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Precise olfactory responses tile the sniff cycle

Nature Neuroscience volume 14, pages 1039–1044 (2011)Cite this article

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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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References

  1. Bair, W. & Koch, C. Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput. 8, 1185–1202 (1996).

    Article  CAS  Google Scholar 

  2. Berry, M.J., Warland, D.K. & Meister, M. The structure and precision of retinal spike trains. Proc. Natl. Acad. Sci. USA 94, 5411–5416 (1997).

    Article  CAS  Google Scholar 

  3. Butts, D.A. et al. Temporal precision in the neural code and the timescales of natural vision. Nature 449, 92–95 (2007).

    Article  CAS  Google Scholar 

  4. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).

    Article  CAS  Google Scholar 

  5. Rieke, F., Warland, D., de Ruyter van Steveninck, R. & Bialek, W. Spikes: Exploring the Neural Code (MIT Press, Cambridge, Massachusetts, 1997).

  6. Laurent, G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3, 884–895 (2002).

    Article  CAS  Google Scholar 

  7. Chaput, M.A. Respiratory-phase-related coding of olfactory information in the olfactory-bulb of awake freely breathing rabbits. Physiol. Behav. 36, 319–324 (1986).

    Article  CAS  Google Scholar 

  8. Fantana, A.L., Soucy, E.R. & Meister, M. Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59, 802–814 (2008).

    Article  CAS  Google Scholar 

  9. Buonviso, N. et al. Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur. J. Neurosci. 17, 1811–1819 (2003).

    Article  Google Scholar 

  10. Kepecs, A., Uchida, N. & Mainen, Z.F. The sniff as a unit of olfactory processing. Chem. Senses 31, 167–179 (2006).

    Article  Google Scholar 

  11. Abraham, N.M. et al. Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44, 865–876 (2004).

    CAS  Google Scholar 

  12. Uchida, N. & Mainen, Z.F. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224–1229 (2003).

    Article  CAS  Google Scholar 

  13. Rinberg, D., Koulakov, A. & Gelperin, A. Speed-accuracy tradeoff in olfaction. Neuron 51, 351–358 (2006).

    Article  CAS  Google Scholar 

  14. Doucette, W. & Restrepo, D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 6, e258 (2008).

    Article  Google Scholar 

  15. Fuentes, R.A., Aguilar, M.I., Aylwin, M.L. & Maldonado, P.E. Neuronal activity of mitral-tufted cells in awake rats during passive and active odorant stimulation. J. Neurophysiol. 100, 422–430 (2008).

    Article  Google Scholar 

  16. Kay, L.M. & Laurent, G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat. Neurosci. 2, 1003–1009 (1999).

    Article  CAS  Google Scholar 

  17. Rinberg, D., Koulakov, A. & Gelperin, A. Sparse odor coding in awake behaving mice. J. Neurosci. 26, 8857–8865 (2006).

    Article  CAS  Google Scholar 

  18. Verhagen, J.V., Wesson, D.W., Netoff, T.I., White, J.A. & Wachowiak, M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10, 631–639 (2007).

    Article  CAS  Google Scholar 

  19. Laurent, G., Wehr, M. & Davidowitz, H. Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837–3847 (1996).

    Article  CAS  Google Scholar 

  20. Pager, J. Respiration and olfactory-bulb unit-activity in the unrestrained rat: statements and reappraisals. Behav. Brain Res. 16, 81–94 (1985).

    Article  CAS  Google Scholar 

  21. Bathellier, B., Buhl, D.L., Accolla, R. & Carleton, A. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57, 586–598 (2008).

    Article  CAS  Google Scholar 

  22. Bhalla, U.S. & Bower, J.M. Multiday recordings from olfactory bulb neurons in awake freely moving rats: spatially and temporally organized variability in odorant response properties. J. Comput. Neurosci. 4, 221–256 (1997).

    Article  CAS  Google Scholar 

  23. Cury, K.M. & Uchida, N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570–585 (2010).

    Article  CAS  Google Scholar 

  24. Vetter, R.S., Sage, A.E., Justus, K.A., Carde, R.T. & Galizia, C.G. Temporal integrity of an airborne odor stimulus is greatly affected by physical aspects of the odor delivery system. Chem. Senses 31, 359–369 (2006).

    Article  Google Scholar 

  25. Raman, B., Joseph, J., Tang, J. & Stopfer, M. Temporally diverse firing patterns in olfactory receptor neurons underlie spatiotemporal neural codes for odors. J. Neurosci. 30, 1994–2006 (2010).

    Article  CAS  Google Scholar 

  26. Nagel, K.I. & Wilson, R.I. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat. Neurosci. 14, 208–216 (2011).

    Article  CAS  Google Scholar 

  27. 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 

  28. Shepherd, G.M. ed. The Synaptic Organization of the Brain (Oxford University Press, 2004).

  29. Adrian, E.D. The electrical activity of the mammalian olfactory bulb. Electroencephalogr. Clin. Neurophysiol. 2, 377–388 (1950).

    Article  CAS  Google Scholar 

  30. 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 

  31. Margrie, T.W. & Schaefer, A.T. Theta oscillation coupled spike latencies yield computational vigor in a mammalian sensory system. J. Physiol. (Lond.) 546, 363–374 (2003).

    Article  CAS  Google Scholar 

  32. 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 

  33. Hopfield, J.J. Pattern-recognition computation using action-potential timing for stimulus representation. Nature 376, 33–36 (1995).

    Article  CAS  Google Scholar 

  34. Brody, C.D. & Hopfield, J.J. Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37, 843–852 (2003).

    Article  CAS  Google Scholar 

  35. Franks, K.M. & Isaacson, J.S. Strong single-fiber sensory inputs to olfactory cortex: Implications for olfactory coding. Neuron 49, 357–363 (2006).

    Article  CAS  Google Scholar 

  36. Poo, C. & Isaacson, J.S. Odor representations in olfactory cortex: 'sparse' coding, global inhibition, and oscillations. Neuron 62, 850–861 (2009).

    Article  CAS  Google Scholar 

  37. Haberly, L.B. & Price, J.L. Axonal projection patterns of mitral and tufted cells of olfactory-bulb in rat. Brain Res. 129, 152–157 (1977).

    Article  CAS  Google Scholar 

  38. Miyamichi, K. et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191–196 (2011).

    Article  CAS  Google Scholar 

  39. Stettler, D.D. & Axel, R. Representations of odor in the piriform cortex. Neuron 63, 854–864 (2009).

    Article  CAS  Google Scholar 

  40. Perez-Orive, J. et al. Oscillations and sparsening of odor representations in the mushroom body. Science 297, 359–365 (2002).

    Article  CAS  Google Scholar 

  41. Cassenaer, S. & Laurent, G. Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448, 709–713 (2007).

    Article  CAS  Google Scholar 

  42. Assisi, C., Stopfer, M., Laurent, G. & Bazhenov, M. Adaptive regulation of sparseness by feedforward inhibition. Nat. Neurosci. 10, 1176–1184 (2007).

    Article  CAS  Google Scholar 

  43. Barlow, H.B. Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1, 371–394 (1972).

    Article  CAS  Google Scholar 

  44. Bishop, C. Pattern Recognition and Machine Learning (Springer, 2006).

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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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Authors and Affiliations

  1. Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA

    Roman Shusterman, Matthew C Smear & Dmitry Rinberg

  2. Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois, USA

    Matthew C Smear

  3. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA

    Alexei A Koulakov

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  1. Roman Shusterman
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  2. Matthew C Smear
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  3. Alexei A Koulakov
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Contributions

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.

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Correspondence to Dmitry Rinberg.

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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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