A comparative analysis of neural taste processing in animals

Sanchez, María Gabriela de Brito; Giurfa, Martín

doi:10.1098/rstb.2010.0327

Cited by 26 publications

(14 citation statements)

References 79 publications

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“…Actually, a similar inconsistency between peripheral recordings and the labeled line theory has been recently demonstrated in an insect, using multicellular recordings to monitor nerve activity and central responses in the suboesophageal ganglion of taste sensilla from the proboscis of Manduca sexta adults (Reiter et al, 2015 ). These opposed views (labeled lines vs across-fiber encoding) are difficult to reconcile (Scott and Giza, 2000 ; Smith et al, 2000 ; de Brito Sanchez and Giurfa, 2011 ) as each theory is missing elements for a complete proof (Fox, 2008 ).…”

Section: Contact Chemoreception In Drosophila Adulmentioning

confidence: 99%

Drosophila Bitter Taste(s)

French

Agha

Mitra

et al. 2015

Front. Integr. Neurosci.

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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.

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Section: Contact Chemoreception In Drosophila Adulmentioning

confidence: 99%

Drosophila Bitter Taste(s)

French

Agha

Mitra

et al. 2015

Front. Integr. Neurosci.

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“…It allows discriminating edible from non-edible items and is, therefore, crucial for survival. Research on taste perception has revealed both common and specific mechanisms of gustatory processing between the few species that have been extensively investigated until now 2 . A proper understanding of taste perception across species thus requires expanding the spectrum of species studied and a careful consideration of their feeding biology as a determinant of taste processing mechanisms.…”

Section: Introductionmentioning

confidence: 99%

Aversive gustatory learning and perception in honey bees

Guiraud

Hotier

Giurfa

et al. 2018

Sci Rep

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Taste perception allows discriminating edible from non-edible items and is crucial for survival. In the honey bee, the gustatory sense has remained largely unexplored, as tastants have been traditionally used as reinforcements rather than as stimuli to be learned and discriminated. Here we provide the first characterization of antennal gustatory perception in this insect using a novel conditioning protocol in which tastants are dissociated from their traditional food-reinforcement role to be learned as predictors of punishment. We found that bees have a limited gustatory repertoire via their antennae: they discriminate between broad gustatory modalities but not within modalities, and are unable to differentiate bitter substances from water. Coupling gustatory conditioning with blockade of aminergic pathways in the bee brain revealed that these pathways are not restricted to encode reinforcements but may also encode conditioned stimuli. Our results reveal unknown aspects of honey bee gustation, and bring new elements for comparative analyses of gustatory perception in animals.

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“…Neuronal structures responsible for acquisition and processing of odorant and taste information display a striking degree of similarity between invertebrates and vertebrates [59,94]. Since specific neuronal circuits can support different behaviours [95], conservation across taxa may not be surprising and could also explain the observation that entire circuits may be retained even across taxa that display different behaviours [96].…”

Section: Towards Formulating a Framework Of Analysis Across Levels Ofmentioning

confidence: 99%

“…The first articles [10,46,63,74] set in motion (or refresh) important discussions on general aspects of development and evolution pertaining to behaviour. These are then more specifically addressed in the studies discussed in the second series of articles [58,93,94,124,125].…”

Section: What the Articles Saymentioning

confidence: 99%

“…Gabriela De Brito Sanchez & Martin Giurfa [94] discuss the principles of taste coding in the animal brain, from insects to mammals. They argue that an essential task for a neuroscience of taste is to determine the connectivity of taste-processing circuits in the central nervous system, and suggest that, beyond labelled-line or across-fibre pattern coding, taste representations are conserved across species and seem to relate to the hedonic value of the tastant (e.g.…”

Section: What the Articles Saymentioning

confidence: 99%

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Morphology and behaviour: functional links in development and evolution

Bertossa

2011

Phil. Trans. R. Soc. B

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Development and evolution of animal behaviour and morphology are frequently addressed independently, as reflected in the dichotomy of disciplines dedicated to their study distinguishing object of study (morphology versus behaviour) and perspective (ultimate versus proximate). Although traits are known to develop and evolve semi-independently, they are matched together in development and evolution to produce a unique functional phenotype. Here I highlight similarities shared by both traits, such as the decisive role played by the environment for their ontogeny. Considering the widespread developmental and functional entanglement between both traits, many cases of adaptive evolution are better understood when proximate and ultimate explanations are integrated. A field integrating these perspectives is evolutionary developmental biology (evo-devo), which studies the developmental basis of phenotypic diversity. Ultimate aspects in evo-devo studieswhich have mostly focused on morphological traits-could become more apparent when behaviour, 'the integrator of form and function', is integrated into the same framework of analysis. Integrating a trait such as behaviour at a different level in the biological hierarchy will help to better understand not only how behavioural diversity is produced, but also how levels are connected to produce functional phenotypes and how these evolve. A possible framework to accommodate and compare form and function at different levels of the biological hierarchy is outlined. At the end, some methodological issues are discussed.

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A comparative analysis of neural taste processing in animals

Cited by 26 publications

References 79 publications

Drosophila Bitter Taste(s)

Drosophila Bitter Taste(s)

Aversive gustatory learning and perception in honey bees

Morphology and behaviour: functional links in development and evolution

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