Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans

Cortical and subcortical mechanosensation of breathing can be measured by short respiratory occlusions. However, the corresponding neural substrates involved in the respiratory sensation elicited by a respiratory mechanical stimulus remained unclear. Therefore, we applied the functional magnetic res...

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Main Authors: Pei-Ying S. Chan, Chia-Hsiung Cheng, Yu-Ting Wu, Changwei W. Wu, Ho-Ling A. Liu, Fu-Zen Shaw, Chia-Yih Liu, Paul W. Davenport
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-12-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2018.01804/full
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spelling doaj-718ae56fe64b407e9f4f9966e75e1be82020-11-24T21:54:51ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2018-12-01910.3389/fphys.2018.01804420871Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in HumansPei-Ying S. Chan0Pei-Ying S. Chan1Chia-Hsiung Cheng2Chia-Hsiung Cheng3Chia-Hsiung Cheng4Yu-Ting Wu5Changwei W. Wu6Changwei W. Wu7Ho-Ling A. Liu8Fu-Zen Shaw9Chia-Yih Liu10Paul W. Davenport11Department of Occupational Therapy and Healthy Aging Center, Chang Gung University, Taoyuan, TaiwanDepartment of Psychiatry, Chang Gung Memorial Hospital at Linkou, Taoyuan, TaiwanDepartment of Occupational Therapy and Healthy Aging Center, Chang Gung University, Taoyuan, TaiwanDepartment of Psychiatry, Chang Gung Memorial Hospital at Linkou, Taoyuan, TaiwanLaboratory of Brain Imaging and Neural Dynamics (BIND Lab), Chang Gung University, Taoyuan, TaiwanDepartment of Occupational Therapy and Healthy Aging Center, Chang Gung University, Taoyuan, TaiwanGraduate Institute of Mind, Brain and Consciousness, Taipei Medical University, Taipei, TaiwanBrain and Consciousness Research Center, Taipei Medical University-Shuang Ho Hospital, New Taipei, TaiwanDepartment of Imaging Physics, The University of Texas MD Anderson Cancer Center, Houston, TX, United StatesDepartment of Psychology, National Cheng-Kung University, Tainan, TaiwanDepartment of Psychiatry, Chang Gung Memorial Hospital at Linkou, Taoyuan, TaiwanDepartment of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL, United StatesCortical and subcortical mechanosensation of breathing can be measured by short respiratory occlusions. However, the corresponding neural substrates involved in the respiratory sensation elicited by a respiratory mechanical stimulus remained unclear. Therefore, we applied the functional magnetic resonance imaging (fMRI) technique to study cortical activations of respiratory mechanosensation. We hypothesized that thalamus, frontal cortex, somatosensory cortex, and inferior parietal cortex would be significantly activated in response to respiratory mechanical stimuli. We recruited 23 healthy adults to participate in our event-designed fMRI experiment. During the 12-min scan, participants breathed with a specialized face-mask. Single respiratory occlusions of 150 ms were delivered every 2–4 breaths. At least 32 successful occlusions were collected for data analysis. The results showed significant neural activations in the thalamus, supramarginal gyrus, middle frontal gyrus, inferior frontal triangularis, and caudate (AlphaSim corrected p < 0.05). In addition, subjective ratings of breathlessness were significantly correlated with the levels of neural activations in bilateral thalamus, right caudate, right supramarginal gyrus, left middle frontal gyrus, left inferior triangularis. Our results demonstrated cortical sources of respiratory sensations elicited by the inspiratory occlusion paradigm in healthy adults were located in the thalamus, supramarginal gyrus, and the middle frontal cortex, inferior frontal triangularis, suggesting subcortical, and cortical neural sources of the respiratory mechanosensation are thalamo-cortical based, especially the connections to the premotor area, middle and ventro-lateral prefrontal cortex, as well as the somatosensory association cortex. Finally, level of neural activation in thalamus is associated with the subjective rating of breathlessness, suggesting respiratory sensory information is gated at the thalamic level.https://www.frontiersin.org/article/10.3389/fphys.2018.01804/fullrespiratory sensationtransient inspiratory occlusions(fMRI ) functional magnetic resonance imagingneural correlatescortical and subcortical mapping
collection DOAJ
language English
format Article
sources DOAJ
author Pei-Ying S. Chan
Pei-Ying S. Chan
Chia-Hsiung Cheng
Chia-Hsiung Cheng
Chia-Hsiung Cheng
Yu-Ting Wu
Changwei W. Wu
Changwei W. Wu
Ho-Ling A. Liu
Fu-Zen Shaw
Chia-Yih Liu
Paul W. Davenport
spellingShingle Pei-Ying S. Chan
Pei-Ying S. Chan
Chia-Hsiung Cheng
Chia-Hsiung Cheng
Chia-Hsiung Cheng
Yu-Ting Wu
Changwei W. Wu
Changwei W. Wu
Ho-Ling A. Liu
Fu-Zen Shaw
Chia-Yih Liu
Paul W. Davenport
Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans
Frontiers in Physiology
respiratory sensation
transient inspiratory occlusions
(fMRI ) functional magnetic resonance imaging
neural correlates
cortical and subcortical mapping
author_facet Pei-Ying S. Chan
Pei-Ying S. Chan
Chia-Hsiung Cheng
Chia-Hsiung Cheng
Chia-Hsiung Cheng
Yu-Ting Wu
Changwei W. Wu
Changwei W. Wu
Ho-Ling A. Liu
Fu-Zen Shaw
Chia-Yih Liu
Paul W. Davenport
author_sort Pei-Ying S. Chan
title Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans
title_short Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans
title_full Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans
title_fullStr Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans
title_full_unstemmed Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans
title_sort cortical and subcortical neural correlates for respiratory sensation in response to transient inspiratory occlusions in humans
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2018-12-01
description Cortical and subcortical mechanosensation of breathing can be measured by short respiratory occlusions. However, the corresponding neural substrates involved in the respiratory sensation elicited by a respiratory mechanical stimulus remained unclear. Therefore, we applied the functional magnetic resonance imaging (fMRI) technique to study cortical activations of respiratory mechanosensation. We hypothesized that thalamus, frontal cortex, somatosensory cortex, and inferior parietal cortex would be significantly activated in response to respiratory mechanical stimuli. We recruited 23 healthy adults to participate in our event-designed fMRI experiment. During the 12-min scan, participants breathed with a specialized face-mask. Single respiratory occlusions of 150 ms were delivered every 2–4 breaths. At least 32 successful occlusions were collected for data analysis. The results showed significant neural activations in the thalamus, supramarginal gyrus, middle frontal gyrus, inferior frontal triangularis, and caudate (AlphaSim corrected p < 0.05). In addition, subjective ratings of breathlessness were significantly correlated with the levels of neural activations in bilateral thalamus, right caudate, right supramarginal gyrus, left middle frontal gyrus, left inferior triangularis. Our results demonstrated cortical sources of respiratory sensations elicited by the inspiratory occlusion paradigm in healthy adults were located in the thalamus, supramarginal gyrus, and the middle frontal cortex, inferior frontal triangularis, suggesting subcortical, and cortical neural sources of the respiratory mechanosensation are thalamo-cortical based, especially the connections to the premotor area, middle and ventro-lateral prefrontal cortex, as well as the somatosensory association cortex. Finally, level of neural activation in thalamus is associated with the subjective rating of breathlessness, suggesting respiratory sensory information is gated at the thalamic level.
topic respiratory sensation
transient inspiratory occlusions
(fMRI ) functional magnetic resonance imaging
neural correlates
cortical and subcortical mapping
url https://www.frontiersin.org/article/10.3389/fphys.2018.01804/full
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