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Sniffing controls an adaptive filter of sensory input to the olfactory bulb

Nature Neuroscience volume 10, pages 631–639 (2007)Cite this article

Abstract

Most sensory stimuli are actively sampled, yet the role of sampling behavior in shaping sensory codes is poorly understood. Mammals sample odors by sniffing, a complex behavior that controls odorant access to receptor neurons. Whether sniffing shapes the neural code for odors remains unclear. We addressed this question by imaging receptor input to the olfactory bulb of awake rats performing odor discriminations that elicited different sniffing behaviors. High-frequency sniffing of an odorant attenuated inputs encoding that odorant, whereas lower sniff frequencies caused little attenuation. Odorants encountered later in a sniff bout were encoded as the combination of that odorant and the background odorant during low-frequency sniffing, but were encoded as the difference between the two odorants during high-frequency sniffing. Thus, sniffing controls an adaptive filter for detecting changes in the odor landscape. These data suggest an unexpected functional role for sniffing and show that sensory codes can be transformed by sampling behavior alone.

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Figure 1: Sniffing behavior during head-fixed odor discriminations.
Figure 2: Receptor input to the olfactory bulb imaged in the awake behaving rat.
Figure 3: Effect of sniff frequency on receptor input to the olfactory bulb.
Figure 4: Minor effect at the onset of high-frequency sniffing on odorant response maps.
Figure 5: High-frequency sniffing attenuates ORN inputs to the olfactory bulb.
Figure 6: Frequency-dependent attenuation of ORN inputs results from low-level processes.
Figure 7: Adaptive filtering of ORN inputs controlled by sniff frequency.

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Acknowledgements

The authors thank D. Katz, A. Fontanini and H. Eichenbaum for help with the restrained preparation and the behavioral paradigm; R. Carey, A. Zaharia and A. Milutinovic for help with data analysis; and M. Shipley, J. McGann and N. Pírez for comments. This work was supported by the US National Institutes of Health and Boston University.

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Author notes

  1. Justus V Verhagen & Theoden I Netoff

    Present address: Current addresses: The John B. Pierce Laboratory, 290 Congress Avenue, New Haven, Connecticut 06519, USA (J.V.V.); Department of Biomedical Engineering, University of Minnesota, 312 Church St. SE NHH 7-105, Minneapolis, Minnesota 55455, USA (T.I.N.).,

Authors and Affiliations

  1. Departments of Biology, Boston University, 24 Cummington Street, Boston, 02215, Massachusetts, USA

    Justus V Verhagen, Daniel W Wesson & Matt Wachowiak

  2. Biomedical Engineering, Boston University, 24 Cummington Street, Boston, Massachusetts 02215, USA.,

    John A White

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Contributions

J.V.V., D.W.W. and M.W. contributed to all aspects of the paper, including experimental design, animal training, data collection and analysis. T.I.N. and J.A.W. helped to develop data analysis methods and custom analysis code. All authors contributed to discussing the implications of the results and to preparing the manuscript.

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Correspondence to Matt Wachowiak.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Schematic of the head-fixed behavioral apparatus. (PDF 87 kb)

Supplementary Fig. 2

Comparison of sniff measurements obtained via intranasal pressure versus flow. (PDF 512 kb)

Supplementary Fig. 3

Behavioral responses to odorant presentation. (PDF 113 kb)

Supplementary Fig. 4

Characterization and initial processing of fluorescence signals in the awake rat. (PDF 152 kb)

Supplementary Fig. 5

Attenuation of ORN inputs by high-frequency sniffing imaged with a low-affinity calcium dye. (PDF 84 kb)

Supplementary Fig. 6

Temporal dynamics of electrically-evoked presynaptic calcium signals in vivo. (PDF 94 kb)

Supplementary Fig. 7

Sniff frequency-dependent attenuation of ORN inputs is a general phenomenon. (PDF 104 kb)

Supplementary Fig. 8

Schematic of the effects of sniff frequency on odor representations. (PDF 87 kb)

Supplementary Table 1

Behavioral performance of rats in the two-odor discrimination task. (PDF 39 kb)

Supplementary Methods (PDF 109 kb)

Supplementary Results (PDF 96 kb)

Supplementary Video 1

Movie showing fluorescence imaged from the dorsal OB during high-frequency sniffing of a novel odorant. Top trace shows sniffing record. There is little noticeable movement of the preparation associated with sniffing. (WMV 701 kb)

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Verhagen, J., Wesson, D., Netoff, T. et al. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 10, 631–639 (2007). https://doi.org/10.1038/nn1892

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