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Biophysical mechanisms underlying olfactory receptor neuron dynamics

Nature Neuroscience volume 14, pages 208–216 (2011)Cite this article

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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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Figure 1: Temporal patterns of ORN spiking are cell and odor dependent.
Figure 2: Field potentials and spikes can be isolated from single ORNs.
Figure 3: Filter models describe transformations between stimulus, LFP and spikes.
Figure 4: Odor and cell dependence of transduction and spiking dynamics.
Figure 5: Knocking down DmNav makes the LFP-to-spiking transformation more differentiating.
Figure 6: Dynamics of transduction and adaptation.
Figure 7: Cross-adaptation between co-expressed odorant receptors.
Figure 8: Encoding the dynamics of natural odor plumes.

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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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Authors and Affiliations

  1. Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, USA

    Katherine I Nagel & Rachel I Wilson

  2. Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts, USA

    Rachel I Wilson

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  1. Katherine I Nagel
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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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Correspondence to Rachel I Wilson.

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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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