Slow-paced inspiration regularizes alpha phase dynamics in the human brain

Author: Shen-Mou Hsu1,2, Chih-Hsin Tseng3, Chao-Hsien Hsieh1,4, Chang-Wei Hsieh5
1 Imaging Center for Integrated Body, Mind and Culture Research, National Taiwan University, Taipei, Taiwan (R.O.C.).
2 MOST AI Biomedical Research Center, Taiwan (R.O.C.).
3 Graduate Institute of Biomedical Electronic and Bioinformatics, National Taiwan University, Taipei, Taiwan (R.O.C.).
4 Interdisciplinary MRI/MRS Laboratory, Department of Electrical Engineering, National Taiwan University, Taipei, Taiwan (R.O.C.).
5 Department of Photonic and Communication Engineering, Asia University, Taichung, Taiwan (R.O.C.).
Conference/Journal: J Neurophysiol
Date published: 2020 Jan 1
Other: Volume ID: 123 , Issue ID: 1 , Pages: 289-299 , Special Notes: doi: 10.1152/jn.00624.2019. , Word Count: 288

The phase of low-frequency, rhythmic cortical activity is essential for organizing brain processes because it provides a recurrent temporal frame for information coding. However, the low-frequency cortical phase exhibits great flexibility in response to external influences. Given that brain rhythms have been found to track respiratory inputs, we hypothesized that slow breathing, commonly associated with mental regulation, could reorganize the relationship between these two rhythmic systems through the adjustment of the cortical phase to such a slow train of inputs. Based on simultaneous magnetoencephalography and respiratory measurements, we report that while participants performed paced breathing, slow relative to normal breathing modulated cortical phase activity in the alpha range across widespread brain areas. Such modulation effects were specifically locked to the middle of the inspiration stage and exhibited a well-structured pattern. At the single-subject level, the phase angles underlying the effects became more likely to be diametrically opposed across breaths, indicating unique and consistent phase adjustment to slow inspiratory inputs. Neither cardiac fluctuations nor breathing-unrelated task effects could account for the findings. We suggest that slow-paced inspiration could organize the cortical phase in a regularized phase pattern, revealing a rhythmic but dynamic neural network integrated with different neurophysiological systems through volitional control.NEW & NOTEWORTHY Breathing is more complicated than a simple gas exchange, as it is integrated with numerous cognitive and emotional functions. Controlled slow breathing has often been used to regulate mental processes. This magnetoencephalography study demonstrates that slow-paced relative to normal-paced inspiration could organize the timing of alpha rhythmic activities across breathing cycles in a structured manner over widespread brain areas. Our results reveal how a volitionally controlled change in respiratory behavior could systematically modulate cortical activity.

Keywords: MEG; alpha; breathing; oscillation; phase.

PMID: 31747328 DOI: 10.1152/jn.00624.2019