Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila

By Wolf Huetteroth, E. Perisse, Suewei Lin, M. Klappenbach, Christopher J. Burke, S. Waddell. 2015

230 citations recorded by the source corpus.

Summary Dopaminergic 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.

Subfields: Cellular and Molecular Neuroscience, Immunology, Insect Science

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135.001”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Metabolic states, such as thirst and hunger, have been shown to gate appetitive reinforcement by water and sugar rewards (Burke et al., 2012; Huetteroth et al., 2015; Lin et al., 2014), permitting state-dependent formation of olfactory associations only in motivated animals.”
The complete connectome of a learning and memory centre in an insect brain (2017, background): “It has been shown in adult Drosophila that co-activation of KCs and DANs can associatively modulate the KC-MBON synapse 5;19;20;22;24;26–28 .”
A connectome of a learning and memory center in the adult Drosophila brain (2017, methodology): “It is possible to induce memory formation in this circuit by pairing odor delivery with artificial activation of DANs (Schroll et al., 2006; Claridge-Chang et al., 2009; Aso et al., 2010, 2012; Yamagata et al., 2015; Liu et al., 2012; Burke et al., 2012; Huetteroth et al., 2015; Perisse et al., 2013”
Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila (2018, background): “Current Opinion in Neurobiology 2018, 49:51–58 different DANs [36,52] and that it is possible to artificially uncouple the taste and nutritious value by manipulating these neurons, or using a sweet but not nutritious sugar in an associative learning paradigm, then delivering nutritious food up to se”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “Surprisingly, the short- and long-term phases of memory are so independent that LTM can form in the absence of any behaviorally measured short-term memory (STM) (Trannoy et al. 2011, Yamagata et al. 2015).”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, background): “This longlasting depression, however, is likely not mediated by b02 PAM neurons but rather depends on PAM neurons innervating other lobe regions including g5 [28, 38].”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “Even reinforcement by sweet taste versus caloric intake is localized to distinct compartments (Huetteroth et al., 2015).”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, unknown): “Interestingly, the induced LTM is undetectable immediately after conditioning but gradually develops with time (Das et al., 2014; Huetteroth et al., 2015; Yamagata et al., 2015).”