Four Individually Identified Paired Dopamine Neurons Signal Reward in Larval Drosophila

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

    Research output: Contribution to journalArticlepeer-review

    45 Citations (Scopus)

    Abstract

    Dopaminergic neurons serve multiple functions, including reinforcement processing during associative learning [1-12]. 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, 13]. Dopaminergic neurons mediating reinforcement in insect olfactory learning target the mushroom bodies, a higher-order "cortical" brain region [1-5, 11, 12, 14, 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 [1-4, 7, 9, 10] (but see [6]). The numerical simplicity and connectomic tractability of the larval nervous system [16-19] now offers a prospect for studying circuit principles of dopamine function at unprecedented resolution.

    Original languageEnglish
    Pages (from-to)661-669
    Number of pages9
    JournalCurrent Biology
    Volume26
    Issue number5
    DOIs
    Publication statusPublished - 2016 Mar 7

    Keywords

    • Drosophila larva
    • dopamine
    • learning and memory
    • mushroom body
    • olfaction
    • reward
    • taste

    ASJC Scopus subject areas

    • Biochemistry, Genetics and Molecular Biology(all)
    • Agricultural and Biological Sciences(all)

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