46. Front Neural Circuits. 2015 Aug 18;9:39 [PMID: 26347614]
  47. Nat Neurosci. 2016 Jul;19(7):897-904 [PMID: 27239939]
  48. Behav Brain Res. 2008 Aug 5;191(1):77-87 [PMID: 18423643]
  49. R Soc Open Sci. 2015 Aug 26;2(8):150220 [PMID: 26361550]
  50. Elife. 2014 Mar 18;3:e02109 [PMID: 24642413]
  51. Curr Biol. 2014 Feb 17;24(4):434-9 [PMID: 24508164]

Grants

  1. FR 1667/2-2/Deutsche Forschungsgemeinschaft
  2. 31003A_135196/Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
  3. 310030B_1528331/Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
  4. 742576/H2020 European Research Council

MeSH Term

Animals
Conditioning, Classical
Discrimination Learning
Feeding Behavior
Female
Male
Odorants
Olfactory Perception
Smell
Zebrafish

Word Cloud

Created with Highcharts 10.0.0olfactorydiscriminationodorzebrafishbehavioralbehaviorCS+efficientmemoryadultCS-foodpreferencesmodelorganismstudyinformationprocessingproceduresanalyzelackingdevisedautomatedtaskbasedconditioningfeedingPresentationconditionedneutralfolloweddeliveryspecificlocationFishdevelopeddifferentialresponseswithintrialsresponsecomplexincludedcomponentsreminiscentsearchincreasedswimmingspeedwatersurfacesamplingAppetitivethereforequantifiedcompositescorecombinedmeasurementsmultipleparametersRobustobserveddifferentstrainsevenodorschemicallysimilarlearnedovercomeinnateresultsconfirmcanrapidlylearnmakefinediscriminationsprocedureprovidesnovelopportunitiesdissectneuralmechanismsunderlyingRapidlearningBehaviorDiscriminationLearningOlfactionZebrafish

Similar Articles

Cited By