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Olfactory conditioning of proboscis activity in Drosophila melanogaster

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Abstract

Olfactory learning and memory processes in Drosophila have been well investigated with aversive conditioning, but appetitive conditioning has rarely been documented. Here, we report for the first time individual olfactory conditioning of proboscis activity in restrained Drosophila melanogaster. The protocol was adapted from those developed for proboscis extension conditioning in the honeybee Apis mellifera. After establishing a scale of small proboscis movements necessary to characterize responses to olfactory stimulation, we applied Pavlovian conditioning, with five trials consisting of paired presentation of a banana odour and a sucrose reward. Drosophila showed conditioned proboscis activity to the odour, with a twofold increase of percentage of responses after the first trial. No change occurred in flies experiencing unpaired presentations of the stimuli, confirming an associative basis for this form of olfactory learning. The adenylyl cyclase mutant rutabaga did not exhibit learning in this paradigm. This protocol generated at least a short-term memory of 15 min, but no significant associative memory was detected at 1 h. We also showed that learning performance was dependent on food motivation, by comparing flies subjected to different starvation regimes.

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Abbreviations

CS:

Conditioned stimulus

US:

Unconditioned stimulus

CR:

Conditioned response

UR:

Unconditioned response

WT:

Wild-type

SOG:

Suboesophageal ganglion

N:

No movement

T:

Labellum trembling

PL:

Palp trembling and/or slight extension of the labellum

E1:

Extension of the labellum

E2:

Extension of the labellum and the haustellum

E3:

Complete extension

Ns:

Samples size

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Acknowledgments

This work was started at the “Laboratoire de Neurobiologie Comparée des Invertébrés”, INRA and completed at the laboratory “Développement, Évolution et Plasticité du Système Nerveux”, CNRS. The authors thank Philippe Vernier for his scientific support to the project, David Laloi, Jean-Christophe Sandoz and Isabelle Bonod for sharing their experience and ideas with the conditioned proboscis activity protocol, Michel Chaminade, Jean-Yves Tiercelin and Pascal Abbas for installation, adaptation and maintenance of the system, Tazu Aoki and Guillaume Isabel for fruitful discussion and Niki Scaplehorn for linguistic advice. This study was supported in part by the “Agence Nationale pour la Recherche” and “the Fondation Bettencourt Schueller”, and Marie-Ange Chabaud was supported by the “Ecole Doctorale Sociétés et Vivant”, option “Biologie du Comportement”, at the University Paris 13.

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Author notes

  1. Thomas Preat

    Present address: Gènes et Dynamique des Systèmes de Mémoire, CNRS, ESPCI, 10 rue Vauquelin, 75005, Paris, France

Authors and Affiliations

  1. Développement, Évolution et Plasticité du Système Nerveux, CNRS, Bât. 32/33, Avenue de la Terrasse, 91198, Gif-sur-Yvette cedex, France

    Marie-Ange Chabaud, Thomas Preat & Laure Kaiser

  2. Centre de Recherches sur la Cognition Animale, Université Paul Sabatier, CNRS UMR 5169, Bât 4R3, 118 route de Narbonne, 31062, Toulouse Cedex 04, France

    Jean-Marc Devaud

  3. Direction des Relations Internationales, CNRS,, 3 rue Michel Ange, 75016, Paris, France

    Minh-Hà Pham-Delègue

Authors
  1. Marie-Ange Chabaud
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  2. Jean-Marc Devaud
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  4. Thomas Preat
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  5. Laure Kaiser
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Correspondence to Laure Kaiser.

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Chabaud, MA., Devaud, JM., Pham-Delègue, MH. et al. Olfactory conditioning of proboscis activity in Drosophila melanogaster . J Comp Physiol A 192, 1335–1348 (2006). https://doi.org/10.1007/s00359-006-0160-3

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  • DOI: https://doi.org/10.1007/s00359-006-0160-3

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