What's all the hype with fibre type? Selective single fibre adaptations with lifelong endurance exercise.

Abstract

Sarcopenia and deteriorating skeletal muscle function are hallmarks of ageing. Investigations into skeletal muscle adaptations – a tissue with high plasticity – have garnered immense research interest given muscle's primary role in locomotion. Given the logistical challenges of conducting long-term (i.e. several years) prospective training interventions, most studies are confined to short durations (i.e. several weeks). As such, there is a paucity of literature examining muscular adaptations to chronic exercise across the lifespan. In this issue of The Journal of Physiology, Grosicki et al. (2021) sought to fill this void in the literature by elucidating the contractile mechanics of skeletal muscle with lifelong (>50 years) endurance exercise at the whole muscle and single fibre level. Previous investigations demonstrated marked improvements in aerobic capacity, peripheral energy metabolism, skeletal muscle mass and intramyocellular lipid content (Grosicki et al. 2021). Thus, the new findings reported by Grosicki et al. (2021) for single fibre contractility build upon previous findings to produce a comprehensive profile of skeletal muscle adaptations to lifelong endurance exercise. Although this was not a prospective trial, the ability to investigate such a rare sample of individuals is intriguing and provides invaluable information on how exercise interacts with the ageing process. Grosicki et al. (2021) studied a unique all-male cohort: 21 endurance exercisers with an impressive history of aerobic fitness and competition (lifelong exercisers; LLE), 10 aged-matched old-healthy controls (OH) and 10 young-exercisers (YE). All participants underwent whole muscle strength and power testing (isometric knee extension) and a muscle biopsy of the vastus lateralis muscle to assess single muscle fibre cross-sectional area (CSA), peak force (Po), shortening velocity (Vo, Vmax), power and quality (force and power normalized to cell size) of myosin heavy chain (MHC) type I and IIa fibres. Grosicki et al. (2021) did not pursue analyses of the type IIx fibre as a result of the lack of fibres harvested. The primary finding of this investigation was that LLE MHC type I fibres were larger (25–40%), stronger (∼20%), faster (∼10%) and more powerful (∼30%) compared to OH and YE. Additionally, MHC type II fibre sizes were similar in LLE and OH but were ∼20% smaller than YE. The muscle quality (normalized to size) of MHC IIa varied between the groups with the older groups outperforming the YE (OH > LLE > YE). By contrast, at the whole muscle level for strength and power, the order was YE > LLE > OH. Regardless of mode, prolonged aerobic exercise influences MHC type I and IIa fibres, leading to an ‘endurance phenotype’. Grosicki et al. (2021) investigated a cohort who primarily engaged in running; however, a previous study demonstrated that single fibre muscle hypertrophy in both young and older adults (∼70 years old) after 12 weeks of progressive lower body cycle ergometry training. Notably, improvements in power and retention of force in MHC type I and II muscle fibres were limited to older adults (Harber et al. 2012). Similar to this short-term exercise training study, Grosicki et al. (2021) reported that LLE type I muscle fibres were greater in size (i.e. hypertrophy), Po and Vmax compared to the OH. Grosicki et al. (2021) highlighted the importance of MHC type I muscle hypertrophy to potentially offset the loss of motor units in older adults. However, LLE did not confer any benefit pertaining to type IIa fibres size, Po and Vmax compared to the OH. As a result of the lack of protective adaptations to type IIa fibres with LLE, Grosicki et al. (2021) concluded that additional resistance-based exercise may be necessary to preserve fast muscle fibre size and performance with age. To compare how different habitual training modalities influence ageing skeletal muscle, a previous cross-sectional study examined the whole muscle profile of lifelong resistance trained exercisers (∼50 years of training), lifelong endurance and age-matched untrained older adults (Aagaard et al. 2007). Similar to LLE, Aagaard et al. (2007) demonstrated that long-term resistance exercise is associated with larger MHC type I slow muscle fibres compared to muscle from less active counterparts. This finding is similar to those reported by Grosicki et al. (2021) where the LLE group exhibited larger type I muscle fibre size. Regarding MHC type II fast muscle fibres, Aagaard et al. (2007) found that the lifelong resistance-trained exercisers had a similar distribution of MHC type IIa and type IIx compared to habitually trained endurance and OH participants. However, the long-term resistance exercisers exhibited larger MHC type II fibres and a greater overall contractile rate of force development compared to the untrained OH group. Similarly, Grosicki et al. (2021) reported that LLEs had similar size type IIa fibres similar to those of OH non-exercisers. However, MHC type IIa fibre contractile function was impaired in LLE compared to OH. Habitual endurance exercise, as stated previously, appears to conserve MHC type I fibres. However, the similar MHC type IIa muscle fibre between the LLE and OH participants size and impaired type IIa fibre contractile function in LLEs reinforces that age has a more profound impact than endurance exercise for retention of size, number and fibre contractile function of MHC type IIa fibres. By contrast, lifelong resistance-trained exercisers exhibit larger MHC type IIa fibres compared to untrained OH groups (Aagaard et al. 2007). Additionally, lifelong resistance training appears to preserve whole muscle rate of force development. These findings imply that resistance training may attenuate the age-related losses of MHC IIa fibres. The gradual neurological decline with ageing muscle, which includes decreased motor unit synchronization and deterioration of individual motor unit firing frequency, can result in a reduced rate of force production. An interesting finding from Grosicki et al. (2021) was that specific tension (Po/CSA) in MHC type I was significantly lower in LLE than OH and YE. The larger CSA in LLE could explain this result because Po alone (i.e. not normalized to size) was greater in this group. Interestingly, a prior investigation in a small sample of octogenarians demonstrated greater normalized Po of MHC IIa in OH (Grosicki et al. 2016). These findings imply that quality of the remaining fibres, particularly Iia, improves with age, thus compensating for the loss of whole muscle function. However, whether there are divergent intrinsic skeletal muscle and neural interactions between LLEs and their less active counterparts remains to be examined. Additionally, in vivo, single fibres interact with neighbouring fibres and are integrated with local connective tissue, such that the co-ordination between the muscle, fascia and tendon together determine contractile quality. Collectively, with age, there are also changes in fascial thickness, tendon stiffness and sarcomere length. Therefore, a high-performing single muscle fibre that is artificially stimulated ex vivo may not be entirely reflective of the other physiological variables that work in tandem. Lastly, Grosicki et al. (2021) provide a detailed training description/history of the LLEs, altthough only hours per week for the YE group. A more complete description of their training may be more insightful to determine whether the greater MHC IIa fibres present are partially a result of the current training programme (i.e. greater intensity or inclusion of resistance training) or simply a function of youth, or a combination of the two. An inclusion of volume/intensity-matched endurance-trained and/or a less fit younger group may help discern the influence of age vs. more intense or varied exercise training. Recent work has used focused ion beam-scanning electron microscopy to elucidate a structural view of skeletal muscle that challenges classic textbook concepts. Willingham et al. (2020) observed a unified myofibrillar matrix with branching of adjacent sarcomeres, that enables force transmission along the longitudinal and lateral axes. Lateral force transmission has long been postulated, and it will be exciting to determine whether changes in the myofibrillar matrix and/or sarcomere are associated with contractile mechanics, adaptation across the lifespan and/or influenced by lifelong exercise (Willingham et al. 2020). Additionally, utilizing techniques to assess innervation/denervation of single fibres would provide further insight regarding intrinsic skeletal muscle function and neural interactions. Moreover, future studies comparing lifelong resistance and endurance training using robust ‘functional’ testing (i.e. sit-to-stand, muscular strength, balance, stair climb, etc.) would add clinical relevance. The ‘endurance phenotype’ is essential for healthy cardiovascular and metabolic ageing, although strength, power and the ability to recruit a high threshold are also critical to prevent accidental falls, comprising a significant burden in the latter decades of life. For example, Master's Olympic weightlifters had significantly greater balance and lean mass than endurance runners (Erickson et al. 2020), suggesting unique benefits of explosive, technically demanding exercises. Therefore, the use of strength training or plyometrics to preserve MHC IIa and neuromuscular function should be emphasized and pursued. The optimum training distribution for healthy ageing probably entails combining several modalities to optimize cardiovascular, metabolic, neural and muscular ageing. It will be interesting to track such individuals who habitually cross-train and explore the interplay of endurance and strength training in a large and diverse population (i.e. inclusive of male/female participants representing a variety of race/ethnic groups). With the proliferation of wearable technologies to precisely track training and monitor health in real time vs. retrospective self-reported questionnaires, we can look forward to advances of the exercise–ageing interaction in the future. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. No competing interests declared. All authors contributed equally. No funding. We thank Austin Robinson PhD, Joseph Watso PhD, McKenna Tharpe and Matthew Watson MS for providing critical feedback on a preliminary draft of the manuscript.