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Two Interacting Olfactory Transduction Mechanisms Have Linked Polarities and Dynamics in Drosophila melanogaster Antennal Basiconic Sensilla Neurons

Department of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, Canada

Submitted 24 February 2009; accepted in final form 14 April 2009

We measured frequency response functions between concentrations of fruit odorants and individual action potentials in large basiconic sensilla of the Drosophila melanogaster antenna. A new method of randomly varying odorant concentration was combined with rapid, continuous measurement of concentration at the antenna by a miniature photoionization detector. All frequency responses decreased progressively at frequencies approaching 100 Hz, providing an upper limit for the dynamics of Drosophila olfaction. We found two distinct response patterns: excitatory band-pass frequency responses were seen with ethyl acetate, ethyl butyrate, and hexanol, whereas inhibitory low-pass responses were seen with methyl salicylate and phenylethyl acetate. Band-pass responses peaked at 1–10 Hz. Frequency responses could be well fitted by simple linear filter equations, and the fitted parameters were consistent within each of the two types of responses. Experiments with equal mixtures of excitatory and inhibitory odorants gave responses that were characteristic of the inhibitory components, indicating that interaction during transduction causes inhibitory odorants to suppress the responses to excitatory odorants. Plots of response amplitude versus odorant concentration indicated that the odorant concentrations used were within approximately linear regions of the dose response relationships. We also estimated linear information capacity from the coherence function of each recording. Although coherence was relatively high, indicating a large signal-to-noise ratio, information capacity for olfaction was much lower than comparable estimates for mechanotransduction or visual transduction because of the limited bandwidth of olfaction. These data offer new insights into transduction by primary chemoreceptors and place temporal constraints on Drosophila olfactory behavior.