Abstract
SummaryDopaminergic neurons provide reward learning signals in mammals and insects [1–4]. Recent work in Drosophila has demonstrated that water-reinforcing dopaminergic neurons are different to those for nutritious sugars [5]. Here, we tested whether the sweet taste and nutrient properties of sugar reinforcement further subdivide the fly reward system. We found that dopaminergic neurons expressing the OAMB octopamine receptor [6] specifically convey the short-term reinforcing effects of sweet taste [4]. These dopaminergic neurons project to the β′2 and γ4 regions of the mushroom body lobes. In contrast, nutrient-dependent long-term memory requires different dopaminergic neurons that project to the γ5b regions, and it can be artificially reinforced by those projecting to the β lobe and adjacent α1 region. Surprisingly, whereas artificial implantation and expression of short-term memory occur in satiated flies, formation and expression of artificial long-term memory require flies to be hungry. These studies suggest that short-term and long-term sugar memories have different physiological constraints. They also demonstrate further functional heterogeneity within the rewarding dopaminergic neuron population.
Highlights
Sweet taste and nutrient value of sugars reinforce learning in Drosophila [7, 8]
Reinforcing octopamine activates a subpopulation of dopaminergic neurons via the Ca2+-coupled a-adrenergic-like octopamine receptor OAMB
We investigated whether octopamine dependence separates rewarding dopaminergic neurons
Summary
Sweet taste and nutrient value of sugars reinforce learning in Drosophila [7, 8]. Octopaminergic neurons convey sweet taste signals [4, 9]. LTM performance of oambP-GAL4;UAS-shits1 flies was indistinguishable from controls, demonstrating a specific loss of STM (Figure 1G), consistent with TbhM18 flies trained with sucrose (Figure 1A). We tested a reinforcing role of oambP-GAL4 neurons by pairing their activation, using UAS-dTrpA1, with odor presentation (Figures 1H and 1I).
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