Intramyofibrillar glycogen drives endurance exercise capacity.

Abstract

In the mid-20th century, Bergström et al. (1967) showed the world that cyclists could exercise three times as long after a high carbohydrate diet as after a low carbohydrate diet, with intermediate performance time after a mixed diet. Exercise time to exhaustion highly correlated with initial glycogen levels in the lateral portion of the quadriceps femoris. Previously, Bergström & Hultman (1966) had demonstrated using one-legged cycling that glycogen supercompensation occurred after exhausting cycling in the exercised leg but not in the leg that had rested during the exercise. Together, these studies spawned a legacy of inquiry regarding diet, glycogen and exercise which has been well-introduced and discussed by Jensen et al. (2020) in this issue of The Journal of Physiology. Given the heterogeneity of intracellular localization of glycogen in skeletal muscle fibres, key questions that arose were whether glycogen repletion after exercise would differ among the intracellular glycogen pools. Marchand et al. (2007) approached the first question by assessing glycogen repletion in vastus lateralis fibres after exhaustive cycling. Subsarcolemmal glycogen volume exceeded total myofibrillar glycogen at all time points (0–48 h) after exercise, but its rate of repletion trailed that of total myofibrillar glycogen. The intramyofibrillar pool recovered at the greatest relative rate. The authors speculated that the low initial glycogen level in the intramyofibrillar pool meant that the exercise had preferentially depleted this depot. A subsequent electron microscopy study compared depot- and fibre-type-specific glycogen use and repletion during and after a 20 km cross-country skiing time trial (Nielsen et al. 2011). Among the intermyofibrillar, intramyofibrillar and subsarcolemmal glycogen fractions, the intramyofibrillar pool suffered the greatest relative depletion during the skiing trial in type I and II fibres of triceps brachii and type I fibres of vastus lateralis. Subsarcolemmal and intermyofibrillar glycogen stores fully recovered to pre-exercise levels by 22 h after exercise independently of carbohydrate ingestion during the first 4 h after exercise. In contrast, repletion of the intramyofibrillar fraction lagged recovery of the other pools and further slackened in the absence of carbohydrate intake in the first 4 h after exercise. To address a remaining gap in the field, Jensen et al. (2020) hypothesized that intramyofibrillar glycogen would be relatively preferentially used and then repleted during and after prolonged aerobic exercise, respectively, and that exercise time-to-exhaustion would be most closely correlated to pre-exercise levels of intramyofibrillar glycogen. In homage to the pioneers of skeletal muscle glycogen research, Jensen et al. (2020) followed the diet and exercise protocol of Bergström et al. (1967). They performed fibre-typing and glycogen volume measures for vastus lateralis fibres by electron microscopy following a protocol similar to that of Nielsen et al. (2011). Intramyofibrillar glycogen volume of type I fibres before exercise and after 1 h of exercise correlated best with time to exhaustion despite having the smallest volume among the subcellular pools (Fig. 1). The subsarcolemmal glycogen fraction responded most to loading by the high carbohydrate diet. Further, the data suggest that large subsarcolemmal glycogen pools mediate sparing of intramyofibrillar glycogen in the initial hour of exercise. Standing on the shoulders of their predecessors (e.g. Bergström & Hultman, 1966; Bergström et al. 1967; Marchand et al. 2007; Nielsen et al. 2011; and others), Jensen et al. (2020) have painted an intriguing picture of depot-specific glycogen depletion and re-loading and set the stage for future discovery. Thus, they continue down the exciting trail of inquiry into diet, glycogen and exercise performance initially blazed by Bergström et al. (Bergström & Hultman, 1966; Bergström et al. 1967). None. Sole author. None.