A functional division of Drosophila sweet taste neurons that is value-based and task-specific

Abstract

Sucrose is an attractive feeding substance and a positive reinforcer for Drosophila. But Drosophila females have been shown to robustly reject a sucrose-containing option for egg-laying when given a choice between a plain and a sucrose-containing option in specific contexts. How the sweet taste system of Drosophila promotes context-dependent devaluation of an egg-laying option that contains sucrose, an otherwise highly appetitive tastant, is unknown. Here, we report that devaluation of sweetness/sucrose for egg-laying is executed by a sensory pathway recruited specifically by the sweet neurons on the legs of Drosophila. First, silencing just the leg sweet neurons caused acceptance of the sucrose option in a sucrose versus plain decision, whereas expressing the channelrhodopsin CsChrimson in them caused rejection of a plain option that was “baited” with light over another that was not. Analogous bidirectional manipulations of other sweet neurons did not produce these effects. Second, circuit tracing revealed that the leg sweet neurons receive different presynaptic neuromodulations compared to some other sweet neurons and were the only ones with postsynaptic partners that projected prominently to the superior lateral protocerebrum (SLP) in the brain. Third, silencing one specific SLP-projecting postsynaptic partner of the leg sweet neurons reduced sucrose rejection, whereas expressing CsChrimson in it promoted rejection of a light-baited option during egg-laying. These results uncover that the Drosophila sweet taste system exhibits a functional division that is value-based and task-specific, challenging the conventional view that the system adheres to a simple labeled-line coding scheme.

Selective integration of diverse taste inputs within a single taste modality

“…The optogenetically induced avoidance may therefore result from unnatural levels or patterns of sugar neuron activation, which may cause compensatory changes in the downstream circuit. However, a recent study showed that activating different subsets of sugar neurons at the same relatively low intensity (6.8 µW/mm 2 ) elicited different effects on positional preference, including avoidance (Chen et al, 2022). Avoidance of sugar may be relevant during specific behaviors such as egg-laying, as flies avoid laying eggs on sugar in some contexts (Yang et al, 2008; Chen et al, 2022).…”

“…We have not performed a similar set of experiments for sugar neurons, and it is possible that they would show a greater degree of organ-specific behavioral regulation. Indeed, several studies have shown that sugar neurons in different organs have different behavioral effects (Thoma et al, 2016; Murata et al, 2017; Chen et al, 2021; Chen et al, 2022). Perhaps organ-specific roles for appetitive tastes are needed to generate the appropriate sequence of motor subprograms during feeding, whereas aversive behaviors do not follow an organ-specific sequence.…”

“…A set of sugar-responsive serotonergic neurons in the SEZ receives input from the labellum, but not the leg, and regulates sugar intake and insulin release (Yao and Scott, 2022). Finally, some tarsal sugar-sensing neurons arborize in the ventral nerve cord (Kwon et al, 2014) and activate leg-specific ascending second-order neurons (Kim et al, 2017), one of which regulates egg-laying behavior (Chen et al, 2022).…”

“…This would allow the fly to execute specific aversive responses depending on the compound that is detected or the organ that detects it. In support of a segregated processing model, several studies have shown that different subsets of sugar-or bitter-sensing neurons have different behavioral roles (Joseph and Heberlein, 2012; Thoma et al, 2016; Murata et al, 2017; Chen et al, 2019; Chen et al, 2021; Chen et al, 2022), with most of these studies comparing sugar-sensing neurons in different organs. Moreover, taste neurons in different organs project axons to spatially segregated regions within the subesophageal zone (SEZ), the primary taste area of the brain, suggesting that they may activate distinct downstream pathways (Wang et al, 2004; Kwon et al, 2014).…”

Evolutionary divergence in sugar valuation shifts Drosophila suzukii oviposition choice towards ripe fruit

“…We cannot exclude that more subtle differences in the numbers of func<onally-dis<nct sugar-GRN subtypes exist between species. Indeed, different sub-popula<ons of sugar-GRNs in D. melanogaster exert opposite effects on oviposi<on behavior, with GRNs on the legs inhibi<ng oviposi<on while GRNs on the proboscis promo<ng oviposi<on in a specific context 37 . Interes<ngly, we observed a reduc<on of sugar-GRNs in tarsal segments 2, 3 and 4 of the D. suzukii foreleg compared to D. melanogaster, raising the possibility that disappearance of specific neuronal subtypes could have relieved inhibitory sugar inputs onto CNS oviposi<on circuits in this species.…”