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Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors

Nature Neuroscience volume 10, pages 348–354 (2007)Cite this article

Abstract

Most sensory systems are primarily specialized to detect one sensory modality. Here we report that olfactory sensory neurons (OSNs) in the mammalian nose can detect two distinct modalities transmitted by chemical and mechanical stimuli. As revealed by patch-clamp recordings, many OSNs respond not only to odorants, but also to mechanical stimuli delivered by pressure ejections of odor-free Ringer solution. The mechanical responses correlate directly with the pressure intensity and show several properties similar to those induced by odorants, including onset latency, reversal potential and adaptation to repeated stimulation. Blocking adenylyl cyclase or knocking out the cyclic nucleotide–gated channel CNGA2 eliminates the odorant and the mechanical responses, suggesting that both are mediated by a shared cAMP cascade. We further show that this mechanosensitivity enhances the firing frequency of individual neurons when they are weakly stimulated by odorants and most likely drives the rhythmic activity (theta oscillation) in the olfactory bulb to synchronize with respiration.

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Figure 1: The septal organ neurons respond to both chemical and mechanical stimuli.
Figure 2: The septal organ neurons respond to diverse odorants and mechanical stimulation.
Figure 3: OSNs from both the septal organ and the main olfactory epithelium show mechanical responses.
Figure 4: The cAMP cascade and CNG channels underlie the mechanical responses of the OSNs.
Figure 5: Increasing puffing pressure enhances the odorant responses in individual OSNs.
Figure 6: The rhythmic activity (theta band) in the olfactory bulb uncouples from respiration in Cnga2−/y mice.

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References

  1. Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 (1991).

    Article  CAS  Google Scholar 

  2. Firestein, S. How the olfactory system makes sense of scents. Nature 413, 211–218 (2001).

    Article  CAS  Google Scholar 

  3. Adrian, E.D. The role of air movement in olfactory stimulation. J. Physiol. (Lond.) 114, 4–5p (1951).

    CAS  Google Scholar 

  4. Fontanini, A., Spano, P. & Bower, J.M. Ketamine-xylazine-induced slow (<1.5 Hz) oscillations in the rat piriform (olfactory) cortex are functionally correlated with respiration. J. Neurosci. 23, 7993–8001 (2003).

    Article  CAS  Google Scholar 

  5. Macrides, F. & Chorover, S.L. Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175, 84–87 (1972).

    Article  CAS  Google Scholar 

  6. Onoda, N. & Mori, K. Depth distribution of temporal firing patterns in olfactory bulb related to air-intake cycles. J. Neurophysiol. 44, 29–39 (1980).

    Article  CAS  Google Scholar 

  7. Philpot, B.D., Foster, T.C. & Brunjes, P.C. Mitral/tufted cell activity is attenuated and becomes uncoupled from respiration following naris closure. J. Neurobiol. 33, 374–386 (1997).

    Article  CAS  Google Scholar 

  8. Ueki, S. & Domino, E.F. Some evidence for a mechanical receptor in olfactory function. J. Neurophysiol. 24, 12–25 (1961).

    Article  CAS  Google Scholar 

  9. Potter, H. & Chorover, S.L. Response plasticity in hamster olfactory bulb: peripheral and central processes. Brain Res. 116, 417–429 (1976).

    Article  CAS  Google Scholar 

  10. Ravel, N., Caille, D. & Pager, J. A centrifugal respiratory modulation of olfactory bulb unit activity: a study on acute rat preparation. Exp. Brain Res. 65, 623–628 (1987).

    Article  CAS  Google Scholar 

  11. Ravel, N. & Pager, J. Respiratory patterning of the rat olfactory bulb unit activity: nasal versus tracheal breathing. Neurosci. Lett. 115, 213–218 (1990).

    Article  CAS  Google Scholar 

  12. Sobel, E.C. & Tank, D.W. Timing of odor stimulation does not alter patterning of olfactory bulb unit activity in freely breathing rats. J. Neurophysiol. 69, 1331–1337 (1993).

    Article  CAS  Google Scholar 

  13. Mainland, J. & Sobel, N. The sniff is part of the olfactory percept. Chem. Senses 31, 181–196 (2005).

    Article  Google Scholar 

  14. Ingber, D.E. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20, 811–827 (2006).

    Article  CAS  Google Scholar 

  15. Lin, S.Y. & Corey, D.P. TRP channels in mechanosensation. Curr. Opin. Neurobiol. 15, 350–357 (2005).

    Article  CAS  Google Scholar 

  16. Zhao, H. & Reed, R.R. X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104, 651–660 (2001).

    Article  CAS  Google Scholar 

  17. Rodolfo-Masera, T. Su 1'esistenza di un particolare organo olfacttivo nel setto nasale della cavia e di altri roditori. Arch. Ital. Anat. Embryol. 48, 157–212 (1943).

    Google Scholar 

  18. Ma, M. et al. Olfactory signal transduction in the mouse septal organ. J. Neurosci. 23, 317–324 (2003).

    Article  CAS  Google Scholar 

  19. Chen, S., Lane, A.P., Bock, R., Leinders-Zufall, T. & Zufall, F. Blocking adenylyl cyclase inhibits olfactory generator currents induced by “IP(3)-odors”. J. Neurophysiol. 84, 575–580 (2000).

    Article  CAS  Google Scholar 

  20. Spehr, M., Wetzel, C.H., Hatt, H. & Ache, B.W. 3-phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron 33, 731–739 (2002).

    Article  CAS  Google Scholar 

  21. Kurahashi, T. & Shibuya, T. Ca2+-dependent adaptive properties in the solitary olfactory receptor cell of the newt. Brain Res. 515, 261–268 (1990).

    Article  CAS  Google Scholar 

  22. Zufall, F., Shepherd, G.M. & Firestein, S. Inhibition of the olfactory cyclic nucleotide gated ion channel by intracellular calcium. Proc. R. Soc. Lond. B 246, 225–230 (1991).

    Article  CAS  Google Scholar 

  23. Zufall, F. & Leinders-Zufall, T. The cellular and molecular basis of odor adaptation. Chem. Senses 25, 473–481 (2000).

    Article  CAS  Google Scholar 

  24. Paoletti, P. & Ascher, P. Mechanosensitivity of NMDA receptors in cultured mouse central neurons. Neuron 13, 645–655 (1994).

    Article  CAS  Google Scholar 

  25. Johnson, B.N., Mainland, J.D. & Sobel, N. Rapid olfactory processing implicates subcortical control of an olfactomotor system. J. Neurophysiol. 90, 1084–1094 (2003).

    Article  Google Scholar 

  26. Laing, D.G. Natural sniffing gives optimum odour perception for humans. Perception 12, 99–117 (1983).

    Article  CAS  Google Scholar 

  27. Lai-Fook, S.J. & Lai, Y.L. Airway resistance due to alveolar gas compression measured by barometric plethysmography in mice. J. Appl. Physiol. 98, 2204–2218 (2005).

    Article  Google Scholar 

  28. Balu, R., Larimer, P. & Strowbridge, B.W. Phasic stimuli evoke precisely timed spikes in intermittently discharging mitral cells. J. Neurophysiol. 92, 743–753 (2004).

    Article  Google Scholar 

  29. Hayar, A., Karnup, S., Shipley, M.T. & Ennis, M. Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J. Neurosci. 24, 1190–1199 (2004).

    Article  CAS  Google Scholar 

  30. Hayar, A., Shipley, M.T. & Ennis, M. Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms. J. Neurosci. 25, 8197–8208 (2005).

    Article  CAS  Google Scholar 

  31. Schoppa, N.E. & Westbrook, G.L. Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31, 639–651 (2001).

    Article  CAS  Google Scholar 

  32. Urban, N.N. & Sakmann, B. Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J. Physiol. (Lond.) 542, 355–367 (2002).

    Article  CAS  Google Scholar 

  33. Chaput, M.A. EOG responses in anesthetized freely breathing rats. Chem. Senses 25, 695–701 (2000).

    Article  CAS  Google Scholar 

  34. Cang, J. & Isaacson, J.S. In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J. Neurosci. 23, 4108–4116 (2003).

    Article  CAS  Google Scholar 

  35. Luo, M. & Katz, L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32, 1165–1179 (2001).

    Article  CAS  Google Scholar 

  36. Spors, H., Wachowiak, M., Cohen, L.B. & Friedrich, R.W. Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J. Neurosci. 26, 1247–1259 (2006).

    Article  CAS  Google Scholar 

  37. Ma, M., Chen, W.R. & Shepherd, G.M. Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation. J. Neurosci. Methods 92, 31–40 (1999).

    Article  CAS  Google Scholar 

  38. Ma, M. & Shepherd, G.M. Functional mosaic organization of mouse olfactory receptor neurons. Proc. Natl. Acad. Sci. USA 97, 12869–12874 (2000).

    Article  CAS  Google Scholar 

  39. Grosmaitre, X., Vassalli, A., Mombaerts, P., Shepherd, G.M. & Ma, M. Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: a patch clamp analysis in gene-targeted mice. Proc. Natl. Acad. Sci. USA 103, 1970–1975 (2006).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the US National Institutes of Health (National Institute on Deafness and Other Communication Disorders), the Whitehall Foundation and the University of Pennsylvania Institute on Aging (a pilot grant). We thank H. Zhao at Johns Hopkins University for providing the Cnga2 knockout mice and A. Gelperin, P. Haydon and M. Nusbaum for insightful discussions.

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Authors and Affiliations

  1. Department of Neuroscience, University of Pennsylvania School of Medicine, 215 Stemmler Hall, 3450 Hamilton Walk, Philadelphia, 19104, Pennsylvania, USA

    Xavier Grosmaitre, Lindsey C Santarelli & Minghong Ma

  2. National Institute of Biological Sciences, No. 7 Science Park Road, Beijing, 102206, China

    Jie Tan & Minmin Luo

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  1. Xavier Grosmaitre
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  2. Lindsey C Santarelli
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Contributions

X.G. performed the recordings in the septal organ, L.C.S. performed the recordings in the main olfactory epithelium, J.T. performed the recordings in the olfactory bulb, M.L. supervised the bulb recordings, and M.M. supervised the whole project and drafted the manuscript.

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Correspondence to Minghong Ma.

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The authors declare no competing financial interests.

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Grosmaitre, X., Santarelli, L., Tan, J. et al. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10, 348–354 (2007). https://doi.org/10.1038/nn1856

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