Abstract
Most animals possess taste receptors neurons detecting potentially noxious compounds. In humans, the ligands which activate these neurons define a sensory space called “bitter”. By extension, this term has been used in animals and insects to define molecules which induce aversive responses. In this review, based on our observations carried out in Drosophila, we examine how bitter compounds are detected and if bitter-sensitive neurons respond only to molecules bitter to humans. Like most animals, flies detect bitter chemicals through a specific population of taste neurons, distinct from those responding to sugars or to other modalities. Activating bitter-sensitive taste neurons induces aversive reactions and inhibits feeding. Bitter molecules also contribute to the suppression of sugar-neuron responses and can lead to a complete inhibition of the responses to sugar at the periphery. Since some bitter molecules activate bitter-sensitive neurons and some inhibit sugar detection, bitter molecules are represented by two sensory spaces which are only partially congruent. In addition to molecules which impact feeding, we recently discovered that the activation of bitter-sensitive neurons also induces grooming. Bitter-sensitive neurons of the wings and of the legs can sense chemicals from the gram negative bacteria, Escherichia coli, thus adding another biological function to these receptors. Bitter-sensitive neurons of the proboscis also respond to the inhibitory pheromone, 7-tricosene. Activating these neurons by bitter molecules in the context of sexual encounter inhibits courting and sexual reproduction, while activating these neurons with 7-tricosene in a feeding context will inhibit feeding. The picture that emerges from these observations is that the taste system is composed of detectors which monitor different “categories” of ligands, which facilitate or inhibit behaviors depending on the context (feeding, sexual reproduction, hygienic behavior), thus considerably extending the initial definition of “bitter” tasting.
Highlights
In humans, bitter taste is defined as a sensation associated with the perception of potentially toxic molecules such as alkaloids, which induce innate aversive reactions (Ventura and Worobey, 2013)
Bitter sensation is inferred in other animals, even in insects, since the activation of specific taste cells triggers aversive reactions often associated with feeding and serves to protect individuals from accidental ingestion of noxious molecules
The hypothesis that categories of receptors deal with different types of molecules inducing appetitive or aversive behaviors, does not match the view that emerged when recording from taste nerves in vertebrates, where no corresponding functional segregation could be made between fibers (Contreras and Lundy, 2000; Chen and Di Lorenzo, 2008; Frank et al, 2008)
Summary
Bitter taste is defined as a sensation associated with the perception of potentially toxic molecules such as alkaloids, which induce innate aversive reactions (Ventura and Worobey, 2013). Molecular studies support the view that bitter taste is mediated in vertebrates by specific receptor proteins Tas2Rs (Mueller et al, 2005; Meyerhof et al, 2011; Barretto et al, 2015), which are expressed within a specific population of taste sensory cells Activating these taste cells either by genuine ligands or through optogenetics, triggers aversive reactions (Chen et al, 2011). Bitter sensation is inferred in other animals, even in insects, since the activation of specific taste cells triggers aversive reactions often associated with feeding and serves to protect individuals from accidental ingestion of noxious molecules. For A. mellifera, it is possible that their food resource has a composition that limits the risks of being exposed to noxious molecules These observations suggest that all organisms have evolved a taste modality that allows them to detect and to avoid molecules which represents a potential danger. We want to review recent evidence drawn mostly from our own experience in Drosophila that cells sensitive to bitter compounds react to classes of molecules important in different behavioral contexts, and stress that bitter molecules have an impact on the detection of other molecules detected through other taste modalities
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