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Multiple perceptible signals from a single olfactory glomerulus

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Abstract

Glomeruli are functional units in the olfactory system. The mouse olfactory bulb contains roughly 2,000 glomeruli, each receiving inputs from olfactory sensory neurons (OSNs) that express a specific odorant receptor gene. Odors typically activate many glomeruli in complex combinatorial patterns and it is unknown which features of neuronal activity in individual glomeruli contribute to odor perception. To address this, we used optogenetics to selectively activate single, genetically identified glomeruli in behaving mice. We found that mice could perceive the stimulation of a single glomerulus. Single-glomerulus stimulation was also detected on an intense odor background. In addition, different input intensities and the timing of input relative to sniffing were discriminated through one glomerulus. Our data suggest that each glomerulus can transmit odor information using identity, intensity and temporal coding cues. These multiple modes of information transmission may enable the olfactory system to efficiently identify and localize odor sources.

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Figure 1: Stimulating single olfactory glomeruli with light.
Figure 2: Detecting monoglomerular activation paired with odor.
Figure 3: Discrimination of monoglomerular amplitude and timing differences.

Change history

  • 30 September 2013

    In the version of this article initially published online, ref. 37 and the sentence "In addition, flies can learn to discriminate odors using only a single class of olfactory sensory neuron37" in the second paragraph of the Discussion were not present, and the following sentence, concerning the mammalian olfactory system, referred to "learned behavior" rather than simply "behavior." The error has been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank C. Guo and the gene targeting facility at Janelia Farm for generation of chimeric mice, B. Weiland for technical help with cloning and gene targeting, M. Karlsson for designing the behavioral controller box, and K. Svoboda, G. Fishell, R. Egnor and Y. Sirotin for comments on the manuscript. This work was supported by the Visiting Scientist Program at the Janelia Farm Research Center. T.B. was supported by funding from the National Institute on Deafness and Other Communication Disorders (R01DC009640 and R21DC010911), the Whitehall Foundation and the Brain Research Foundation.

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Authors and Affiliations

Authors

Contributions

M.S., T.B. and D.R. designed the study. M.S. and D.R. built the experimental setup. A.R. developed software for behavioral experiments. M.S. and A.R. performed the experiments. M.S., A.R. and D.R. analyzed the behavioral data. J.Z. and T.B. performed the electrophysiological recordings. J.Z. and T.B. analyzed the electrophysiological data. T.B. initiated the transgenic approach and generated the gene-targeted mice. M.S., T.B. and D.R. wrote the manuscript. D.R. and T.B. supervised the project.

Corresponding authors

Correspondence to Thomas Bozza or Dmitry Rinberg.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 High-power monoglomerular activation can be detected in the presence of M72 ligand.

High-power monoglomerular activation can be detected in the presence of M72 ligand. Detection performance for low (20 mW; data as in Fig. 2C) and high (40 mW) stimulus power in the absence and presence of methyl benzoate (10-3 of saturated vapor pressure), an M72 ligand, is shown. Increasing light stimulus power evokes above-chance detection performance.

Supplementary information

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Supplementary Figure 1 and Supplementary Table 1 (PDF 281 kb)

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Smear, M., Resulaj, A., Zhang, J. et al. Multiple perceptible signals from a single olfactory glomerulus. Nat Neurosci 16, 1687–1691 (2013). https://doi.org/10.1038/nn.3519

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