Abstract
Locomotor-respiratory coupling (LRC), phase-locking between breathing and stepping rhythms, occurs in many vertebrates. When quadrupedal mammals gallop, 1∶1 stride per breath coupling is necessitated by pronounced mechanical interactions between locomotion and ventilation. Humans show more flexibility in breathing patterns during locomotion, using LRC ratios of 2∶1, 2.5∶1, 3∶1, or 4∶1 and sometimes no coupling. Previous studies provide conflicting evidence on the mechanical significance of LRC in running humans. Some studies suggest LRC improves breathing efficiency, but others suggest LRC is mechanically insignificant because ‘step-driven flows’ (ventilatory flows attributable to step-induced forces) contribute a negligible fraction of tidal volume. Yet, although step-driven flows are brief, they cause large fluctuations in ventilatory flow. Here we test the hypothesis that running humans use LRC to minimize antagonistic effects of step-driven flows on breathing. We measured locomotor-ventilatory dynamics in 14 subjects running at a self-selected speed (2.6±0.1 ms−1) and compared breathing dynamics in their naturally ‘preferred’ and ‘avoided’ entrainment patterns. Step-driven flows occurred at 1-2X step frequency with peak magnitudes of 0.97±0.45 Ls−1 (mean ±S.D). Step-driven flows varied depending on ventilatory state (high versus low lung volume), suggesting state-dependent changes in compliance and damping of thoraco-abdominal tissues. Subjects naturally preferred LRC patterns that minimized antagonistic interactions and aligned ventilatory transitions with assistive phases of the step. Ventilatory transitions initiated in ‘preferred’ phases within the step cycle occurred 2x faster than those in ‘avoided’ phases. We hypothesize that humans coordinate breathing and locomotion to minimize antagonistic loading of respiratory muscles, reduce work of breathing and minimize rate of fatigue. Future work could address the potential consequences of locomotor-ventilatory interactions for elite endurance athletes and individuals who are overweight or obese, populations in which respiratory muscle fatigue can be limiting.
Highlights
Effective ventilation is essential for sustained animal locomotion
Step-driven flows reach a large fraction of concurrent ventilatory flow, sometimes resulting in a brief midbreath reversal in flow. We suggest that these transient flows have potential to influence breathing dynamics and ventilatory muscle loading without directly driving large ventilatory volumes
Note that our calculation of locomotor driven volume (LDV) differs slightly from that used by Banzett and colleagues, who reported the fractional contribution to tidal volume per step; whereas we report the total fractional contribution to ventilation
Summary
Effective ventilation is essential for sustained animal locomotion. For many animals, including birds and mammals, this requires integrating movement and breathing so that inspiration and expiration occur during mechanically compatible periods of the locomotor cycle. Several direct mechanical links between locomotion and ventilation necessitate integration [1,2,3,4]. Sagittal bending of the trunk assists forward progression during locomotion in quadrupeds, and creates a ‘bellows’ effect, altering the pressure and volume of the abdomen and thorax. Impact loads induce inertial motions of soft-tissues (viscera, adipose), creating a ‘visceral piston’ effect, pulling and pushing on the diaphragm and body wall muscles (abdominals, intercostals) and altering thoraco-abdominal pressures. As a result of these factors, active inspiration is most compatible with a specific and different phase of the locomotor cycle than active expiration
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