Non-redundant coding of aversive odours in the main olfactory pathway

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Abstract

Many species are critically dependent on olfaction for survival. In the main olfactory system of mammals, odours are detected by sensory neurons that express a large repertoire of canonical odorant receptors and a much smaller repertoire of trace amine-associated receptors (TAARs)1,2,3,4. Odours are encoded in a combinatorial fashion across glomeruli in the main olfactory bulb, with each glomerulus corresponding to a specific receptor5,6,7. The degree to which individual receptor genes contribute to odour perception is unclear. Here we show that genetic deletion of the olfactory Taar gene family, or even a single Taar gene (Taar4), eliminates the aversion that mice display to low concentrations of volatile amines and to the odour of predator urine. Our findings identify a role for the TAARs in olfaction, namely, in the high-sensitivity detection of innately aversive odours. In addition, our data reveal that aversive amines are represented in a non-redundant fashion, and that individual main olfactory receptor genes can contribute substantially to odour perception.

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Figure 1: Deleting the olfactory TAARs abolishes high-sensitivity amine and predator odour responses in the dorsal olfactory bulb.
Figure 2: Deletion of all olfactory Taar genes abolishes aversion to low concentrations of structurally diverse amines and predator urine.
Figure 3: Deletion of a single Taar gene abolishes aversion to a specific amine and to natural predator odours.

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Acknowledgements

We thank T. Schmidt, C. Waldron, L. Tunmer, V. Dewan and the staff of the Philadelphia Zoo for collecting predator urine and for providing images of the animals. We thank D. Ferster for help with video tracking, D. Cawley, A. Ge and T. Alconada for help analysing behavioural data, the Northwestern University Center for Comparative Medicine for behavioural space, and the Northwestern University Biostatistics Collaboration Center for advice on statistical analyses. T.B. was a participant in the Visiting Scientist Program at HHMI Janelia Farm Research Campus. This work was supported by grants from the NIH/NIDCD (R01DC009640 to T.B. and F32DC012004 to A.D.), The Whitehall Foundation and The Brain Research Foundation (T.B.).

Author information

A.D., D.R. and T.B. planned the experiments. A.D. and R.Z. performed the behavioural analyses. R.P. and T.B. generated the mouse strains and performed in vivo imaging experiments. A.D., R.P., D.R. and T.B. analysed the data. A.D., R.P. and T.B. wrote the manuscript.

Correspondence to Thomas Bozza.

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The authors declare no competing financial interests.

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Dewan, A., Pacifico, R., Zhan, R. et al. Non-redundant coding of aversive odours in the main olfactory pathway. Nature 497, 486–489 (2013). https://doi.org/10.1038/nature12114

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