Electroencephalographic evidence for pre‐motor cortex activation during inspiratory loading in humans

Abstract

Faced with mechanical inspiratory loading, awake animals and anaesthetized humans develop alveolar hypoventilation, whereas awake humans do defend ventilation. This points to a suprapontine compensatory mechanism instead of or in addition to the 'traditional' brainstem respiratory regulation. This study assesses the role of the cortical pre-motor representation of inspiratory muscles in this behaviour. Ten healthy subjects (age 19-34 years, three men) were studied during quiet breathing, CO 2 -stimulated breathing, inspiratory resistive loading, inspiratory threshold loading, and during self-paced voluntary sniffs. Pre-triggered ensemble averaging of Cz EEG epochs starting 2.5 s before the onset of inspiration was used to look for pre-motor activity. Pre-motor potentials were present during voluntary sniffs in all subjects (average latency (±S.D.): 1325 ± 521 ms), but also during inspiratory threshold loading (1427 ± 537 ms) and during inspiratory resistive loading (1109 ± 465 ms). Pre-motor potentials were systematically followed by motor potentials during inspiratory loading. Pre-motor potentials were lacking during quiet breathing (except in one case) and during CO 2 -stimulated breathing (except in two cases). The same pattern was observed during repeated experiments at an interval of several weeks in a subset of three subjects. The behavioural component of inspiratory loading compensation in awake humans could thus depend on higher cortical motor areas. Demonstrating a similar role of the cerebral cortex in the compensation of disease-related inspiratory loads (e.g. asthma attacks) would have important pathophysiological implications: it could for example contribute to explain why sleep is both altered and deleterious in such situations.

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

“…In our subjects, it could thus be hypothesized that visuo-respiratory stimulation, by ungating respiratory sensations, resulted in a cortical motor response and the corresponding perception. This would be similar to the description of a respiratory-related cortical activity occurring during normal, unloaded breathing in certain healthy subjects participating to inspiratory loading experiments (Raux et al, 2007;Tremoureux et al, 2014). This phenomenon has been interpreted as the result of respiratory ungating following the mere institution of breathing measurements.…”

“…Indeed, in contrast to cardiac control that is purely neurovegetative, breathing control has both vegetative and behavioural determinants. Several cortical networks allow for voluntary breathing (Gandevia et al, 1990;Gandevia and Rothwell, 1987;Macefield and Gandevia, 1991;Similowski et al, 1996) and other non-homeostatic disruptions of ventilation such as speech production (Loucks et al, 2007;Murphy et al, 1997), and are engaged during inspiratory load compensation (Raux et al, 2007). In our subjects, it could thus be hypothesized that visuo-respiratory stimulation, by ungating respiratory sensations, resulted in a cortical motor response and the corresponding perception.…”

The Pathophysiology of Respiratory Failure: Control of Breathing, Respiratory Load, and Muscle Capacity

“…Gait is considered as an automatic function, but under certain conditions, gait control becomes dependent on higher specific cortical regions and cognitive function [9]. Recent evidence suggests that the cortical networks [10, 11] engaged in response to inspiratory loading are also activated during complex motor tasks requiring cognitive input, such as gait. It is hypothesized that competition for cortical resources accounts for breathing-cognition interference [12, 13].…”

Pathophysiologie der Ateminsuffizienz: Atmungsregulation, Atemlast und Muskelkapazität

“…Gehen gilt als automatische Funktion, doch je nach Umständen können auch übergeordnete spezifische kortikale Regionen und kognitive Funktionen eingreifen [9]. Aktuelle Studien deuten darauf hin, dass die kortikalen Netzwerke [10,11], die an der Reaktion auf inspiratorische Belastung beteiligt sind, auch bei komplexen motorischen Aufgaben mit kognitivem Input aktiviert werden, zum Beispiel beim Gehen. Einer Hypothese zufolge ist der Wettbewerb um kortikale Ressourcen der Grund für die Atmungs-Kognitions-Interferenz [12,13].…”

“…Bei gesunden Personen, die ruhig atmen, ist hingegen keinerlei atmungsbezogene kortikale Aktivität zu erkennen. Der Inspiration vorausgehende Potenziale treten bei experimenteller Belastung des Atmungssystems auf und spiegeln die Aktivierung kortikal-subkortikaler Netzwerke wider, an denen auch das supplementäre motorische Areal beteiligt ist [10]. Solche Bereitschaftspotenziale wurden auch im Wachzustand bei Patienten mit schwerer OSA beobachtet und als zentraler kompensatorischer Mechanismus für eine intrinsische Belastung des Atmungssystems interpretiert (verringerte Querschnittsfläche und hochgradig kollabierbare obere Atemwege) [21].…”