Abstract
The responses of olfactory receptor neurons (ORNs) to odors have complex dynamics. Using genetics and pharmacology, we found that these dynamics in Drosophila ORNs could be separated into sequential steps, corresponding to transduction and spike generation. Each of these steps contributed distinct dynamics. Transduction dynamics could be largely explained by a simple kinetic model of ligand-receptor interactions, together with an adaptive feedback mechanism that slows transduction onset. Spiking dynamics were well described by a differentiating linear filter that was stereotyped across odors and cells. Genetic knock-down of sodium channels reshaped this filter, implying that it arises from the regulated balance of intrinsic conductances in ORNs. Complex responses can be understood as a consequence of how the stereotyped spike filter interacts with odor- and receptor-specific transduction dynamics. However, in the presence of rapidly fluctuating natural stimuli, spiking simply increases the speed and sensitivity of encoding.
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Acknowledgements
We thank J.R. Carlson for Or33c-Gal4, Or46a-Gal4, UAS-Or47a and UAS-Or47b, B.J. Dickson for Or59c-Gal4 and Or42a-Gal4, L. Luo for pebbled-Gal, L. Stevens for UAS-DTl, J.S. Bell, J.B. Cohen, A.L. Fairhall, M. Wachowiak and G. Yellen for conversations, and A.W. Liu, M. Meister, D. Schoppik and members of the Wilson laboratory for feedback on the manuscript. This work was funded by a Helen Hay Whitney Foundation Fellowship (to K.I.N.), a grant from the US National Institutes of Health (R01DC008174), a McKnight Scholar Award and a Beckman Young Investigator Award (to R.I.W.), and a Howard Hughes Medical Institute Early Career Scientist award (to R.I.W.).
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K.I.N. performed the experiments and analyzed the data. K.I.N. and R.I.W. designed the experiments and wrote the paper.
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Nagel, K., Wilson, R. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat Neurosci 14, 208–216 (2011). https://doi.org/10.1038/nn.2725
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DOI: https://doi.org/10.1038/nn.2725
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