Suk-tak Chan1 and Kenneth Kwong K Kwong1
1Martinos Center, Radiology, Massachusetts General Hospital, Charlestown, MA, United States
Synopsis
A preliminary comparison of physiological and fMRI data from an
experienced meditator during mindfulness, paced breathing at 6 breaths/min, and
spontaneous breathing provided several characteristic findings related to the
brain-body mechanisms of mindfulness: 1) a reduction of breathing rate together
with indicators of improved respiratory gas exchange (RGE); 2) a significant correlation
between the temporal oscillation of RGE metrics and cerebral hemodynamic
fluctuations (CHF) in regions within the salience and default mode networks; 3)
a difference in the coherence of CHF with RGE and with heart cycle duration
(NN).
Introduction
Our objective is to study the physiological mechanism of brain-body
interaction between respiratory gas exchange (RGE) and brain activities during
mindfulness (short for mindfulness meditation) in experienced meditation
practitioners. Mindfulness involves attention to breathing. It reduces
breathing rate naturally to around 6 breaths/min1, 2. Paced breathing at 6
breaths/min has been reported to improve RGE3-5, and motivates the
investigation of the role of RGE in mindfulness. RGE metrics include oxygen (O2)
uptake and carbon dioxide (CO2) release and breath-by-breath O2-CO2 exchange ratio (bER)6, which takes into account the effect of both O2 uptake and CO2 release. These
metrics were reported to be superior to respiratory rate/volume in correlating
with brain activities6. The main question is: Is the brain-body
mechanism of mindfulness attributable primarily to the mechanism of slow-paced breathing
of around 6 breaths/min? As inspiration and expiration strongly impact the
change of heart rate7, we also explored how cerebral hemodynamic
fluctuations (CHF) correlated with heart cycle duration (NN).Subjects and Methods
An experienced
meditation practitioner participated in an fMRI scan during three conditions:
1) mindfulness; 2) paced breathing at 6 breaths per minute; 3) spontaneous
breathing. MRI was performed on a 3-Tesla (Siemens Medical, Erlangen, Germany).
Whole-brain BOLD-fMRI datasets were acquired for 10 minutes (TR=1250ms, TE=30ms).
Physiological data including respiration, EKG, partial pressure of O2 (PO2),
and CO2 (PCO2) were collected simultaneously with MRI acquisition.
Data analysis: BOLD-fMRI data were imported into
the software AFNI8.
The physiological data were analyzed using Matlab R2020a. The RGE
metrics of DPO2, DPCO2, and bER were calculated using
the same procedures as described in our previous studies6. Cardiovascular metrics included
normal heart cycle duration (NN), NN variability related to heart rate
variability (HRV). For each of the 3 conditions
(mindfulness, paced breathing, and spontaneous breathing), BOLD signal changes (DBOLD) were cross-correlated separately
with bER and NN using Hilbert Transform analysis. A significant correlation was considered at
corrected p<0.05.
Wavelet transform
coherence analysis was used to measure the dynamic correlation of global DBOLD with RGE
metrics and NN in the time-frequency domain6.Results
Mindfulness lowered the
breathing rate naturally to close to 6 breaths per minute (Table 1). bER had
the highest value during mindfulness, where there was a simultaneous rise of O2
uptake (DPO2).
NN was similar among the three conditions, while the NN variability decreased
from spontaneous breathing to mindfulness and then to slow-paced breathing.
Multiple brain
regions common in mindfulness and slow-paced breathing (Figure 1A; M and P, in
yellow) showed a significant bER-DBOLD
correlation. Regions with significant bER-DBOLD
correlation (Figure 1A; M, in red) was also found only during mindfulness.
Mindfulness shared
the significant bER-DBOLD correlation
with spontaneous breathing but not with slow-paced breathing at the posterior
cingulate and precuneus (Figure 1A; M and S, in purple). NN-DBOLD
correlation maps were also reported (Figure 1B), indicating that bER and
NN interact differently with DBOLD in the three
conditions.
RGE metrics were
shown to oscillate with DBOLD at a very low
frequency of 0.008-0.063Hz in all three conditions (Figure 2), while NN
oscillated with DBOLD at both a low
frequency of 0.063-0.25Hz and a very low frequency of 0.008-0.063Hz during
mindfulness and spontaneous breathing. NN oscillated with DBOLD mainly at the frequency band of
0.063-0.25Hz during slow-paced breathing (Figure 2).Discussion
Although the salience and default mode networks have been reported during
mindfulness9, 10, to our knowledge,
no previous study reported their physiological relationship with RGE. Common brain regions showing significant bER-DBOLD correlation during mindfulness and
slow-paced breathing (Figure 1A) explain perhaps the shared features of slow
breathing and mindfulness. Posterior cingulate and precuneus regions common for
mindfulness and spontaneous breathing but not for slow-paced breathing in their
significant bER-DBOLD correlation
(Figure 1A) suggest that the internal attention to breathing during mindfulness
is different from the attention to external pacing stimuli. The findings in Figure
2 suggest that the bER-DBOLD and NN-DBOLD correlations have different frequency
distributions. It is also not surprising that NN variability (Table 1) is
smallest for slow-paced breathing but largest for spontaneous breathing. Steffen et al.11 reported reduced HRV at high (respiratory)
frequencies but increased HRV at low frequencies for 6 breaths/min. It suggests
that potential health benefits can involve the modulation of both the
parasympathetic and sympathetic systems. A reduction of HRV by attention12 may partly explain why mindfulness also has
smaller NN variability than spontaneous breathing.Conclusion
Our
data show that mindfulness differs from slow-paced breathing and from spontaneous
breathing in their brain-body interaction, which can be studied with fMRI to
map the correlation of brain activities with RGE and cardiovascular metrics.
Acknowledgements
This research was carried out at the
Athinoula A. Martinos Center at the Massachusetts General Hospital, using
resources provided by
NCCIH grant R21AT010955 and by NIH grant P41EB015896 of Center for Functional Neuroimaging
Technologies.
References
1. Bernardi L, Sleight
P, Bandinelli G, et al. Effect of rosary prayer and yoga mantras on autonomic
cardiovascular rhythms: comparative study. BMJ 2001;323:1446-1449.
2. Wielgosz J, Schuyler
BS, Lutz A, et al. Long-term mindfulness training is associated with reliable
differences in resting respiration rate. Sci Rep 2016;6:27533.
3. Bernardi L, Spadacini
G, Bellwon J, et al. Effect of breathing rate on oxygen saturation and exercise
performance in chronic heart failure. Lancet 1998;351:1308-1311.
4. Bilo G, Revera M,
Bussotti M, et al. Effects of slow deep breathing at high altitude on oxygen
saturation, pulmonary and systemic hemodynamics. PLoS One 2012;7:e49074.
5. Sin PY, Webber MR,
Galletly DC, et al. Interactions between heart rate variability and pulmonary
gas exchange efficiency in humans. Exp Physiol 2010;95:788-797.
6. Chan ST, Evans KC,
Song TY, et al. Dynamic brain-body coupling of breath-by-breath O2-CO2 exchange
ratio with resting state cerebral hemodynamic fluctuations. PLoS One
2020;15:e0238946.
7. Grossman P, Taylor
EW. Toward understanding respiratory sinus arrhythmia: relations to cardiac
vagal tone, evolution and biobehavioral functions. Biol Psychol
2007;74:263-285.
8. Cox RW. AFNI:
software for analysis and visualization of functional magnetic resonance
neuroimages. Comput Biomed Res 1996;29:162-173.
9. Ramirez-Barrantes R,
Arancibia M, Stojanova J, et al. Default Mode Network, Meditation, and Age-Associated
Brain Changes: What Can We Learn from the Impact of Mental Training on
Well-Being as a Psychotherapeutic Approach? Neural Plast 2019;2019:7067592.
10. Holzel BK, Lazar SW,
Gard T, et al. How Does Mindfulness Meditation Work? Proposing Mechanisms of
Action From a Conceptual and Neural Perspective. Perspect Psychol Sci
2011;6:537-559.
11. Steffen PR, Austin T,
DeBarros A, et al. The Impact of Resonance Frequency Breathing on Measures of
Heart Rate Variability, Blood Pressure, and Mood. Front Public Health
2017;5:222.
12. Gazzellini S, Dettori M, Amadori F,
et al. Association between Attention and Heart Rate Fluctuations in
Pathological Worriers. Front Hum Neurosci 2016;10:648.