Influence of endurance training on central sympathetic outflow to skeletal muscle in response to a mixed meal

Abstract

Nutrient intake is accompanied by increases in central sympathetic outflow, a response that has been mainly attributed to insulin. Insulin-mediated sympathoexcitation appears to be blunted in insulin-resistant conditions, suggesting that aside from peripheral insulin insensitivity, such conditions may also impair the central action of insulin in mediating sympathetic activation. What remains unclear is whether an insulin-sensitive state, such as that induced by chronic endurance training, alters the central sympathetic effects of insulin during postprandial conditions. To examine this question plasma insulin and glucose, muscle sympathetic nerve activity (MSNA), heart rate, and arterial blood pressure were measured in 11 high-fit [HF; peak oxygen uptake (V(O(2peak))) 65.9 +/- 1.4 ml x kg(-1) x min(-1)] and 9 average-fit (AF; V(O(2peak)) 43.6 +/- 1.3 ml x kg(-1) x min(-1)) male subjects before and for 120 min after ingestion of a mixed meal drink. As expected, the insulin response to meal ingestion was lower in HF than AF participants (insulin area under the curve(0-120): 2,314 +/- 171 vs. 4,028 +/- 460 microIU x ml(-1) x 120(-1), HF vs. AF, P < 0.05), with similar plasma glucose responses between groups. Importantly, following consumption of the meal, the HF subjects demonstrated a greater rise in MSNA compared with the AF subjects (e.g., 120 min: Delta21 +/- 1 vs. 8 +/- 3 bursts/100 heart beats, HF vs. AF, P < 0.05). Furthermore, when expressed relative to plasma insulin, HF subjects exhibited a greater change in MSNA for any given change in insulin. Arterial blood pressure responses following meal intake were similar between groups. Collectively, these data suggest that, in addition to improved peripheral insulin sensitivity, endurance training may enhance the central sympathetic effect of insulin to increase MSNA following consumption of a mixed meal.

Fig. 1.

Mean plasma glucose (A) and insulin (B) at baseline (time 0) and for 120 min following consumption of the mixed meal in the average-fit and high-fit groups, as well as the area under the curve for glucose (C) and insulin (D). Values are means ± SE. *P < 0.05 vs. average fit.

Fig. 2.

Original records from an average-fit (A) and high-fit (B) subject illustrating muscle sympathetic nerve activity (MSNA) and respiratory tracings at baseline and 120 min following consumption of the mixed meal. In response to the mixed meal, MSNA burst incidence increased 11 and 23 bursts/100 heart beats in the average-fit and high-fit subject, respectively. V, volts; AU, arbitrary units.

Fig. 3.

Mean MSNA burst incidence responses (A) at baseline (time 0) and for 120 min following consumption of the mixed meal in the average-fit and high-fit groups. Panel B shows the changes (Δ) in MSNA burst incidence from baseline in both groups. Hb, heart beats. Values are means ± SE. *P < 0.05 vs. average fit.

Fig. 4.

Group averages for the ratios relating changes from baseline in MSNA burst incidence (A) to changes in plasma insulin (Δinsulin) following mixed meal intake. Panel B shows the ratio of MSNA burst incidence area under the curve (AUC_0–120) to the insulin AUC_0–120. Values are mean ± SE. *P < 0.05 vs. average fit.