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.