Skeletal muscle vasodilatation at the onset of exercise

Abstract

The mechanism for exercise hyperaemia is a century old enigma. Much of the research on the topic has focused on the factors controlling skeletal muscle blood flow during steady-state dynamic exercise. It is likely that the factors which initiate the increase in blood flow are distinct from those which sustain the elevated blood flow. There is now convincing evidence that there is rapid vasodilatation following release of muscle contraction. Metabolic, neural and acetylcholine spillover mechanisms do not appear to explain the initial dilatation. Heretofore there has been only circumstantial evidence regarding the role of potassium released by skeletal muscle fibres. Studies which interrupt potassium-mediated dilatation are just emerging and are not conclusive. In addition, the latency of the vascular smooth muscle response to potassium makes it desirable to identify a mechanism that does not rely on diffusion of a vasoactive agent. Compression of the intramuscular arterioles during contraction could activate a mechanosensitive response by the vascular smooth muscle and/or endothelium. Recent in vitro and in vivo data support the notion that brief periods of mechanical compression elicit rapid vasodilatation. Thus, vascular compression could represent a feedforward mechanism for initiating skeletal muscle vasodilatation at the onset of exercise.

Figure 1

Muscle blood flow response to a 1 s tetanic contraction (upper panel) and mild intensity dynamic exercise (lower panel) in dogs with perivascular flowprobes implanted around the iliac artery The initiation of contraction or exercise is denoted by the arrows. From Clifford & Hellsten (2004) with permission.

Figure 2

Venous outflow following a single muscular contraction Vertical lines represent 5 s intervals. From Gaskell (1878).

Figure 3

Forearm blood flow responses to contraction and cuff inflation Forearm blood flow response averaged across 10 subjects to a single 1 s cuff inflation (CUFF), a single 1 s contraction (CONTRACTION), and a single contraction within a cuff inflation (CUFF + CONTRACTION) with arm below (A) and above (B) the heart. From Tschakovsky et al. (1996) with permission.

Figure 4

Time course of the change in transverse arteriolar diameter frollowing a single contraction of 500 ms duration at a stimulus frequency of 60 Hz Modified from Mihok & Murrant (2004).

Figure 5

Vasodilator responses to single tetanic contractions in hamster retractor muscle Data represent peak red blood cell velocity in the feed artery (FA) and peak dilatation in feed artery, first-order arteriole (1A), second-order arteriole (2A), and third order arteriole (3A). From VanTeeffelen & Segal (2006) with permission.

Figure 6

Original tracings of the mean femoral blood flow response to a 1 s contraction of the hindlimb of one dog during the K⁺ and phenylephrine infusion PE, phenylephrine. Arrows indicate the start of contraction. Note the rapid and marked increase in blood flow for all the contractions except for K⁺ infusion. From Hamann et al. (2004a).

Figure 7

Haemodynamic responses averaged over 1 s intervals at the onset of exercise under control (saline) and ganglionic blockade (hexamethonium) conditions There were no statistically significant differences in the conductance response between the two treatments at 5, 10 and 15 s of exercise. However, the conductance values were significantly elevated with ganglionic blockade at 20, 25 and 30 s of exercise (P < 0.01). From Buckwalter & Clifford (1999) with permission.

Figure 8

Summary of the blood flow response to sciatic nerve stimulation under control and neuromuscular blockade conditions Single refers to an individual 1 s sciatic nerve stimulation (30 Hz, 1 ms, 10× motor threshold). Train refers to a 30 s train of sciatic nerve of sciatic nerve stimulations (30 Hz, 1 ms, 10× motor threshold at 50% duty cycle). Following neuromuscular blockade the blood flow response to sciatic stimulation was completely abolished. From Naik et al. (1999) with permission.

Figure 9

Effect of 10⁻⁴ M ouabain on the change in diameter of transverse arterioles at 4 s across all stimulus frequencies tested *Significantly different with ouabain. From Armstrong et al. (2007).

Figure 10

Time course of vasodilatation following application of 10 mM KCl at time 0 Data are presented as means ±s.e.m. No differences were detected between vasodilatory responses of soleus (open symbols) and gastrocnemius (filled symbols) arterioles. From Wunsch et al. (2000) with permission.

Figure 11

Peak blood flow responses to a brief contraction obtained at three intensities in which the time-tension integral was held constant Despite the lack of change in work performed, blood flow was augmented in relation with contraction intensity. From Hamann et al. (2004b) with permission.

Figure 12

Effect of increases in time-tension integral Peak blood flow responses to a brief contraction obtained at three intensities in which there were graded increases in time-tension integral due to increased contraction intensity (left) and graded increases in time-tension integral due to increased contraction duration (right). From Hamann et al. (2004b) with permission.

Figure 13

Response of a single soleus feed artery to external pressure 1 × 1 signifies one pressure pulse of 1 s duration. 1 × 5 signifies one pressure pulse of 5 s duration. 5 × 1 signifies five separate 1 s pulses with 1 s between each pulse. Diameters were tracked manually by moving a cursor on the video screen. From Clifford et al. (2006).

Figure 14

Peak dilatation produced by compression of soleus feed arteries (n = 6) 1 × 1 signifies one pressure pulse of 1 s duration. 1 × 5 signifies one pressure pulse of 5 s duration. 5 × 1 signifies five separate 1 s pulses with 1 s between each pulse. *P < 0.01 compared to 1 × 1 and 1 × 5. From Clifford et al. (2006).