Rapid Olfactory Discrimination Learning in Adult Zebrafish

Overview

Journal Exp Brain Res

Specialty Neurology

Date 2018 Aug 9

PMID 30088022

Citations 7

Authors

Iori Namekawa

Nila R Moenig

Rainer W Friedrich

Affiliations

Soon will be listed here.

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.

Citing Articles

Olfactory Impairment and Recovery in Zebrafish () Following Cadmium Exposure.

Motta C, Carotenuto R, Fogliano C, Rosati L, Denre P, Panzuto R Biology (Basel). 2025; 14(1).

PMID: 39857307 PMC: 11761868. DOI: 10.3390/biology14010077.

Assessment of Replicability and Efforts to Refine an Operant Conditioning Procedure for Larval Zebrafish.

Agrillo C, Rovegno E, Dadda M, Bertolucci C, Bisazza A Animals (Basel). 2025; 14(24.

PMID: 39765587 PMC: 11672825. DOI: 10.3390/ani14243684.

Representational learning by optimization of neural manifolds in an olfactory memory network.

Hu B, Temiz N, Chou C, Rupprecht P, Meissner-Bernard C, Titze B bioRxiv. 2024; .

PMID: 39605658 PMC: 11601331. DOI: 10.1101/2024.11.17.623906.

Learning and memory formation in zebrafish: Protein dynamics and molecular tools.

Reemst K, Shahin H, Shahar O Front Cell Dev Biol. 2023; 11:1120984.

PMID: 36968211 PMC: 10034119. DOI: 10.3389/fcell.2023.1120984.

A simple semi-automated home-tank method and procedure to explore classical associative learning in adult zebrafish.

Buatois A, Siddiqi Z, Naim S, Marawi T, Gerlai R Behav Res Methods. 2023; 56(2):736-749.

PMID: 36814006 PMC: 10830691. DOI: 10.3758/s13428-023-02076-7.

References

Niessing J, Friedrich R . Olfactory pattern classification by discrete neuronal network states. Nature. 2010; 465(7294):47-52. DOI: 10.1038/nature08961. View

Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M . The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci. 2010; 13(11):1354-6. DOI: 10.1038/nn.2654. View

Yamada Y, Bhaukaurally K, Madarasz T, Pouget A, Rodriguez I, Carleton A . Context- and Output Layer-Dependent Long-Term Ensemble Plasticity in a Sensory Circuit. Neuron. 2017; 93(5):1198-1212.e5. PMC: 5352733. DOI: 10.1016/j.neuron.2017.02.006. View

Zhu P, Frank T, Friedrich R . Equalization of odor representations by a network of electrically coupled inhibitory interneurons. Nat Neurosci. 2013; 16(11):1678-86. DOI: 10.1038/nn.3528. View

Bodyak N, Slotnick B . Performance of mice in an automated olfactometer: odor detection, discrimination and odor memory. Chem Senses. 1999; 24(6):637-45. DOI: 10.1093/chemse/24.6.637. View

Blumhagen F, Zhu P, Shum J, Scharer Y, Yaksi E, Deisseroth K . Neuronal filtering of multiplexed odour representations. Nature. 2011; 479(7374):493-8. DOI: 10.1038/nature10633. View

Miklavc P, Valentincic T . Chemotopy of amino acids on the olfactory bulb predicts olfactory discrimination capabilities of zebrafish Danio rerio. Chem Senses. 2011; 37(1):65-75. DOI: 10.1093/chemse/bjr066. View

Chapuis J, Wilson D . Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci. 2011; 15(1):155-61. PMC: 3245808. DOI: 10.1038/nn.2966. View

Abraham N, Spors H, Carleton A, Margrie T, Kuner T, Schaefer A . Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron. 2004; 44(5):865-76. DOI: 10.1016/j.neuron.2004.11.017. View

10.

MacRae C, Peterson R . Zebrafish as tools for drug discovery. Nat Rev Drug Discov. 2015; 14(10):721-31. DOI: 10.1038/nrd4627. View

11.

Darland T, Dowling J . Behavioral screening for cocaine sensitivity in mutagenized zebrafish. Proc Natl Acad Sci U S A. 2001; 98(20):11691-6. PMC: 58791. DOI: 10.1073/pnas.191380698. View

12.

Kalueff A, Gebhardt M, Stewart A, Cachat J, Brimmer M, Chawla J . Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish. 2013; 10(1):70-86. PMC: 3629777. DOI: 10.1089/zeb.2012.0861. View

13.

Wanner A, Genoud C, Masudi T, Siksou L, Friedrich R . Dense EM-based reconstruction of the interglomerular projectome in the zebrafish olfactory bulb. Nat Neurosci. 2016; 19(6):816-25. DOI: 10.1038/nn.4290. View

14.

Rinberg D, Koulakov A, Gelperin A . Speed-accuracy tradeoff in olfaction. Neuron. 2006; 51(3):351-8. DOI: 10.1016/j.neuron.2006.07.013. View

15.

Friedrich R, Genoud C, Wanner A . Analyzing the structure and function of neuronal circuits in zebrafish. Front Neural Circuits. 2013; 7:71. PMC: 3632777. DOI: 10.3389/fncir.2013.00071. View

16.

Friedrich R, Laurent G . Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science. 2001; 291(5505):889-94. DOI: 10.1126/science.291.5505.889. View

17.

Braubach O, Wood H, Gadbois S, Fine A, Croll R . Olfactory conditioning in the zebrafish (Danio rerio). Behav Brain Res. 2008; 198(1):190-8. DOI: 10.1016/j.bbr.2008.10.044. View

18.

Friedrich R, Korsching S . Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron. 1997; 18(5):737-52. DOI: 10.1016/s0896-6273(00)80314-1. View

19.

Rupprecht P, Prendergast A, Wyart C, Friedrich R . Remote z-scanning with a macroscopic voice coil motor for fast 3D multiphoton laser scanning microscopy. Biomed Opt Express. 2016; 7(5):1656-71. PMC: 4871072. DOI: 10.1364/BOE.7.001656. View

20.

Sison M, Gerlai R . Associative learning in zebrafish (Danio rerio) in the plus maze. Behav Brain Res. 2009; 207(1):99-104. PMC: 2814798. DOI: 10.1016/j.bbr.2009.09.043. View