Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Feeding Behavior Regulation in the Fly: Effect of a Noxious Substance through the Taste and Olfactory Neurons
Department of Applied Biology, Faculty of Textile Science, Kyoto Institute of Technology, Sakyo-ku, Kyoto 606-8585, Japan
Correspondence to be sent to: Mamiko Ozaki, e-mail: mamiko{at}ipc.kit.ac.jp
Key words: appetite, deterrent cell, fly, odorant-binding protein, olfaction, taste
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Introduction |
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 Top Introduction Gustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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The contact chemosensilla on the labellum of the fly are in the form of a hair housing five sensory neurons, i.e. four contact chemoreceptor cells and one mechanoreceptor neuron (Ozaki and Tominaga, 1999
).
Three of the four chemoreceptor cells are the sugar, salt and water receptor cells,
respectively. The remaining chemoreceptor cell, traditionally called the ‘fifth
cell’, has recently been proposed to function as a deterrent cell (Liscia and Solari, 2000;
Ozaki et al., 2003). Thus,
the balance of response between the sugar receptor cell and the deterrent cell could
determine feeding behavior of the fly.
Previously,
Ozaki et al. (1995) found an
odorant-binding protein (chemical sense-related lipophilic ligand-binding protein, CRLBP)
common to the taste and olfactory sensilla of the blowfly, Phormia regina. This
acidic, small molecular protein binds lipophilic noxious compounds like
D-limonene, and since aversive behavior is triggered when the fly touches such
a noxious compound, this sensory cell may be related to aversive behavior via CRLBP.
On the other hand, during food searching by flies, a noxious compound such as
D-limonene, which has strong oral toxicity (Ozaki et al., 2003), should carefully be avoided.
Phormia regina is not counted as a phytophagous insect but the adult flies are
nectar feeders. Hence they could encounter monoterpenes, which are abundantly present in
citrus rinds, by chance. The flies may exhibit more effective aversive behavior toward
the D-limonene when both the taste and the olfactory receptors are stimulated
spontaneously. Thus, the olfactory inputs from the antennae and/or the maxillary palps
may be expected to influence the feeding or the aversive behavior in the flies.
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Gustatory cue of D-limonene induces aversive reaction |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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To evaluate the oral toxicity of monoterpenes, we measured the electrophysiological response to them. Of all the monoterpenes examined, D-limonene exhibited the strongest oral toxicity (Ozaki et al., 2003
). When the flies were forced to ingest 0.3 µl of
D-limonene, L-limonene, cineol, citral or ß-myrcene, 87, 40,
30, 0 or 0% of number of flies were killed within 30 min, respectively. Contact of
a chemosensillum with D-limonene induced the severest aversive behavior with
vomiting and/or excretion in the fly. D-Limonene, when dispersed in an aqueous
solution including CRLBP, evoked impulses from the ‘fifth cell’. Considering
the relationship between the aversive effects of D-limonene and the response
of the ‘fifth cell’ to D-limonene, we suggested that in the insect
contact-chemosensillum, the CRLBP carries lipophilic members of the noxious taste
substances to the ‘fifth cell’ through the aqueous sensillum lymph, and that
the ‘fifth cell’ is indispensable receptor neuron for the toxin detection
system in the fly. Thus, our work on P. regina is the first electrophysiological
study of the role of an odorant-binding protein in an insect taste system. |
Olfactory stimulation with D-limonene decreases the fly’s appetite |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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The relationship between the feeding response and sugar concentration was investigated using the proboscis extension reflex (PER) test, and the feeding sensitivity of a group of flies was indicated as a mean value of the feeding threshold concentration of sucrose. The mean value of the feeding threshold was taken as an indicator of appetite and was determined by half of the maximum concentration of the PER–concentration curve. When the flies increased their appetite, the mean value of the feeding threshold decreased, and vice versa. We carried out the PER test at various concentrations of sucrose in the absence or presence of D-limonene odor. In the presence of D-limonene, the mean value of the feeding threshold increased threefold. The appetite reducing effect was also observed after the dietary experience with the D-limonene odor. The flies, which were fed on sucrose in the presence of D-limonene for 5 days after eclosion, exhibited obvious appetite reduction to sucrose even in the absence of this compound. Thus, dietary experience with the odor of a toxic substance suppresses the feeding motivation in the flies, reducing the probability of ingesting toxic substances.
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Effect of mushroom body ablation |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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Considering the experiential effect of the diet in the presence of D-limonene, one may expect that the mushroom body, a neural structure involved in learning in the insect brain, may contribute to the effect. We succeeded in ablating the mushroom body of P. regina by hydroxy urea treatment of the larvae (de Belle and Heisenberg, 1994
). When
we carried out the same PER test in the mushroom body-ablated flies, they showed appetite
reduction in the presence of D-limonene both before and after the dietary
experience with that odor. Thus, the fly can integrate olfactory information about
D-limonene with the taste information about sucrose without the mushroom body.
However, the mushroom body-ablated fly showed normal appetite to sucrose even after the
dietary experience with the odor of D-limonene. This suggested that the
mushroom body-ablated fly could not learn or remember the dietary experience, through
which aversive conditioning between the taste of sucrose and the odor of
D-limonene should occur. |
Effect of antennae or maxillary palps |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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We also carried out the same PER tests with the flies whose antennae or maxillary palps were removed. Removal of antennae influenced the memory of dietary experience with the odor of D-limonene, but removal of maxillary palps did not. Thus, the neural routes from the maxillary palps may not be involved in formation of associative memory between the taste of sucrose and the noxious odor of D-limonene.
Fluorescence labeling of maxillary afferents revealed a distinct fiber bundles that projected into the subesophageal ganglion (SOG) and ascended further into the glomeruli in the ipsilateral and contralateral antennal lobes. The antennal afferents innervated into all the remaining glomeruli in the ipsilateral and contralateral antennal lobes, and some fiber bundles projected into SOG. Thus, the projection patterns from the antennae and the maxillary palps may not overlap, suggesting that olfactory inputs from the antennae are processed independently of those from the maxillary palps.
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Conclusion |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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The blowfly, P. regina, has taste sensilla with four contact-chemoreceptor cells. The sugar receptor cell activity induces feeding response of the fly. We measured the electrophysiological response of the ‘fifth cell’ to monoterpenes having oral toxicity for the flies. D-limonene, which exhibited the strongest oral toxicity of all the monoterpenes examined, evoked impulses of the ‘fifth cell’ with the help of an odorant-binding protein in the taste sensillum, and induced strong aversive behavior (vomiting or excretion). The ‘fifth cell’ may be a warning cell that functions as a taste system for detecting and avoiding dangerous foods.
Moreover, the odor of D-limonene inhibited the feeding behavior, which was induced by excitation of the sugar receptor cell. The dietary experience with the odor caused appetite reduction lasting for a month or longer (The life time of Phormia is up to 2 months). Thus, one substance, D-limonene, when detected as a taste and an odor through two different modalities of chemical senses, respectively, strongly deterred the flies from feeding.
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Acknowledgements |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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This study was supported by grants from the ProBRAIN and National Institute of Agrobiological Sciences to M.O.
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References |
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TopIntroductionGustatory cue of d-limonene...Olfactory stimulation with d...Effect of mushroom body...Effect of antennae or...ConclusionAcknowledgementsReferences |
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de Belle, J.S. and Heisenberg, M. (1994) Associative odor learning in Drosophila abolishes by chemical ablation of mushroom bodies. Science, 263, 692–695.
Liscia, A. and Solari, P. (2000) Bitter taste recognition in the blowfly: electrophysiological and behavioral evidence. Physiol. Behav., 70, 61–65.[CrossRef][Medline]
Ozaki, M., Morisaki, K., Idei, W., Ozaki, K. and Tokunaga, F. (1995) A putative lipophilic stimulant carrier protein commonly found in the taste and the olfactory systems. A unique member of the pheromone-binding protein superfamily. Eur. J. Biochem., 230, 298–308.[Web of Science][Medline]
Ozaki, M., Takahara, T., Kawahara, Y., Wada, A., Seno, K., Amakawa, T., Yamaoka, R. and Nakamura, T. (2003) Perception of noxious compounds by contact chemoreceptor of the blowfly, Phormia regina: putative role of an odorant-binding protein. Chem. Senses, 28, 349–359.
Ozaki, M. and Tominaga, Y. (1999) Chemoreceptors. In Eguchi, E. and Tominaga, Y. (eds), Atlas of Arthropod Sensory Receptors. Springer-Verlag, Tokyo, pp. 143–154.
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