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Olfactory cortical neurons read out a relative time code in the olfactory bulb

Nature Neuroscience volume 16, pages 949–957 (2013)Cite this article

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Abstract

Odor stimulation evokes complex spatiotemporal activity in the olfactory bulb, suggesting that both the identity of activated neurons and the timing of their activity convey information about odors. However, whether and how downstream neurons decipher these temporal patterns remains unknown. We addressed this question by measuring the spiking activity of downstream neurons while optogenetically stimulating two foci in the olfactory bulb with varying relative timing in mice. We found that the overall spike rates of piriform cortex neurons (PCNs) were sensitive to the relative timing of activation. Posterior PCNs showed higher sensitivity to relative input times than neurons in the anterior piriform cortex. In contrast, olfactory bulb neurons rarely showed such sensitivity. Thus, the brain can transform a relative time code in the periphery into a firing rate–based representation in central brain areas, providing evidence for the relevance of a relative time–based code in the olfactory bulb.

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Figure 1: Characterization of responses to single spot optogenetic activation of olfactory nerve input.
Figure 2: Acquisition of TTCs for olfactory bulb and PCNs.
Figure 3: Piriform cortex neurons show higher sensitivity to the lag of olfactory bulb stimulation.
Figure 4: Order–specific responses of PCNs.
Figure 5: Delayed inhibition shapes the responsiveness of PCNs.
Figure 6: Rate code conveys relative timing information progressively more at the central areas.
Figure 7: Order selectivity is largely preserved across different respiration phases.
Figure 8: Direct activation of mitral and tufted cells produced consistent results.

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Acknowledgements

We thank C. Dulac (Harvard University) for sharing resources generously, comments on the manuscript and providing Tbet-cre; ChR2loxP/loxP mice (generated by A.L.). We thank E. Soucy and T. Sato for technical support and D.F. Albeanu and A.K. Dhawale for technical advice. We thank Y. Ben-Shaul, C. Poo, N. Eshel and J.Y. Cohen for their comments on the manuscript. This work was supported by Human Frontier Science Program (R.H.), a Howard Hughes Medical Institute Collaborative Innovation Award, a Smith Family New Investigator Award, the Alfred Sloan Foundation and the Milton Fund (N.U.), and a grant from the US National Institutes of Health (V.N.M.).

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Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts, USA

    Rafi Haddad, Anne Lanjuin, Venkatesh N Murthy & Naoshige Uchida

  2. Allen Institute for Brain Science, Seattle, Washington, USA

    Linda Madisen & Hongkui Zeng

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  1. Rafi Haddad
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Contributions

R.H. and N.U. conceived the experiment. R.H. performed the experiment. A.L. generated and characterized the Tbet-cre; ChR2loxP/loxP mice, and L.M. and H.Z. generated and characterized the ChR2loxP/loxP mice. V.N.M. provided the Omp-ChR2 mice. R.H. and N.U. wrote the paper and A.L., V.N.M. and H.Z. provided feedback on the manuscript.

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Correspondence to Naoshige Uchida.

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Haddad, R., Lanjuin, A., Madisen, L. et al. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat Neurosci 16, 949–957 (2013). https://doi.org/10.1038/nn.3407

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