Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficult...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 7; pp. E902 - E911
Main Authors Cao, Li-Hui, Jing, Bi-Yang, Yang, Dong, Zeng, Xiankun, Shen, Ying, Tu, Yuhai, Luo, Dong-Gen
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 16.02.2016
National Acad Sciences
SeriesPNAS Plus
Subjects
Adaptation, Physiological
Animals
Biological Sciences
Calcium - metabolism
Chemosensory perception
Drosophila
Drosophila melanogaster - physiology
Insects
Neurons
Odorants
Odors
Olfactory Receptor Neurons - physiology
Patch-Clamp Techniques
PNAS Plus
Sensory Receptor Cells - metabolism
Signal Transduction
olfaction
sensory adaptation
OSN
Drosophila
chemoreceptor
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Summary:In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficulty of obtaining intracellular recordings from Drosophila OSNs. Here, we developed an antennal preparation that enabled the first recordings (to our knowledge) from targeted Drosophila OSNs through a patch-clamp technique. We found that brief odor pulses triggered graded inward receptor currents with distinct response kinetics and current–voltage relationships between Or- and Ir-driven responses. When stimulated with long-step odors, the receptor current of Ir-expressing OSNs did not adapt. In contrast, Or-expressing OSNs showed a strong Ca2+-dependent adaptation. The adaptation-induced changes in odor sensitivity obeyed the Weber–Fechner relation; however, surprisingly, the incremental sensitivity was reduced at low odor backgrounds but increased at high odor backgrounds. Our model for odor adaptation revealed two opposing effects of adaptation, desensitization and prevention of saturation, in dynamically adjusting odor sensitivity and extending the sensory operating range.
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Edited by Richard W. Aldrich, The University of Texas at Austin, Austin, TX, and approved December 24, 2015 (received for review September 15, 2015)
Author contributions: L.-H.C. and D.-G.L. designed research; L.-H.C., Y.T., and D.-G.L. developed the adaptation model; L.-H.C., B.-Y.J., D.Y., X.Z., and D.-G.L. performed research; L.-H.C., B.-Y.J., D.Y., Y.S., and D.-G.L. analyzed data; and L.-H.C., Y.T., and D.-G.L. wrote the paper.
1B.-Y.J., D.Y., and X.Z. contributed equally to this work.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.1518329113