Dynamic mechanisms that couple the brain and breathing to the external environment

Figures

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  Fig. 1. Illustration of brain-breathing synchronization at shorter timescales. Panels (A) and (B) illustrate coherence between brain and breathing activity in the same frequency range as demonstrated by Ito et al. and Herrero et al.24,26. Panels (A) and (C) illustrate cross-frequency coupling between faster frequency activity of the brain and breathing.

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  Fig. 2. Illustration of entrainment. Entrainment results in stable wavelength, phase, and amplitude synchronization through a series of rhythmic phase resets. As entrainment is measured across a sequence of multiple external inputs, entrainment links breathing and brain activity to external inputs on a longer timescale than a phase reset.

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  Fig. 3. Breathing metrics were collected during rest and task conditions (N = 21). Results indicate an overall faster (A) and less variable (B) breathing rhythm in the task relative to the resting state. In (C, D), the black dotted line indicates the exact intertrial interval of the task condition (1.3 seconds). Inspiration (C) and expiration times (D) tended to align themselves with these timings. Statistical measures above bar plots indicate results from F-tests. Results indicate significant decreases in the group variance of the SDBBI, inspiration, and expiration phase lengths during the task compared to resting conditions. A lower amount of intersubject variability during task states indicates that the breathing rhythm shapes itself to match the temporal structure of the external input. SDBBI = standard deviation of the breath-to-breath intervals. Error bars represent the 95% confidence interval.

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  Fig. 4. Visualization of the differences in the distributions of inspiration and expiration times between rest and task. Panels (A) and (B) represent the rest condition and panels (C) and (D) represent task conditions across participants (N = 21). Black dotted lines represent the intertrial interval of 1.3 s (0.769 Hz). Results indicate that participants’ inspiration and expiration times group themselves around the intertrial interval of the task (1.3 s). Error bars represent the 95% confidence interval.

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  Fig. 5. Visualization of dynamic attunement. A Power spectrum of respiration and EEG signals averaged across participants (N = 21). For the breathing, we observe an overall shift from slower to faster frequencies in task versus resting state conditions. A zoom-in to the light blue shaded area for each subject can be found in the supplemental material. B In both breathing and brain, a larger peak is found at the rate of stimulus presentation (0.769 Hz, exact frequency indicated by red dotted line) during the task indicating the presence of task-dependent entrainment (i.e., task periodicity). C Total PSD and peak to total PSD ratio for breathing and brain. PSD = power spectral density. Error bars represent the 95% confidence interval.

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  Fig. 6. Breathing-brain coupling is shaped by the external environment. Synchronization of brain and local breathing to the external temporal stimulus pattern (N = 21). A Increases in brain-breathing coupling during task conditions are indicated by the increase in coherence at precisely the intertrial interval of the task (i.e., 0.769 Hz). B Synchronization of the breathing activity with faster frequencies in the brain. Increases in brain-breathing coupling during task conditions are further supported by increases in the modulation index. Higher degrees of coherence and modulation indices between breathing and the Cz channel during task conditions suggest that the external task dynamics impact the brain-breathing coupling relationship. Error bars represent the 95% confidence interval.

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  Fig. 7. Summary of findings. Overall, our findings support two dynamic mechanisms of brain-breathing alignment. First, we show that the lungs and brain synchronize their activity with one another over shorter timescales like milliseconds or seconds as evidenced by coherence, cross-frequency coupling, and entrainment. Second, operating over longer timescales of minutes if not hours, our empirical data suggest that the temporal structure of the environmental inputs shapes the temporal structure of the activities within both lungs and brain activity at the Cz channel. This is indicated by the frequency-specific adaptations in their power spectrums to the exact frequency of the intertrial interval of the task (i.e., dynamic attunement). Dynamic attunement describes a form of alignment in which the lungs and brain adapt the temporal structure of their activities like in their power spectra to the specific temporal characteristics of the external environmental inputs. Brain-breathing dynamic attunement is further supported by the increase in coherence between the lungs and brain at 0.769 Hz during the task which indicates their common alignment to a shared third party (i.e., the input…