Cortical Sources of Respiratory Mechanosensation, Laterality, and Emotion: An MEG Study

Abstract

Airway obstruction activates mechanoreceptors that project to the cerebral cortices in humans, as evidenced by scalp encephalography recordings of cortical neuronal activation, i.e., respiratory-related evoked potential (RREP). However, neural evidence of both high spatial and temporal resolution of occlusion-elicited cortical activation in healthy individuals is lacking. In the present study, we tested our hypothesis that inspiratory mechanical stimuli elicit neural activation in cortical structures that can be recorded using magnetoencephalography (MEG). We further examined the relationship between depression and respiratory symptoms and hemispheric dominance in terms of emotional states. A total of 14 healthy nonsmoking participants completed a respiratory symptom questionnaire and a depression symptom questionnaire, followed by MEG and RREP recordings of inspiratory occlusion. Transient inspiratory occlusion of 300 ms was provided randomly every 2 to 4 breaths, and approximately 80 occlusions were collected in every study participant. Participants were required to press a button for detection when they sensed occlusion. Respiratory-related evoked fields (RREFs) and RREP peaks were identified in terms of latencies and amplitudes in the right and left hemispheres. The Wilcoxon signed-rank test was further used to examine differences in peak amplitudes between the right and left hemispheres. Our results showed that inspiratory occlusion elicited RREF M1 peaks between 80 and 100 ms after triggering. Corresponding neuromagnetic responses peaked in the sensorimotor cortex, insular cortex, lateral frontal cortex, and middle frontal cortex. Overall, the RREF M1 peak amplitude in the right insula was significantly higher than that in the left insula (p = 0.038). The RREP data also showed a trend of higher N1 peak amplitudes in the right hemisphere compared to the left (p = 0.064, one-tailed). Subgroup analysis revealed that the laterality index of sensorimotor cortex activation was significantly different between higher- and lower-depressed individuals (−0.33 vs. −0.02, respectively; p = 0.028). For subjective ratings, a significant relationship was found between an individual’s depression level and their respiratory symptoms (Spearman’s rho = 0.54, p = 0.028, one-tailed). In summary, our results demonstrated that the inspiratory occlusion paradigm is feasible to elicit an RREF M1 peak with MEG. Our imaging results showed that cortical neurons were activated in the sensorimotor, frontal, middle temporal, and insular cortices for the M1 peak. Respiratory occlusion elicited higher cortical neuronal activation in the right insula compared to the left, with a higher tendency for right laterality in the sensorimotor cortex for higher-depressed rather than lower-depressed individuals. Higher levels of depression were associated with higher levels of respiratory symptoms. Future research with a larger sample size is recommended to investigate the role of emotion and laterality in cerebral neural processing of respiratory sensation.

The impact of emotional context on neural substrates of respiratory sensory gating

“…Based on the activated areas elicited by the paired inspiratory occlusion paradigm in the three conditions, it can be inferred that these brain regions, including the thalamus, hippocampus, sensorimotor cortex, temporal gyrus, frontal gyrus, and cingulate cortex, are involved in mediating respiratory gating functions. This view is consistent with our previous study (Chan et al, 2022a) and is further supported by another study examining voluntary breathing (McKay et al, 2003). Both previous studies demonstrated comparable brain activation patterns than the present study.…”

“…One set of ROIs were defined based on the between-condition contrast maps (Contrast N–F compared with Contrast P–F ). In addition, ROIs from the automated anatomical labeling (AAL) templates were chosen on the basis of previous studies to test the effects of emotional contexts on paired-occlusion elicited brain areas, which included bilateral anterior cingulate cortex, insula, middle cingulate cortex, thalamus, precentral cortex, postcentral cortex, and calcarine fissure ( Tzourio-Mazoyer et al, 2002 ; Chan et al, 2016 , 2019 , 2022b , a ).…”