Presynaptic Peptidergic Modulation of Olfactory Receptor Neurons in Drosophila

The role of classical neurotransmitters in the transfer and processing of olfactory information is well established in many organisms. Neuropeptide action, however, is largely unexplored in any peripheral olfactory system. A subpopulation of local interneurons (LNs) in the Drosophila antannal lobe i...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 106; no. 31; pp. 13070 - 13075
Main Authors Ignell, Rickard, Root, Cory M., Birse, Ryan T., Wang, Jing W., Nässel, Dick R., Winther, Åsa M. E., Dickson, Barry
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 04.08.2009
National Acad Sciences
Subjects
Animals
Antennal lobe
Biologi
Biological Sciences
Biology
Brain
Calcium
Cell and molecular biology
Cell- och molekylärbiologi
Drosophila
Drosophila - physiology
Drosophila Proteins - analysis
Drosophila Proteins - physiology
Gene expression
Insect antennae
Insects
Microbiology
Mikrobiologi
Modulated signal processing
NATURAL SCIENCES
NATURVETENSKAP
Neural Inhibition
Neurobiologi
Neurobiology
Neurochemistry and Molecular Neurobiology
neurokemi med molekylär neurobiologi
Neurons
Neuropeptides
Neurotransmitters
Odorants
Odors
olfactory behavior
Olfactory Receptor Neurons - physiology
Peptides
presynaptic inhibition
Protein Precursors - analysis
Protein Precursors - physiology
Receptors
Receptors, Neurotransmitter - analysis
Receptors, Neurotransmitter - physiology
Signal Transduction
T cell receptors
tachykinin
Tachykinins - analysis
Tachykinins - physiology
two-photon imaging
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Summary:The role of classical neurotransmitters in the transfer and processing of olfactory information is well established in many organisms. Neuropeptide action, however, is largely unexplored in any peripheral olfactory system. A subpopulation of local interneurons (LNs) in the Drosophila antannal lobe is peptidergic, expressing Drosophila tachykinins (DTKs). We show here that olfactory receptor neurons (ORNs) express the DTK receptor (DTKR). Using twophoton microscopy, we found that DTK applied to the antennal lobe suppresses presynaptic calcium and synaptic transmission in the ORNs. Furthermore, reduction of DTKR expression in ORNs by targeted RNA interference eliminates presynaptic suppression and alters olfactory behaviors. We detect opposite behavioral phenotypes after reduction and over expression of DTKR in ORNs. Our findings suggest a presynaptic inhibitory feedback to ORNs from peptidergic LNs in the antennal lobe.
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Author contributions: R.I., C.M.R., J.W.W., D.R.N., and Å.M.E.W. designed research; R.I., C.M.R., R.T.B., and Å.M.E.W. performed research; R.T.B. contributed new reagents/analytic tools; R.I., C.M.R., J.W.W., D.R.N., and Å.M.E.W. analyzed data; and R.I., C.M.R., J.W.W., D.R.N., and Å.M.E.W. wrote the paper.
2Present address: The Burnham Institute for Medical Research, Cancer Research Center, La Jolla, CA 92037.
Edited by Barry Dickson, Research Institute of Molecular Pathology, Austria, and accepted by the Editorial Board June 24, 2009
1R.I. and C.M.R. contributed equally to this work.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.0813004106