Four individually identified paired dopamine neurons signal reward in larval Drosophila

Rohwedder, Astrid; Wenz, Nana L.; Stehle, Bernhard; Huser, Annina; Yamagata, Nobuhiro; Zlatic, Marta; Truman, James W.; Tanimoto, Hiromu; Saumweber, Timo; Gerber, Bertram; Thum, Andreas S.

doi:10.1016/j.cub.2016.01.012

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Four individually identified paired dopamine neurons signal reward in larval Drosophila

Rohwedder, Astrid Department of Biology, University of Fribourg, Switzerland - Department of Biology, University of Konstanz, Germany
Wenz, Nana L. Department of Biology, University of Konstanz, Germany
Stehle, Bernhard Department of Biology, University of Konstanz, Germany
Huser, Annina Department of Biology, University of Konstanz, Germany
Yamagata, Nobuhiro Graduate School of Life Sciences, Tohoku University, Sendai, Japan
Zlatic, Marta Janelia Research Campus, Ashburn, USA
Truman, James W. Janelia Research Campus, Ashburn, USA
Tanimoto, Hiromu Graduate School of Life Sciences, Tohoku University, Sendai, Japan
Saumweber, Timo Abteilung Genetik von Lernen und Gedächtnis, Leibniz Institut für Neurobiologie (LIN), Magdeburg, Germany
Gerber, Bertram Abteilung Genetik von Lernen und Gedächtnis, Leibniz Institut für Neurobiologie (LIN), Magdeburg, Germany - Otto von Guericke Universität Magdeburg, Institut für Biologie, Verhaltensgenetik, Magdeburg, Germany - Center for Behavioral Brain Sciences (CBBS), 39106 Magdeburg, Germany
Thum, Andreas S. Department of Biology, University of Fribourg, Switzerland - Department of Biology, University of Konstanz, Germany - Zukunftskolleg, University of Konstanz, Germany

07.03.2016

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Current Biology. - 2016, vol. 26, no. 5, p. 661–669

English Dopaminergic neurons serve multiple functions, including reinforcement processing during associative learning [1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11 and 12]. It is thus warranted to understand which dopaminergic neurons mediate which function. We study larval Drosophila, in which only approximately 120 of a total of 10,000 neurons are dopaminergic, as judged by the expression of tyrosine hydroxylase (TH), the rate- limiting enzyme of dopamine biosynthesis [ 5 and 13]. Dopaminergic neurons mediating reinforcement in insect olfactory learning target the mushroom bodies, a higher-order “cortical” brain region [ 1, 2, 3, 4, 5, 11, 12, 14 and 15]. We discover four previously undescribed paired neurons, the primary protocerebral anterior medial (pPAM) neurons. These neurons are TH positive and subdivide the medial lobe of the mushroom body into four distinct subunits. These pPAM neurons are acutely necessary for odor-sugar reward learning and require intact TH function in this process. However, they are dispensable for aversive learning and innate behavior toward the odors and sugars employed. Optogenetical activation of pPAM neurons is sufficient as a reward. Thus, the pPAM neurons convey a likely dopaminergic reward signal. In contrast, DL1 cluster neurons convey a corresponding punishment signal [5], suggesting a cellular division of labor to convey dopaminergic reward and punishment signals. On the level of individually identified neurons, this uncovers an organizational principle shared with adult Drosophila and mammals [ 1, 2, 3, 4, 7, 9 and 10] (but see [6]). The numerical simplicity and connectomic tractability of the larval nervous system [ 16, 17, 18 and 19] now offers a prospect for studying circuit principles of dopamine function at unprecedented resolution.

Faculty

Faculté des sciences et de médecine

Department

Département de Biologie

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