Post-exercise recovery of contractile function and endurance in humans and mice is accelerated by heating and slowed by cooling skeletal muscle

Abstract

Key points: We investigated whether intramuscular temperature affects the acute recovery of exercise performance following fatigue-induced by endurance exercise. Mean power output was better preserved during an all-out arm-cycling exercise following a 2 h recovery period in which the upper arms were warmed to an intramuscular temperature of ̴ 38°C than when they were cooled to as low as 15°C, which suggested that recovery of exercise performance in humans is dependent on muscle temperature. Mechanisms underlying the temperature-dependent effect on recovery were studied in intact single mouse muscle fibres where we found that recovery of submaximal force and restoration of fatigue resistance was worsened by cooling (16-26°C) and improved by heating (36°C). Isolated whole mouse muscle experiments confirmed that cooling impaired muscle glycogen resynthesis. We conclude that skeletal muscle recovery from fatigue-induced by endurance exercise is impaired by cooling and improved by heating, due to changes in glycogen resynthesis rate.

Abstract: Manipulation of muscle temperature is believed to improve post-exercise recovery, with cooling being especially popular among athletes. However, it is unclear whether such temperature manipulations actually have positive effects. Accordingly, we studied the effect of muscle temperature on the acute recovery of force and fatigue resistance after endurance exercise. One hour of moderate-intensity arm cycling exercise in humans was followed by 2 h recovery in which the upper arms were either heated to 38°C, not treated (33°C), or cooled to ∼15°C. Fatigue resistance after the recovery period was assessed by performing 3 × 5 min sessions of all-out arm cycling at physiological temperature for all conditions (i.e. not heated or cooled). Power output during the all-out exercise was better maintained when muscles were heated during recovery, whereas cooling had the opposite effect. Mechanisms underlying the temperature-dependent effect on recovery were tested in mouse intact single muscle fibres, which were exposed to ∼12 min of glycogen-depleting fatiguing stimulation (350 ms tetani given at 10 s interval until force decreased to 30% of the starting force). Fibres were subsequently exposed to the same fatiguing stimulation protocol after 1-2 h of recovery at 16-36°C. Recovery of submaximal force (30 Hz), the tetanic myoplasmic free [Ca²⁺ ] (measured with the fluorescent indicator indo-1), and fatigue resistance were all impaired by cooling (16-26°C) and improved by heating (36°C). In addition, glycogen resynthesis was faster at 36°C than 26°C in whole flexor digitorum brevis muscles. We conclude that recovery from exhaustive endurance exercise is accelerated by raising and slowed by lowering muscle temperature.

Keywords: cold-water immersion; fatigue; glycogen; recovery; skeletal muscle; temperature.

Figure 1. Schematic of the exercise protocol performed in humans

Warmup at low intensity (grey bars) was followed by a 3 × 5 min all‐out exercise fatigue bout (F1) (green bars), and then 4 × 15 min of exhaustive exercise (black bars). During the subsequent 2 h recovery, subjects were given 1.1 g kg⁻¹ h⁻¹ carbohydrate at one of the three different muscle temperature conditions at each visit. After the recovery period, a warmup was followed by a second fatigue bout (F2). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 2. Decreased mean power output in humans following recovery at low muscle temperatures

Mean data (± SEM; n = 5) showing changes in lateral triceps brachii intramuscular temperature (A) and body core temperature (B) during the 2 h recovery period, and relative power (C) during the 3 × 5 min fatigue test performed before (S1–S3) and after 2 h recovery (S4–S6). ^*Main temperature effect (one‐way ANOVA, P = 0.027). Heating (red), control (black), and cooling (blue). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3. Recovery of submaximal force is temperature and glucose dependent

Mean data (± SEM) showing relative force at 30 Hz (A), 70 Hz (B), and 120 Hz (C) during 2 h recovery with glucose (5 mm) at 36°C (red), 31°C (black), 26°C (blue), 16°C (green), and without glucose (open symbols). Tetanic [Ca²⁺]_i at 30 Hz (D), 70 Hz (E), and 120 Hz (F) at 30 min of recovery. Force and [Ca²⁺]_i before the first fatigue test were set to 100% at each frequency. ^*Two‐way repeated measures ANOVA showed main temperature effect for 30 Hz force (P = 0.0001), 70 Hz force (P = 0.0001), 30 Hz tetanic [Ca²⁺]_i (P = 0.036), 70 Hz tetanic [Ca²⁺]_i (P = 0.006), and 120 Hz tetanic [Ca²⁺]_i (P = 0.002) (n = 4—11 per group). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 4. Repeated bout fatigue resistance is glucose and temperature dependent

Typical records from a single fibre fatigued with 70 Hz repeated tetani before 2 h recovery (A) and fatigued after 2 h recovery with 120 Hz tetani (B) at 31°C in the absence of glucose. Note the similar starting forces in panels A and B, and the markedly faster fatigue development in panel B. C, typical record from a control experiment with 150 Hz repeated tetani showing that the faster fatigue development in B is not caused by a higher stimulation frequency. D, mean data (± SEM) of relative endurance, expressed as the relative number of contractions performed in the first vs. second fatigue bout for fibres that recovered at 16°C (green), 26°C (blue), 31°C (black), and 36°C (red). ^*Significantly different from the number of contractions performed in the first fatigue run, (Student's paired t test, P < 0.05, n = 3–5 per group); thick horizontal line at 0% indicates no difference between the first and second fatigue bouts. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 5. Fatigue resistance is decreased after 1 h recovery at low temperature

Typical force records from a single fibre during repeated tetanic stimulation performed before (A) and after 1 h of recovery at 26°C (B), and before (C) and after 1 h of recovery at 36°C (D). Right panels show force and [Ca²⁺]_i for the first and last contractions of the fatigue runs. The line (red) indicates the mean tetanic [Ca²⁺]_i during the tetanus. E, mean data (± SEM) comparing relative fibre endurance, which is expressed as the number of contractions performed in the first vs. second fatigue test for fibres that recovered at 26°C (blue), and 36°C (red). ^*Endurance was significantly different following recovery at 26°C vs. 36°C (Student's unpaired t test, P = 0.0035, n = 6–7). F, mean data (± SEM) of the relative fatigue‐induced decline in tetanic [Ca²⁺]_i during each fatigue test. Thick horizontal line at 0% signifies no change in endurance between the first and second fatigue bouts (E) and no fatigue‐induced change in tetanic [Ca²⁺]_i (F). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 6. Glycogen resynthesis is slower at low temperature

Mean data (± SEM) of muscle glycogen content before (PRE), after (POST), and after 30 min recovery at 26°C (blue bars) and 36°C (red bars) with repeated stimulation that caused moderate (A) and severe glycogen depletion (B). One‐way ANOVA showed significant differences over time for the moderate (P = 0.0038, n = 5) and severe glycogen depletion protocol (P < 0.0001, n = 6); ^*Significantly different from PRE (P < 0.005) with Sidak's post hoc test. Muscle glycogen returned to PRE values following recovery from moderate glycogen depletion at 26°C and 36°C, whereas muscle glycogen content was restored to PRE values at 36°C but not at 26°C following the severe glycogen depletion. [Color figure can be viewed at wileyonlinelibrary.com]