The evolution of human fatigue resistance

Marino, Francesco; Sibson, Benjamin E; Lieberman, Daniel E.

doi:10.1007/s00360-022-01439-4

Cited by 7 publications

(10 citation statements)

References 111 publications

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“…The ability of skeletal muscle to adapt to internal and external perturbations is a fundamental function, indispensable for human evolution as persistence hunters 32,33 . The plasticity evoked by endurance and resistance training leads to a pleiotropic remodeling of the function of many organs beyond muscle, linked to potent health benefits 1,6,7,34,35 .…”

Section: Discussionmentioning

confidence: 99%

Molecular control of endurance training adaptation in mouse skeletal muscle

Furrer

Heim

Schmid

et al. 2023

Preprint

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Skeletal muscle has an enormous plastic potential to adapt to various external and internal perturbations. While morphological changes in endurance-trained muscles are well-described, the molecular underpinnings of training adaptation are poorly understood. We aimed at defining the molecular signature of a trained muscle and unraveling the training status-dependent responses to an acute bout of exercise. Our results reveal that even though at baseline, the transcriptomes of trained and untrained muscles are very similar, training status substantially affects the transcriptional response to an acute challenge, both quantitatively and qualitatively, in part mediated by epigenetic modifications. Second, proteomic changes were elicited by different transcriptional modalities. Finally, transiently activated factors such as the peroxisome proliferator-activated receptor gamma coactivator alpha (PGC-1alpha) are indispensable for normal training adaptation. Together, these results provide a molecular framework of the temporal and training status-dependent exercise response that defines muscle plasticity in training.

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Section: Discussionmentioning

confidence: 99%

Molecular control of endurance training adaptation in mouse skeletal muscle

Furrer

Heim

Schmid

et al. 2023

Preprint

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“…Why should muscle activation be prioritized over energy cost? One answer may be that minimizing high activations that overburden or fatigue a given muscle will likely permit longer movement duration, a performance criterion that is regarded to be fundamental to the evolution of human bipedalism and with known ecological relevance [61][62][63][64]. For instance, to effectively travel long distances in persistence hunting (regarded as a key feature of human evolution [62]) there is a clear selective advantage to resist fatigue.…”

Section: (A) Energy Expenditure Is Not Always the Principal Objective...mentioning

confidence: 99%

Humans trade off whole-body energy cost to avoid overburdening muscles while walking

et al. 2022

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Metabolic cost minimization is thought to underscore the neural control of locomotion. Yet, avoiding high muscle activation, a cause of fatigue, often outperforms energy minimization in computational predictions of human gait. Discerning the relative importance of these criteria in human walking has proved elusive, in part, because they have not been empirically decoupled. Here, we explicitly decouple whole-body metabolic cost and ‘fatigue-like' muscle activation costs (estimated from electromyography) by pitting them against one another using two distinct gait tasks. When experiencing these competing costs, participants ( n = 10) chose the task that avoided overburdening muscles (fatigue avoidance) at the expense of higher metabolic power ( p < 0.05). Muscle volume-normalized activation more closely models energy use and was also minimized by the participants' decision ( p < 0.05), demonstrating that muscle activation was, at best, an inaccurate signal for metabolic energy. Energy minimization was only observed when there was no adverse effect on muscle activation costs. By decoupling whole-body metabolic and muscle activation costs, we provide among the first empirical evidence of humans embracing non-energetic optimality in favour of a clearly defined neuromuscular objective. This finding indicates that local muscle fatigue and effort may well be key factors dictating human walking behaviour and its evolution.

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“…Why should muscle activation be prioritized over energy cost? One answer may be that minimizing high activations that overburden or fatigue a given muscle will likely permit longer movement duration, a performance criterion that is regarded to be fundamental to the evolution of human bipedalism and with known ecological relevance (61)(62)(63)(64). For instance, to effectively travel long distances in persistence hunting (regarded as a key feature of human evolution; 62) there is a clear selective advantage to resist fatigue.…”

Section: Does a 'Division Of Muscle Labor' Dictate Gait Control?mentioning

confidence: 99%

Humans trade-off whole-body energy cost to avoid overburdening muscles while walking

McDonald

Cusumano

Hieronymi

et al. 2022

Preprint

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Metabolic cost minimization is widely regarded as the principal optimality criterion that governs walking. Minimizing muscle activation has, nevertheless, outperformed energy optimization in simulating human gait and predicting certain gait behaviors. The highly coupled nature of metabolic and muscle activation costs makes it difficult to empirically discern the interrelationship between these objectives. We implemented a unique experimental design that pits metabolic cost against muscle activation costs estimated from electromyography of seven lower limb muscles. Healthy adults (N=10) selected between walking on a treadmill incline versus walking in a crouched posture (that disproportionately affected activation cost), forcing a choice between minimizing metabolic cost or activation cost. When experiencing these Competing-Cost-Pairs, participants systematically protected their activation cost at the expense of high metabolic power (19% penalty, p<0.05). This held true when activation cost was expressed as the sum of the muscle activations squared (66% saving, p<0.05) and as the maximal activation across muscles (44% saving, p<0.05), both of which penalize overburdening any individual muscle and thus indicate fatigue avoidance. Activation cost, expressed as the sum of muscle volume-normalized activation, more closely models energy use and was also protected by the participants' decision (23% saving, p<0.05) demonstrating that activation was, at best, an inaccurate proxy signal for metabolic energy. Energy minimization was only observed when there was no adverse effect on muscle activation. By decoupling metabolic and activation costs, we provide the first empirical evidence of humans embracing non-energetic optimality in favor of a clearly defined alternate neuromuscular objective.

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The evolution of human fatigue resistance

Cited by 7 publications

References 111 publications

Molecular control of endurance training adaptation in mouse skeletal muscle

Molecular control of endurance training adaptation in mouse skeletal muscle

Humans trade off whole-body energy cost to avoid overburdening muscles while walking

Humans trade-off whole-body energy cost to avoid overburdening muscles while walking

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