期刊名称:Proceedings of the National Academy of Sciences
印刷版ISSN:0027-8424
电子版ISSN:1091-6490
出版年度:2022
卷号:119
期号:3
DOI:10.1073/pnas.2110158119
语种:English
出版社:The National Academy of Sciences of the United States of America
摘要:Significance
Sweet taste neurons in both
Drosophila and mice are often thought to be hardwired to promote appetitive responses and signal the presence of reward. Here, exploiting
Drosophila females’ robust rejection of sucrose substrates over plain ones during egg-laying in one specific context, we discovered that
Drosophila sweet neurons can be divided into at least two anatomically and functionally distinct groups that confer positive and negative values, respectively, to options during egg-laying. This discovery reveals one design feature of the
Drosophila sweet taste system that allows sweetness/sugars to be valued differently according to context and animals’ behavioral goal (i.e., feeding versus egg-laying), pointing to a level of flexibility and sophistication that is not seen in the system’s mammalian counterparts.
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.