Functional magnetic resonance imaging suggests automatization of the cortical response to inspiratory threshold loading in humans

Raux, Mathieu; Tyvaert, Louise; Ferreira, M. N.; Kindler, Felix; Bardinet, Éric; Karachi, Carine; Morélot-Panzini, Capucine; Gotman, Jean; Pike, G. Bruce; Koski, Lisa; Similowski, Thomas

doi:10.1016/j.resp.2013.08.005

Cited by 58 publications

(81 citation statements)

References 66 publications

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“…They account for voluntary ventilatory capabilities and tonically contribute to the so-called “wakefulness drive to breathe” (Laviolette et al, 2013; Tremoureux et al, 2014; Dubois et al, 2016). Cortical and cortico-subcortical circuits with respiratory projections are also engaged during inspiratory load compensation (Raux et al, 2007a,b, 2013). Electroencephalographic data have evidenced premotor cortical potentials preceding inspiration (pre-inspiratory potentials) in normal individuals exposed to inspiratory constraints (Raux et al, 2007a,b).…”

Section: Introductionmentioning

confidence: 99%

“…Such potentials constitute a signature of cortical activity originating in the supplementary motor complex, which includes the supplementary motor area (SMA) (Ball et al, 1999; Shibasaki, 2012). Functional magnetic resonance imaging data (fMRI) have confirmed that inspiratory threshold loading induces complex cortical activation (Raux et al, 2013), and have shown that the spread and intensity of the corresponding respiratory-related cortical activation dramatically decrease when a discrete load (presented to the subject on a single breath basis) becomes sustained (Raux et al, 2013). These reductions in cortical activation are observed both in premotor/motor and sensory cortical areas (Raux et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Functional magnetic resonance imaging data (fMRI) have confirmed that inspiratory threshold loading induces complex cortical activation (Raux et al, 2013), and have shown that the spread and intensity of the corresponding respiratory-related cortical activation dramatically decrease when a discrete load (presented to the subject on a single breath basis) becomes sustained (Raux et al, 2013). These reductions in cortical activation are observed both in premotor/motor and sensory cortical areas (Raux et al, 2013). They have been interpreted as reflecting motor cortical reorganization and automatization (Raux et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…These reductions in cortical activation are observed both in premotor/motor and sensory cortical areas (Raux et al, 2013). They have been interpreted as reflecting motor cortical reorganization and automatization (Raux et al, 2013). They are also likely to proceed from sensory and/or affective habituation (von Leupoldt et al, 2009), that could modify not only activies in sensory areas but also in premotor/motor areas through cortico-cortical connections.…”

Section: Introductionmentioning

confidence: 99%

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Reduced Phrenic Motoneuron Recruitment during Sustained Inspiratory Threshold Loading Compared to Single-Breath Loading: A Twitch Interpolation Study

et al. 2016

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In humans, inspiratory constraints engage cortical networks involving the supplementary motor area. Functional magnetic resonance imaging (fMRI) shows that the spread and intensity of the corresponding respiratory-related cortical activation dramatically decrease when a discrete load becomes sustained. This has been interpreted as reflecting motor cortical reorganization and automatisation, but could proceed from sensory and/or affective habituation. To corroborate the existence of motor reorganization between single-breath and sustained inspiratory loading (namely changes in motor neurones recruitment), we conducted a diaphragm twitch interpolation study based on the hypothesis that motor reorganization should result in changes in the twitch interpolation slope. Fourteen healthy subjects (age: 21–40 years) were studied. Bilateral phrenic stimulation was delivered at rest, upon prepared and targeted voluntary inspiratory efforts (“vol”), upon unprepared inspiratory efforts against a single-breath inspiratory threshold load (“single-breath”), and upon sustained inspiratory efforts against the same type of load (“continuous”). The slope of the relationship between diaphragm twitch transdiaphragmatic pressure and the underlying transdiaphragmatic pressure was −1.1 ± 0.2 during “vol,” −1.5 ± 0.7 during “single-breath,” and −0.6 ± 0.4 during “continuous” (all slopes expressed in percent of baseline.percent of baseline−1) all comparisons significant at the 5% level. The contribution of the diaphragm to inspiration, as assessed by the gastric pressure to transdiaphragmatic pressure ratio, was 31 ± 17% during “vol,” 22 ± 16% during “single-breath” (p = 0.13), and 19 ± 9% during “continuous” (p = 0.0015 vs. “vol”). This study shows that the relationship between the amplitude of the transdiaphragmatic pressure produced by a diaphragm twitch and its counterpart produced by the underlying diaphragm contraction is not unequivocal. If twitch interpolation is interpreted as reflecting motoneuron recruitment, this study supports motor reorganization compatible with “diaphragm sparing” when an inspiratory threshold load becomes sustained.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Reduced Phrenic Motoneuron Recruitment during Sustained Inspiratory Threshold Loading Compared to Single-Breath Loading: A Twitch Interpolation Study

et al. 2016

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“…For instance, breathing is heavily involved in interhuman communication, as one of the markers of emotion and through the implication of the respiratory system in speech production. Finally, noxious respiratory sensations strongly involve the insular cortex (Banzett et al, 2000;Evans et al, 2002;Peiffer et al, 2001;Raux et al, 2013) that is otherwise known for its role in bodily self-consciousness (Craig, 2003;Critchley et al, 2004;Damasio, 1999).…”

Section: Introductionmentioning

confidence: 99%

Reprint of “Breathing and sense of self: Visuo-respiratory conflicts alter body self-consciousness”

Adler

Herbelin

Similowski

et al. 2014

Respiratory Physiology & Neurobiology

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a b s t r a c tBodily self-consciousness depends on the processing of interoceptive and exteroceptive signals. It can be disrupted by inducing signal conflicts. Breathing, at the crossroad between interoception and exteroception, should contribute to bodily self-consciousness. We induced visuo-respiratory conflicts in 17 subjects presented with a virtual body or a parallelepidedal object flashing synchronously or asynchronously with their breathing. A questionnaire detected illusory changes in bodily self-consciousness and breathing agency (the feeling of sensing one's breathing command). Changes in self-location were tested by measuring reaction time during mental ball drop (MBD). Synchronous illumination changed the perceived location of breathing (body: p = 0.008 vs. asynchronous; object: p = 0.013). It resulted in a significant change in breathing agency, but no changes in self-identification. This was corroborated by prolonged MBD reaction time (body: +0.045 s, 95%CI [0.013; 0.08], p = 0.007). We conclude that breathing modulates bodily self-consciousness. We also conclude that one can induce the irruption of unattended breathing into consciousness without modifying respiratory mechanics or gas exchange.

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The Effects of Respiratory Muscle Training on Resting‐State Brain Activity and Thoracic Mobility in Healthy Subjects: A Randomized Controlled Trial

Vardar-Yağlı

Sağlam

Dasgin

et al. 2022

Magnetic Resonance Imaging

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Background: Although inspiratory muscle training (IMT) is an effective intervention for improving breath perception, brain mechanisms have not been studied yet. Purpose: To examine the effects of IMT on insula and default mode network (DMN) using resting-state functional MRI (RS-fMRI). Study Type: Prospective. Population: A total of 26 healthy participants were randomly assigned to two groups as IMT group (n = 14) and sham IMT groups (n = 12). Field Strength/Sequence: A 3-T, three-dimensional T2* gradient-echo echo planar imaging sequence for RS-fMRI was obtained. Assessment: The intervention group received IMT at 60% and sham group received at 15% of maximal inspiratory pressure (MIP) for 8 weeks. Pulmonary and respiratory muscle function, and breathing patterns were measured. Groups underwent RS-fMRI before and after the treatment. Statistical Tests: Statistical tests were two-tailed P < 0.05 was considered statistically significant. Student's t test was used to compare the groups. One-sample t-test for each group was used to reveal pattern of functional connectivity. A statistical threshold of P < 0.001 uncorrected value was set at voxel level. We used False discovery rate (FDR)-corrected P < 0.05 cluster level. Results: The IMT group showed more prominent alterations in insula and DMN connectivity than sham group. The MIP was significantly different after IMT. Respiratory rate (P = 0.344), inspiratory time (P = 0.222), expiratory time (P = 1.000), and inspiratory time/total breath time (P = 0.572) of respiratory patterns showed no significant change after IMT. All DMN components showed decreased, while insula showed increased activation significantly. Data Conclusion: Differences in brain activity and connectivity may reflect improved ventilatory perception with IMT with a possible role in regulating breathing pattern by processing interoceptive signals.Evidence Level: 2 Technical Efficacy: Stage 4

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Functional magnetic resonance imaging suggests automatization of the cortical response to inspiratory threshold loading in humans

Cited by 58 publications

References 66 publications

Reduced Phrenic Motoneuron Recruitment during Sustained Inspiratory Threshold Loading Compared to Single-Breath Loading: A Twitch Interpolation Study

Reduced Phrenic Motoneuron Recruitment during Sustained Inspiratory Threshold Loading Compared to Single-Breath Loading: A Twitch Interpolation Study

Reprint of “Breathing and sense of self: Visuo-respiratory conflicts alter body self-consciousness”

The Effects of Respiratory Muscle Training on Resting‐State Brain Activity and Thoracic Mobility in Healthy Subjects: A Randomized Controlled Trial

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