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Precise olfactory responses tile the sniff cycle

Abstract

In terrestrial vertebrates, sniffing controls odorant access to receptors, and therefore sets the timescale of olfactory stimuli. We found that odorants evoked precisely sniff-locked activity in mitral/tufted cells in the olfactory bulb of awake mouse. The trial-to-trial response jitter averaged 12 ms, a precision comparable to other sensory systems. Individual cells expressed odor-specific temporal patterns of activity and, across the population, onset times tiled the duration of the sniff cycle. Responses were more tightly time-locked to the sniff phase than to the time after inhalation onset. The spikes of single neurons carried sufficient information to discriminate odors. In addition, precise locking to sniff phase may facilitate ensemble coding by making synchrony relationships across neurons robust to variation in sniff rate. The temporal specificity of mitral/tufted cell output provides a potentially rich source of information for downstream olfactory areas.

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Figure 1: Odor response analysis: sniff-alignment and warping.
Figure 2: Diversity of odor responses.
Figure 3: Excitatory and inhibitory odor responses tile the sniff cycle.
Figure 4: Sharp events of firing rate increase.
Figure 5: Mitral cell response precision in warped-time and real-time coordinates.
Figure 6: Discrimination performance of individual neurons.
Figure 7: Discrimination among five odors by mitral/tufted cell populations.

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Acknowledgements

We thank J. Osborne and T. Tabachnik for design and fabrication of experimental equipment, S. Royer for help with electrophysiological setup, J. Nunez-Iglesias for help with statistical analysis, P. Ahammad, D.B. Chklovskii and S. Druckmann for discussions and A. Resulaj, J.T. Dudman, V. Jayaraman, E. Pastalkova and K. Svoboda for comments on the manuscript. R.S., M.C.S. and D.R. are supported by the Howard Hughes Medical Institute. A.A.K. was supported by US National Institutes of Health grant R01 EY018068.

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R.S. and D.R. conceived and designed the experiments. R.S., M.C.S. and D.R. performed experiments. R.S., A.A.K. and D.R. analyzed the data. R.S., M.C.S., A.A.K. and D.R. wrote the manuscript.

Corresponding author

Correspondence to Dmitry Rinberg.

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The authors declare no competing financial interests.

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Supplementary Figures 1–3, Supplementary Tables 1 and 2, and Supplementary Note (PDF 3868 kb)

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Shusterman, R., Smear, M., Koulakov, A. et al. Precise olfactory responses tile the sniff cycle. Nat Neurosci 14, 1039–1044 (2011). https://doi.org/10.1038/nn.2877

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