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Bilateral olfactory sensory input enhances chemotaxis behavior

Abstract

Neural comparisons of bilateral sensory inputs are essential for visual depth perception and accurate localization of sounds in space. All animals, from single-cell prokaryotes to humans, orient themselves in response to environmental chemical stimuli, but the contribution of spatial integration of neural activity in olfaction remains unclear. We investigated this problem in Drosophila melanogaster larvae. Using high-resolution behavioral analysis, we studied the chemotaxis behavior of larvae with a single functional olfactory neuron on either the left or right side of the head, allowing us to examine unilateral or bilateral olfactory input. We developed new spectroscopic methods to create stable odorant gradients in which odor concentrations were experimentally measured. In these controlled environments, we observed that a single functional neuron provided sufficient information to permit larval chemotaxis. We found additional evidence that the overall accuracy of navigation is enhanced by the increase in the signal-to-noise ratio conferred by bilateral sensory input.

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Figure 1: FT-IR spectroscopy used to measure odorant gradients in single and multiple source odor devices.
Figure 2: Larvae show robust chemotaxis behavior in single and multiple–odor-source devices.
Figure 3: The spectroscopic method for measuring odorant gradients can be generalized to other odors.
Figure 4: Local heading and turning bias analysis suggests that Drosophila larvae are able to detect the direction of local odorant gradients.
Figure 5: Chemotaxis mediated by a single functional Or42a olfactory neuron.
Figure 6: Chemotaxis mediated by a single functional Or1a olfactory neuron.
Figure 7: Sensitivity of animals with unilateral or bilateral olfactory function.
Figure 8: Bilateral sensory input enhances olfactory navigation.

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Acknowledgements

We thank K. Fishilevich, C. Ilch, S. Piccinotti, P. Rivkin, L. Salas and S. Vasquez for expert technical assistance, M. Cobb for providing the image in Figure 5a, and the Rockefeller University Chemical Biology Spectroscopy Research Center for access to instrumentation. This work benefited from helpful discussions with S. Benhamou, V. Jayaraman, L.C. Katz, J.D. Levine, M. Magnasco, M. Meister and D. Wolpert. We are grateful to S. Benhamou, W. Bialek, N. Buchler, M. Geffen, A.J. Hudspeth, S. Shaham and the Vosshall lab for their comments on the manuscript. This work was supported by grants from the US National Institutes of Health to L.B.V., the Ellison Medical Foundation to T.P.S., the Helen Hay Whitney Foundation to R.B., and the Belgian-American Educational Foundation and the Revson Foundation to M.L.

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Authors and Affiliations

Authors

Contributions

M.L. and T.H. devised and implemented the spectroscopic approach. R.B. conceived the design of the Or83b FLP-out construct, which was constructed together with M.L. T.P.S. provided input into the spectroscopy and supervised T.H. T.H. contributed to the conceptualization of the multiple–odor-source device, which was implemented by M.L. M.L. conceived of the project and carried out all the experiments in the paper. L.B.V. provided guidance and wrote the paper together with M.L.

Corresponding author

Correspondence to Leslie B Vosshall.

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Supplementary Figures 1–17, Table 1 and Methods (PDF 1566 kb)

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Louis, M., Huber, T., Benton, R. et al. Bilateral olfactory sensory input enhances chemotaxis behavior. Nat Neurosci 11, 187–199 (2008). https://doi.org/10.1038/nn2031

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