Abstract
Speech or programmed sentences must often be interrupted in order to listen to and interact with interlocutors. Among many processes that produce such complex acts, the brain must precisely adjust breathing to produce adequate phonation. The mechanism of these adjustments is multifactorial and still poorly understood. In order to selectively examine the adjustment in breath control, we recorded respiratory-related premotor cortical potentials from the scalp of human subjects while they performed a single breathing initiation or inhibition task. We found that voluntary breathing is initiated if, and only if, the cortical premotor potential activity reaches a threshold activation level. The stochastic variability in the threshold correlates to the distribution of initiation times of breathing. The data also fitted a computerized interactive race model. Modeling results confirm that this model is also as effective in respiratory modality, as it has been found to be for eye and hand movements. No modifications were required to account for respiratory cycle inhibition processes. In this overly simplified task, we showed a link between voluntary initiation and control of breathing and activity in a fronto-median region of the cerebral cortex. These results shed light on some of the physiological constraints involved in the complex mechanisms of respiration, phonation, and language.
Highlights
In vertebrate animals, the central nervous system generates a rhythmic command that drives the contraction of respiratory muscles in order to move air in and out of the lungs
Our study focused on the magnitude and timing of the frontomedian cortical premotor potential activity, examining whether its stochastic variability could account for breathing initiation time and inhibition
Our study focused on specific premotor activity potentials in the fronto-medial cortex that increase in relation to voluntary breathing (Macefield and Gandevia, 1991), loaded breathing (Raux et al, 2007), or speech breathing (Tremoureux et al, 2014b)
Summary
The central nervous system generates a rhythmic command that drives the contraction of respiratory muscles in order to move air in and out of the lungs. Cortico-subcortical cooperation in generating the neural drive to breathe has been demonstrated in patients with deficient respiratory automatism (Tremoureux et al, 2014a), in normal subjects during hypocapnia-related inhibition of the respiratory automatism (Dubois et al, 2016), in patients with inspiratory muscle weakness (Georges et al, 2016), and in patients with abnormally high inspiratory resistances (Launois et al, 2015). In all cases their electroencephalographic activity suggests involvement of the premotor cortex. In this study we pushed the argument further by testing the hypothesis of a causal involvement of the cerebral cortex in the voluntary initiation and inhibition of a single breath command, and tested it by recording respiratory-related premotor cortical potentials in the scalp of awake subjects during such maneuvres
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