Abstract
Certain motor activities - like walking or breathing - present the interesting property of proceeding either automatically or under voluntary control. In the case of breathing, brainstem structures located in the medulla are in charge of the automatic mode, whereas cortico-subcortical brain networks - including various frontal lobe areas - subtend the voluntary mode. We speculated that the involvement of cortical activity during voluntary breathing could impact both on the “resting state” pattern of cortical-subcortical connectivity, and on the recruitment of executive functions mediated by the frontal lobe. In order to test this prediction we explored a patient suffering from central congenital hypoventilation syndrome (CCHS), a very rare developmental condition secondary to brainstem dysfunction. Typically, CCHS patients demonstrate efficient cortically-controlled breathing while awake, but require mechanically-assisted ventilation during sleep to overcome the inability of brainstem structures to mediate automatic breathing. We used simultaneous EEG-fMRI recordings to compare patterns of brain activity between these two types of ventilation during wakefulness. As compared with spontaneous breathing (SB), mechanical ventilation (MV) restored the default mode network (DMN) associated with self-consciousness, mind-wandering, creativity and introspection in healthy subjects. SB on the other hand resulted in a specific increase of functional connectivity between brainstem and frontal lobe. Behaviorally, the patient was more efficient in cognitive tasks requiring executive control during MV than during SB, in agreement with her subjective reports in everyday life. Taken together our results provide insight into the cognitive and neural costs of spontaneous breathing in one CCHS patient, and suggest that MV during waking periods may free up frontal lobe resources, and make them available for cognitive recruitment. More generally, this study reveals how the active maintenance of cortical control over a continuous motor activity impacts on brain functioning and cognition.
Highlights
Breathing belongs to the limited number of behaviors that can operate either under an automatic or a voluntary controlled mode, and the only one in this class of which the interruption poses an immediate vital threat
We explored one patient affected with congenital central hypoventilation syndrome (CCHS) using a combination of behavioral and simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) brain-imaging measures both under spontaneous breathing (SB) and mechanical ventilation (MV) during wakefulness
In a CCHS patient, we tested the general hypothesis that the executive brain network, whose intervention is required for controlling breathing during SB, should be released and made more available for other cognitive purposes during MV
Summary
Breathing belongs to the limited number of behaviors that can operate either under an automatic or a voluntary controlled mode, and the only one in this class of which the interruption poses an immediate vital threat. The automatic mode is operated by brainstem respiratory pattern generators involving the Pre-Botzinger complex and the parafacial/retrotrapezoid nuclei located in the medulla and their associated bulbospinal neurons [1], while the controlled mode depends on the activity of a large cortico-subcortical network including notably the anterior cingulate, supplementary-motor and insular cortices, as well as other regions [2,3,4,5,6] This mapping between brainstem and automatic breathing on the one hand, and cortex and voluntary breathing on the other hand is central to our understanding of breathing, it does not inform us about the neural mechanisms at work, and about how these two modes of breathing interact. Multiple brain regions responded inappropriately to ventilatory or blood pressure challenges, including forebrain, diencephalic, and brainstem related areas such as cerebellum
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