Human non-olfactory cognition phase-locked with inhalation

Abstract

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: https://github.com/WORGOlfaction/perl-2019.

Data availability

The data that support the findings in this study are available from the corresponding authors on request and are also posted at https://www.weizmann.ac.il/neurobiology/worg/materials.html.

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Acknowledgements

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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The authors declare no competing interests.

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Supplementary Figure 1–16, Supplementary Tables 1–3.

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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). https://doi.org/10.1038/s41562-019-0556-z

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