Animals approach stimuli that predict a pleasant outcome1. After the paired presentation of an odour and a reward, Drosophila melanogaster can develop a conditioned approach towards that odour2,3. Despite recent advances in understanding the neural circuits for associative memory and appetitive motivation4, the cellular mechanisms for reward processing in the fly brain are unknown. Here we show that a group of dopamine neurons in the protocerebral anterior medial (PAM) cluster signals sugar reward by transient activation and inactivation of target neurons in intact behaving flies. These dopamine neurons are selectively required for the reinforcing property of, but not a reflexive response to, the sugar stimulus. In vivo calcium imaging revealed that these neurons are activated by sugar ingestion and the activation is increased on starvation. The output sites of the PAM neurons are mainly localized to the medial lobes of the mushroom bodies (MBs), where appetitive olfactory associative memory is formed5,6. We therefore propose that the PAM cluster neurons endow a positive predictive value to the odour in the MBs. Dopamine in insects is known to mediate aversive reinforcement signals5,7,8,9,10,11. Our results highlight the cellular specificity underlying the various roles of dopamine and the importance of spatially segregated local circuits within the MBs.
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We thank L. Bräcker, M. Feind, C. Murphy, C. Schnaitmann and T. Templier for technical assistance and experiments that inspired this study; P. Garrity, the Kyoto Drosophila Genetic Resource Center and the Bloomington Stock Center for fly stocks; and Y.Y. Ma, Z. Q. Meng, R. Menzel, A. Thum, S. Waddell and the members of the Tanimoto laboratory for discussion and/or critical reading of the manuscript. C.L., Y.A., N.Y. and P.-Y.P. were sponsored by a Chinese–European doctoral training program from Max-Planck-Gesellschaft and the Chinese Academy of Sciences, the Deutscher Akademischer Austausch Dienst, the Alexander von Humboldt Foundation, and the Région Île-de-France, respectively. This work was supported by the Agence Nationale pour la Recherche (T.P.), the Howard Hughes Medical Institute (G.M.R.), Bernstein Focus Learning from the Bundesministerium für Bildung und Forschung and the Max-Planck-Gesellschaft (H.T.).
This file contains a movie showing the expression pattern of R58E02-GAL4 in the brain.
This file contains a movie showing the expression pattern of DDC-GAL4 in the central brain.
This file contains a movie showing the expression pattern of DDC-GAL4 with R58E02-GAL80 in the central brain.
This file contains a movie showing differential labelling of NP5272-GAL4 and R58E02-LexA in the cell body region of the PAM cluster.
This file contains a movie showing differential labelling of TH-GAL4 and R58E02-LexA in the MB.