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Perception of sniff phase in mouse olfaction

Abstract

Olfactory systems encode odours by which neurons respond and by when they respond1,2,3. In mammals, every sniff evokes a precise, odour-specific sequence of activity across olfactory neurons4,5,6. Likewise, in a variety of neural systems, ranging from sensory periphery7,8 to cognitive centres9, neuronal activity is timed relative to sampling behaviour and/or internally generated oscillations. As in these neural systems, relative timing of activity may represent information in the olfactory system10,11. However, there is no evidence that mammalian olfactory systems read such cues12,13. To test whether mice perceive the timing of olfactory activation relative to the sniff cycle (‘sniff phase’), we used optogenetics in gene-targeted mice to generate spatially constant, temporally controllable olfactory input. Here we show that mice can behaviourally report the sniff phase of optogenetically driven activation of olfactory sensory neurons. Furthermore, mice can discriminate between light-evoked inputs that are shifted in the sniff cycle by as little as 10 milliseconds, which is similar to the temporal precision of olfactory bulb odour responses14,15. Electrophysiological recordings in the olfactory bulb of awake mice show that individual cells encode the timing of photoactivation in relation to the sniff in both the timing and the amplitude of their responses. Our work provides evidence that the mammalian olfactory system can read temporal patterns, and suggests that timing of activity relative to sampling behaviour is a potent cue that may enable accurate olfactory percepts to form quickly11,16.

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Figure 1: Stimulating olfaction with light.
Figure 2: OMP–ChR2 mice perceive sniff phase.
Figure 3: Response of mitral/tufted cells to light stimulation.

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Acknowledgements

We thank L. Doglio and the Transgenic and Targeted Mutagenesis Laboratory at Northwestern University for generation of chimaeric mice, B. Weiland for technical help with cloning and gene targeting, D. Huber, D. O'Connor and T. Komiyama for advice on mouse behaviour, D. Wesson and M. Wachowiak for instruction on sniff measurement, J. Nunez-Iglesias for assistance with statistics, G. Shtengel for advice on laser set-up, and T. Tabachnik and H. Davidowitz for help designing the behavioural rig. J. Osborne fabricated the microdrive. G. Lott provided digital acquisition software. A. Koulakov contributed to spike-sorting and classification algorithms. We thank W. Denk, K. Svoboda, R. Gütig, R. Egnor, M. Orger and A. Resulaj for comments on the manuscript. This work was supported by the Visiting Scientist Program at JFRC. T.B. was supported by NIDCD (R01DC009640, R21DC010911), the Whitehall Foundation and the Brain Research Foundation.

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M.S. and D.R. designed the study and build the experimental set-up, M.S. performed the experiments and analysed the behavioural data. R.S. and M.S. performed the electrophysiological recordings, R.S. and D.R. analysed the electrophysiological data, and T.B. initiated the transgenic approach and generated the gene-targeted mice. R.O. developed the laser optics and optical fibre design. 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.

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Smear, M., Shusterman, R., O’Connor, R. et al. Perception of sniff phase in mouse olfaction. Nature 479, 397–400 (2011). https://doi.org/10.1038/nature10521

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