Human non-olfactory cognition phase-locked with inhalation


Olfactory stimulus acquisition is perfectly synchronized with inhalation, which tunes neuronal ensembles for incoming information. Because olfaction is an ancient sensory system that provided a template for brain evolution, we hypothesized that this link persisted, and therefore nasal inhalations may also tune the brain for acquisition of non-olfactory information. To test this, we measured nasal airflow and electroencephalography during various non-olfactory cognitive tasks. We observed that participants spontaneously inhale at non-olfactory cognitive task onset and that such inhalations shift brain functional network architecture. Concentrating on visuospatial perception, we observed that nasal inhalation drove increased task-related brain activity in specific task-related brain regions and resulted in improved performance accuracy in the visuospatial task. Thus, mental processes with no link to olfaction are nevertheless phase-locked with nasal inhalation, consistent with the notion of an olfaction-based template in the evolution of human brain function.

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Fig. 1: Humans spontaneously nasally inhale at cognitive task onset.
Fig. 2: Inhalation drives changes in functional brain connectivity at rest.
Fig. 3: Nasal inhalation at visuospatial task onset is associated with improved performance.
Fig. 4: Nasal inhalation drives task-specific increased local brain activity in non-limbic regions.
Fig. 5: Respiratory-phase-locked shifts in neural activity are correlated with phase-locked shifts in behavioural performance.
Fig. 6: Nasal inhalation drives localized task-specific reductions in EEG power.
Fig. 7: Inhale–exhale differences in resting brain connectivity reflected later inhale–exhale differences in performance accuracy.

Code availability

The custom MATLAB scripts used to process and visualize the data collected in this study are available at:

Data availability

The data that support the findings in this study are available from the corresponding authors on request and are also posted at


  1. 1.

    Craven, B. A., Paterson, E. G. & Settles, G. S. The fluid dynamics of canine olfaction: unique nasal airflow patterns as an explanation of macrosmia. J. R. Soc. Interface 7, 933–943 (2009).

    Article  Google Scholar 

  2. 2.

    Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M. & Ma, M. Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 10, 348–354 (2007).

    CAS  Article  Google Scholar 

  3. 3.

    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).

    CAS  Article  Google Scholar 

  4. 4.

    Shusterman, R., Smear, M. C., Koulakov, A. A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039–1044 (2011).

    CAS  Article  Google Scholar 

  5. 5.

    Smear, M., Shusterman, R., O’Connor, R., Bozza, T. & Rinberg, D. Perception of sniff phase in mouse olfaction. Nature 479, 397–400 (2011).

    CAS  Article  Google Scholar 

  6. 6.

    Sobel, N. et al. Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392, 282–286 (1998).

    CAS  Article  Google Scholar 

  7. 7.

    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).

    CAS  Article  Google Scholar 

  8. 8.

    Kepecs, A., Uchida, N. & Mainen, Z. F. The sniff as a unit of olfactory processing. Chem. Senses 31, 167–179 (2005).

    Article  Google Scholar 

  9. 9.

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

    Article  Google Scholar 

  10. 10.

    Strausfeld, N. J. & Hildebrand, J. G. Olfactory systems: common design, uncommon origins? Curr. Opin. Neurobiol. 9, 634–639 (1999).

    CAS  Article  Google Scholar 

  11. 11.

    Rowe, T. B., Macrini, T. E. & Luo, Z.-X. Fossil evidence on origin of the mammalian brain. Science 332, 955–957 (2011).

    CAS  Article  Google Scholar 

  12. 12.

    Rowe, T. B. & Shepherd, G. M. Role of ortho‐retronasal olfaction in mammalian cortical evolution. J. Comp. Neurol. 524, 471–495 (2016).

    Article  Google Scholar 

  13. 13.

    Freeman, W. J. The place of ‘codes’ in nonlinear neurodynamics. Prog. Brain Res. 165, 447–462 (2007).

    Article  Google Scholar 

  14. 14.

    Heck, D. H. et al. Breathing as a fundamental rhythm of brain function. Front. Neural Circuits 10, 115 (2017).

    Article  Google Scholar 

  15. 15.

    Fontanini, A. & Bower, J. M. Slow-waves in the olfactory system: an olfactory perspective on cortical rhythms. Trends Neurosci. 29, 429–437 (2006).

    CAS  Article  Google Scholar 

  16. 16.

    Tort, A., Brankačk, J. & Draguhn, A. Respiration-entrained brain rhythms are global but often overlooked. Trends Neurosci. 41, 186–197 (2018).

    CAS  Article  Google Scholar 

  17. 17.

    Biskamp, J., Bartos, M. & Sauer, J.-F. Organization of prefrontal network activity by respiration-related oscillations. Sci. Rep. 7, 45508 (2017).

    CAS  Article  Google Scholar 

  18. 18.

    Zhong, W. et al. Selective entrainment of gamma subbands by different slow network oscillations. Proc. Natl Acad. Sci. USA 114, 4519–4524 (2017).

    CAS  Article  Google Scholar 

  19. 19.

    Herrero, J. L., Khuvis, S., Yeagle, E., Cerf, M. & Mehta, A. D. Breathing above the brain stem: volitional control and attentional modulation in humans. J. Neurophysiol. 119, 145–159 (2017).

    Article  Google Scholar 

  20. 20.

    Piarulli, A. et al. Ultra-slow mechanical stimulation of olfactory epithelium modulates consciousness by slowing cerebral rhythms in humans. Sci. Rep. 8, 6581 (2018).

    CAS  Article  Google Scholar 

  21. 21.

    Cao, Y., Roy, S., Sachdev, R. N. & Heck, D. H. Dynamic correlation between whisking and breathing rhythms in mice. J. Neurosci. 32, 1653–1659 (2012).

    CAS  Article  Google Scholar 

  22. 22.

    Moore, J. D. et al. Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature 497, 205–210 (2013).

    CAS  Article  Google Scholar 

  23. 23.

    Sirotin, Y. B., Costa, M. E. & Laplagne, D. A. Rodent ultrasonic vocalizations are bound to active sniffing behavior. Front. Behav. Neurosci. 8, 399 (2014).

    Article  Google Scholar 

  24. 24.

    Wong, J. & Waters, D. The synchronisation of signal emission with wingbeat during the approach phase in soprano pipistrelles (Pipistrellus pygmaeus). J. Exp. Biol. 204, 575–583 (2001).

    CAS  PubMed  Google Scholar 

  25. 25.

    Suthers, R. A., Thomas, S. P. & Suthers, B. J. Respiration, wing-beat and ultrasonic pulse emission in an echo-locating bat. J. Exp. Biol. 56, 37–48 (1972).

    Google Scholar 

  26. 26.

    Kleinfeld, D., Deschênes, M., Wang, F. & Moore, J. D. More than a rhythm of life: breathing as a binder of orofacial sensation. Nat. Neurosci. 17, 647–651 (2014).

    CAS  Article  Google Scholar 

  27. 27.

    Zelano, C. et al. Nasal respiration entrains human limbic oscillations and modulates cognitive function. J. Neurosci. 36, 12448–12467 (2016).

    CAS  Article  Google Scholar 

  28. 28.

    Bensafi, M. et al. Olfactomotor activity during imagery mimics that during perception. Nat. Neurosci. 6, 1142–1144 (2003).

    CAS  Article  Google Scholar 

  29. 29.

    Arshamian, A., Iravani, B., Majid, A. & Lundström, J. N. Respiration modulates olfactory memory consolidation in humans. J. Neurosci. 38, 10286–10294 (2018).

    CAS  Article  Google Scholar 

  30. 30.

    Nakamura, N. H., Fukunaga, M. & Oku, Y. Respiratory modulation of cognitive performance during the retrieval process. PLoS One 13, e0204021 (2018).

    Article  Google Scholar 

  31. 31.

    Frost, R., Siegelman, N., Narkiss, A. & Afek, L. What predicts successful literacy acquisition in a second language? Psychol. Sci. 24, 1243–1252 (2013).

    Article  Google Scholar 

  32. 32.

    Uecker, A. et al. Neuroanatomical correlates of implicit and explicit memory for structurally possible and impossible visual objects. Learn. Mem. 4, 337–355 (1997).

    CAS  Article  Google Scholar 

  33. 33.

    Rubinson, M. et al. Hierarchy measurement for modeling network dynamics under directed attacks. Phys. Rev. E 96, 052307 (2017).

    CAS  Article  Google Scholar 

  34. 34.

    Barry, R. J., Clarke, A. R. & Johnstone, S. J. A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography. Clin. Neurophysiol. 114, 171–183 (2003).

    Article  Google Scholar 

  35. 35.

    Renault, B., Ragot, R., Lesevre, N. & Remond, A. Onset and offset of brain events as indices of mental chronometry. Science 215, 1413–1415 (1982).

    CAS  Article  Google Scholar 

  36. 36.

    Kenemans, J., Kok, A. & Smulders, F. Event-related potentials to conjunctions of spatial frequency and orientation as a function of stimulus parameters and response requirements. Electroencephalogr. Clin. Neurophysiol. 88, 51–63 (1993).

    CAS  Article  Google Scholar 

  37. 37.

    Pascual-Marqui, R. D., Michel, C. M. & Lehmann, D. Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int. J. Psychophysiol. 18, 49–65 (1994).

    CAS  Article  Google Scholar 

  38. 38.

    Grech, R. et al. Review on solving the inverse problem in EEG source analysis. J. Neuroeng. Rehabil. 5, 25 (2008).

    Article  Google Scholar 

  39. 39.

    Pascual-Marqui, R. D. Review of methods for solving the EEG inverse problem. Int. J. Bioelectromagn. 1, 75–86 (1999).

    Google Scholar 

  40. 40.

    Brown, R. P. & Gerbarg, P. L. Sudarshan Kriya yogic breathing in the treatment of stress, anxiety, and depression: part I—neurophysiologic model. J. Altern. Complement. Med. 11, 189–201 (2005).

    Article  Google Scholar 

  41. 41.

    Park, H.-J. & Friston, K. Structural and functional brain networks: from connections to cognition. Science 342, 1238411 (2013).

    Article  Google Scholar 

  42. 42.

    Egner, T. & Gruzelier, J. H. EEG biofeedback of low beta band components: frequency-specific effects on variables of attention and event-related brain potentials. Clin. Neurophysiol. 115, 131–139 (2004).

    CAS  Article  Google Scholar 

  43. 43.

    Bassett, D. S. & Bullmore, E. Small-world brain networks. Neuroscientist 12, 512–523 (2006).

    Article  Google Scholar 

  44. 44.

    Stam, C. J., Jones, B., Nolte, G., Breakspear, M. & Scheltens, P. Small-world networks and functional connectivity in Alzheimer’s disease. Cereb. Cortex 17, 92–99 (2006).

    Article  Google Scholar 

  45. 45.

    Micheloyannis, S. et al. Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr. Res. 87, 60–66 (2006).

    Article  Google Scholar 

  46. 46.

    Naim-Feil, J. et al. Altered brain network dynamics in schizophrenia: a cognitive electroencephalography study. Biol. Psychiatry Cogn. Neurosci. Neuroimaging 3, 88–98 (2018).

    Article  Google Scholar 

  47. 47.

    Klimesch, W., Sauseng, P. & Hanslmayr, S. EEG alpha oscillations: the inhibition–timing hypothesis. Brain Res. Rev. 53, 63–88 (2007).

    Article  Google Scholar 

  48. 48.

    Ritter, P., Moosmann, M. & Villringer, A. Rolandic alpha and beta EEG rhythms’ strengths are inversely related to fMRI‐BOLD signal in primary somatosensory and motor cortex. Hum. Brain Mapp. 30, 1168–1187 (2009).

    Article  Google Scholar 

  49. 49.

    Janzen, G. & Weststeijn, C. G. Neural representation of object location and route direction: an event-related fMRI study. Brain Res. 1165, 116–125 (2007).

    CAS  Article  Google Scholar 

  50. 50.

    Del Negro, C. A., Funk, G. D. & Feldman, J. L. Breathing matters. Nat. Rev. Neurosci. 19, 351–367 (2018).

    Article  Google Scholar 

  51. 51.

    Dlouhy, B. J. et al. Breathing inhibited when seizures spread to the amygdala and upon amygdala stimulation. J. Neurosci. 35, 10281–10289 (2015).

    CAS  Article  Google Scholar 

  52. 52.

    Nobis, W. P. et al. Amygdala‐stimulation‐induced apnea is attention and nasal‐breathing dependent. Ann. Neurol. 83, 460–471 (2018).

    Article  Google Scholar 

  53. 53.

    Birn, R. M., Murphy, K., Handwerker, D. A. & Bandettini, P. A. fMRI in the presence of task-correlated breathing variations. Neuroimage 47, 1092–1104 (2009).

    Article  Google Scholar 

  54. 54.

    Simonsohn, U., Nelson, L. D. & Simmons, J. P. p-Curve and effect size: correcting for publication bias using only significant results. Perspect. Psychol. Sci. 9, 666–681 (2014).

    Article  Google Scholar 

  55. 55.

    Kozma, R. & Freeman, W. Analysis of visual theta rhythm—experimental and theoretical evidence of visual sniffing. In IJCNN'01. International Joint Conference on Neural Networks 1118–1121 (IEEE, 2001).

  56. 56.

    Faul, F., Erdfelder, E., Lang, A. G. & Buchner, A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39, 175–191 (2007).

    Article  Google Scholar 

  57. 57.

    Johnson, B. N., Russell, C., Khan, R. M. & Sobel, N. A comparison of methods for sniff measurement concurrent with olfactory tasks in humans. Chem. Senses 31, 795–806 (2006).

    Article  Google Scholar 

  58. 58.

    Homan, R. W., Herman, J. & Purdy, P. Cerebral location of international 10–20 system electrode placement. Electroencephal. Clin. Neurophysiol. 66, 376–382 (1987).

    CAS  Article  Google Scholar 

  59. 59.

    Gratton, G., Coles, M. G. & Donchin, E. A new method for off-line removal of ocular artifact. Electroencephal. Clin. Neurophysiol. 55, 468–484 (1983).

    CAS  Article  Google Scholar 

  60. 60.

    Koenig, T., Kottlow, M., Stein, M. & Melie-García, L. Ragu: a free tool for the analysis of EEG and MEG event-related scalp field data using global randomization statistics. Comput. Intell. Neurosci. 2011, 938925 (2011).

    Article  Google Scholar 

  61. 61.

    Bailey, N. et al. Mindfulness meditators show altered distributions of early and late neural activity markers of attention in a response inhibition task. Preprint at (2018).

  62. 62.

    Xia, M., Wang, J. & He, Y. BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 8, e68910 (2013).

    CAS  Article  Google Scholar 

  63. 63.

    Tibshirani, R. The lasso method for variable selection in the Cox model. Stat. Med. 16, 385–395 (1997).

    CAS  Article  Google Scholar 

  64. 64.

    Antony, A. R. et al. Functional connectivity estimated from intracranial EEG predicts surgical outcome in intractable temporal lobe epilepsy. PLoS One 8, e77916 (2013).

    CAS  Article  Google Scholar 

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This work was supported by grant 1599/14 from the Israel Science Foundation, a grant from Joy Ventures and by the Rob and Cheryl McEwen Fund for Brain Research. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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O.P. and N.S. developed the idea for the study. O.P., A.E., T.S. and N.M. designed and ran the experiments. O.P., A.R. and M.R. analysed the data. O.P., L.S. and N.S. wrote the manuscript.

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Correspondence to Ofer Perl or Noam Sobel.

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Perl, O., Ravia, A., Rubinson, M. et al. Human non-olfactory cognition phase-locked with inhalation. Nat Hum Behav 3, 501–512 (2019).

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