Distinct sweet taste receptor neurons in the legs of Drosophila

• Applicant: Professor Dr. Thomas Wachtler-Kulla, since 5/2014
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2013 to 2017
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 239139988

• Final Report Year: 2017

Final Report Abstract

Taste is critical for deciding what to eat. In mammals, the tongue is the main taste organ. However, insects have many taste organs, distributed all over their bodies. The role of these organs is not understood well. In this project, we used the fruit fly Drosophila melanogaster as a model for insects to answer this question. Using powerful genetic tools available in this model organism, we found that sweet taste sensory neurons have specialized functions. In particular, one group of neurons in the legs projects directly to the brain and controls feeding initiation through extension of the proboscis. Another group of leg neurons projects locally, to the thoracic ganglia, and controls stopping when food is detected. These results show how different sets of sweet taste sensory neurons help coordinate the early stages of feeding. Food selection can also depend on the animal’s previous experiences and memory. In particular, fruit flies can remember not only the sweetness of a sugar, but also its nutritional content. To understand how these two properties are conveyed to the brain, we blocked subsets of PAM cluster neurons, which mediate sugar reward, and tested various sugars. To our surprise, we found that the PAM cluster can be subdivided into two subclusters. One subcluster conveys sweet taste information, which only supports short-term memory, while the other conveys nutrition information and supports long-term memory. In this way, longterm memory is only formed for nutritive sugars, highlighting their importance for survival.

Publications

• Converging Circuits Mediate Temperature and Shock Aversive Olfactory Conditioning in Drosophila. 2014. Curr Biol. 24(15), 1712
  Galili, Dana Shani; Dylla, Kristina V.; Lüdke, Alja; Friedrich, Anja B.; Yamagata, Nobuhiro; Wong, Jin Yan Hilary; Ho, Chien Hsien; Szyszka, Paul & Tanimoto, Hiromu
  
• Distinct dopamine neurons mediate reward signals for short- and long-term memories. 2015. Proc Natl Acad Sci USA. 112(2), 578
  Yamagata, Nobuhiro; Ichinose, Toshiharu; Aso, Yoshinori; Plaçais, Pierre-Yves; Friedrich, Anja B.; Sima, Richard J.; Preat, Thomas; Rubin, Gerald M. & Tanimoto, Hiromu
  
• Reward signal in a recurrent circuit drives appetitive long-term memory formation. 2015. ELife 4, e10719
  Ichinose, Toshiharu; Aso, Yoshinori; Yamagata, Nobuhiro; Abe, Ayako; Rubin, Gerald M & Tanimoto, Hiromu
  
• Functional dissociation in sweet taste receptor neurons between and within taste organs of Drosophila. 2016. Nat Commun. 7, 10628
  Thoma, Vladimiros; Knapek, Stephan; Arai, Shogo; Hartl, Marion; Kohsaka, Hiroshi; Sirigrivatanawong, Pudith; Abe, Ayako; Hashimoto, Koichi & Tanimoto, Hiromu
  
• Supression of Dopamine Neurons Mediates Reward. 2016. PLoS Biol. 14(12), e1002586
  Yamagata, Nobuhiro; Hiroi, Makoto; Kondo, Shu; Abe, Ayako & Tanimoto, Hiromu
  
• The Role of the Gustatory System in the Coordination of Feeding. 2017. eNeuro 4(6) ENEURO.0324-17.2017
  Thoma, Vladimiros; Kobayashi, Kimiko & Tanimoto, Hiromu