Rapid vasodilation in isolated skeletal muscle arterioles: impact of branch order

Abstract

We tested the hypothesis that segmental differences in the responsiveness and time course of vasodilation to metabolic signals putatively involved in rapid onset vasodilation (ROV) at the start of exercise exist within the skeletal muscle vasculature. Cannulated first-order (1As) and third-order arterioles (3As) of the rat gastrocnemius (G) muscle were exposed to cumulative doses of KCl, acetylcholine (Ach), or adenosine (Ado). In addition, time course and magnitude of vasodilation to localized application of these agonists were determined. 1As and 3As dilated similarly to incremental doses of the agonists. Continuous monitoring of internal diameter revealed a fast and transient dilatory response to microinjections of the agonists, with an average time delay (TD) before the onset of vasodilation of 2.8 +/- 0.2 seconds (1As: 3.0 +/- 0.3 seconds and 3As: 2.6 +/- 0.3 seconds) and time-to-peak (TP) of 8.2 +/- 0.7 seconds (1As: 10.3 +/- 1 seconds and 3As:5.7 +/- 0.5 seconds). No significant differences were detected for all parameters between 1As and 3As for KCl or Ado application, while 1As had a significantly longer TP and greater peak dilation than 3As to Ach. These findings demonstrate that 1As and 3As from the rat G muscle appear to have similar responsiveness to vasoactive agonists. Furthermore, the average TD before vasodilation supports a role for metabolic signals as contributors to the ROV.

Figure 1

Schematic diagram of the proximal section of the rat gastrocnemius muscle (medial head) arteriolar tree. First-order arterioles (1As) supplying both the red and white portions and third-order arterioles (3A) within the red portion of the muscle (enclosed segments) were studied. See the text and reference for details.

Figure 2

Vasodilatory responses to cumulative exposure to potassium chloride (Panel A), acetylcholine (Panel B) or adenosine (Panel C) in both first-order (1As) and third-order (3As) arterioles. Values are means ± SE.

Figure 3

Typical diameter responses to localized application of the agonists in the vicinity of the arterioles. Potassium chloride (KCl 30mM, Panel A), Ach (1 × 10⁻⁵M, Panel B) and Ado (1 × 10⁻⁴M, Panel C) were applied via a short pressure pulse ejection from a micropipette positioned nearby. Diameter was continuously tracked by an automated tracking system. Upper traces in each panel show the responses of 1As and lower traces are representative examples of 3As. Dashed lines show the time the vasoactive agents were applied.

Figure 4

Time delay before the onset of vasodilation following localized application of KCl (30mM), Ach (1 × 10⁻⁵M) and Ado (1 × 10⁻⁴M) in 1As and 3As. Each symbol corresponds to a single arteriole (closed circles – 1As and open circles – 3As).

Figure 5

Time from baseline diameter to 50, 63, 75 and 95% of the overall diameter amplitude following localized application of KCl (30mM), Ach (1 × 10⁻⁵M) and adenosine (1 × 10⁻⁴M). *p<0.05 between 1As and 3As.

Figure 6

Absolute (panel A) and relative (panel B) changes in inner diameter in response to localized application of potassium chloride (KCl, 30mM) (1As: n = 7, 3As: n = 5), acetylcholine (Ach, 1 × 10⁻⁵M) (1As: n = 7, 3As: n = 6) and adenosine (Ado, 1 × 10⁻⁴M) (1As: n = 5, 3As: n = 5). Values are as mean ± SE. * p<0.05 between 1As and 3As. Solid bars – 1As and open bars – 3As.