Competition for blood flow distribution between respiratory and locomotor muscles: implications for muscle fatigue

Abstract

Sympathetically induced vasoconstrictor modulation of local vasodilation occurs in contracting skeletal muscle during exercise to ensure appropriate perfusion of a large active muscle mass and to maintain also arterial blood pressure. In this synthesis, we discuss the contribution of group III-IV muscle afferents to the sympathetic modulation of blood flow distribution to locomotor and respiratory muscles during exercise. This is followed by an examination of the conditions under which diaphragm and locomotor muscle fatigue occur. Emphasis is given to those studies in humans and animal models that experimentally changed respiratory muscle work to evaluate blood flow redistribution and its effects on locomotor muscle fatigue, and conversely, those that evaluated the influence of coincident limb muscle contraction on respiratory muscle blood flow and fatigue. We propose the concept of a "two-way street of sympathetic vasoconstrictor activity" emanating from both limb and respiratory muscle metaboreceptors during exercise, which constrains blood flow and O transport thereby promoting fatigue of both sets of muscles. We end with considerations of a hierarchy of blood flow distribution during exercise between respiratory versus locomotor musculatures and the clinical implications of muscle afferent feedback influences on muscle perfusion, fatigue, and exercise tolerance.

Work of breathing influences muscle sympathetic nerve activity during semi‐recumbent cycle exercise

“…Our findings support the role of increased respiratory muscle work increasing type III/IV muscle afferent activity and influencing the subsequent integrative exercise response. Overall, our findings advance the respiratory sympathetic reflex hypothesis whereby high respiratory muscle work augments type III/IV muscle afferent activity, which in turn increases sympathetic vasomotor outflow, eliciting a redistribution of blood flow.…”

“…In addition, locomotor blood flow is influenced by Wb in those with chronic heart failure . The proposed mechanism for these changes is a sympathetically mediated redistribution of blood flow, termed the respiratory muscle metaboreflex . Imposing a high Wb is known to modulate muscle sympathetic nerve activity (MSNA, ie, sympathetic vasomotor outflow,) at rest and during mild leg cycling .…”

Diaphragm fatigue and inspiratory muscle metaboreflex in men and women matched for absolute diaphragmatic work during pressure‐threshold loading

“…Group III and IV phrenic afferent fibres are stimulated, eliciting a time-dependent increase in muscle sympathetic nerve activity (MSNA), heart rate (HR), mean arterial blood pressure (MAP) and limb vascular resistance. We have previously made the case that a global increase in sympathetic outflow under conditions of high respiratory muscle work results in a sequela of cardiovascular changes including a preferential redistribution of blood flow away from the peripheral musculature Sheel et al 2018), which is in turn directed towards respiratory muscles (Dominelli et al 2017). An important caveat to the above is that human investigations of the neurovascular effects of diaphragm fatigue have largely utilized male research participants.…”

Effect of increased inspiratory muscle work on blood flow to inactive and active limbs during submaximal dynamic exercise

“…The respiratory muscle-induced redistribution of blood flow has been termed the 'respiratory muscle metaboreflex' (Dempsey, Romer, Rodman, Miller, & Smith, 2006;Sheel, Boushel, & Dempsey, 2018). The working hypothesis is that ventilation during high-intensity exercise leads to metabolite accumulation in the diaphragm and compromised leg blood flow via a sympathetically mediated vasoconstrictor reflex.…”