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      The tarsal taste of honey bees: behavioral and electrophysiological analyses

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          Abstract

          Taste plays a crucial role in the life of honey bees as their survival depends on the collection and intake of nectar and pollen, and other natural products. Here we studied the tarsal taste of honey bees through a series of behavioral and electrophysiological analyses. We characterized responsiveness to various sweet, salty and bitter tastants delivered to gustatory sensilla of the fore tarsi. Behavioral experiments showed that stimulation of opposite fore tarsi with sucrose and bitter substances or water yielded different outcomes depending on the stimulation sequence. When sucrose was applied first, thereby eliciting proboscis extension, no bitter substance could induce proboscis retraction, thus suggesting that the primacy of sucrose stimulation induced a central excitatory state. When bitter substances or water were applied first, sucrose stimulation could still elicit proboscis extension but to a lower level, thus suggesting central inhibition based on contradictory gustatory input on opposite tarsi. Electrophysiological experiments showed that receptor cells in the gustatory sensilla of the tarsomeres are highly sensitive to saline solutions at low concentrations. No evidence for receptors responding specifically to sucrose or to bitter substances was found in these sensilla. Receptor cells in the gustatory sensilla of the claws are highly sensitive to sucrose. Although bees do not possess dedicated bitter-taste receptors in the tarsi, indirect bitter detection is possible because bitter tastes inhibit sucrose receptor cells of the claws when mixed with sucrose solution. By combining behavioral and electrophysiological approaches, these results provide the first integrative study on tarsal taste detection in the honey bee.

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          Most cited references42

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          Molecular architecture of smell and taste in Drosophila.

          The chemical senses-smell and taste-allow animals to evaluate and distinguish valuable food resources from dangerous substances in the environment. The central mechanisms by which the brain recognizes and discriminates attractive and repulsive odorants and tastants, and makes behavioral decisions accordingly, are not well understood in any organism. Recent molecular and neuroanatomical advances in Drosophila have produced a nearly complete picture of the peripheral neuroanatomy and function of smell and taste in this insect. Neurophysiological experiments have begun to provide insight into the mechanisms by which these animals process chemosensory cues. Given the considerable anatomical and functional homology in smell and taste pathways in all higher animals, experimental approaches in Drosophila will likely provide broad insights into the problem of sensory coding. Here we provide a critical review of the recent literature in this field and comment on likely future directions.
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            A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila.

            A novel family of candidate gustatory receptors (GRs) was recently identified in searches of the Drosophila genome. We have performed in situ hybridization and transgene experiments that reveal expression of these genes in both gustatory and olfactory neurons in adult flies and larvae. This gene family is likely to encode both odorant and taste receptors. We have visualized the projections of chemosensory neurons in the larval brain and observe that neurons expressing different GRs project to discrete loci in the antennal lobe and subesophageal ganglion. These data provide insight into the diversity of chemosensory recognition and an initial view of the representation of gustatory information in the fly brain.
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              Candidate taste receptors in Drosophila.

              Little is known about the molecular mechanisms of taste perception in animals, particularly the initial events of taste signaling. A large and diverse family of seven transmembrane domain proteins was identified from the Drosophila genome database with a computer algorithm that identifies proteins on the basis of structure. Eighteen of 19 genes examined were expressed in the Drosophila labellum, a gustatory organ of the proboscis. Expression was not detected in a variety of other tissues. The genes were not expressed in the labellum of a Drosophila mutant, pox-neuro70, in which taste neurons are eliminated. Tissue specificity of expression of these genes, along with their structural similarity, supports the possibility that the family encodes a large and divergent family of taste receptors.
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                Author and article information

                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                04 February 2014
                2014
                : 8
                : 25
                Affiliations
                [1] 1Centre National de la Recherche Scientifique (CNRS), Research Center on Animal Cognition (UMR5169) Toulouse, France
                [2] 2University Paul-Sabatier, Research Center on Animal Cognition (UMR5169) Toulouse, France
                [3] 3College of Animal Sciences, Zhejiang University Hangzhou, China
                [4] 4Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences Kunming, China
                Author notes

                Edited by: Carmen Sandi, Ecole Polytechnique Federale De Lausanne, Switzerland

                Reviewed by: Judith Reinhard, University of Queensland, Australia; Fernando J. Guerrieri, Univesité François Rabelais Tours, France

                *Correspondence: Maria Gabriela de Brito Sanchez, Centre de Recherches sur la Cognition Animale, Building 4R3, Université de Toulouse, 31062 Toulouse Cedex 9, France e-mail: maria.de-brito-sanchez@ 123456univ-tlse3.fr

                This article was submitted to the journal Frontiers in Behavioral Neuroscience.

                Article
                10.3389/fnbeh.2014.00025
                3913880
                24550801
                9ea968cd-1997-4051-88b7-798953d3d782
                Copyright © 2014 de Brito Sanchez, Lorenzo, Su, Liu, Zhan and Giurfa.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 December 2013
                : 16 January 2014
                Page count
                Figures: 9, Tables: 0, Equations: 0, References: 61, Pages: 16, Words: 12651
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                gustation,electrophysiology,gustatory receptors,taste,honey bee,tarsi,insect,proboscis extension reflex

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