A century of exercise physiology: key concepts in muscle energetics

Abstract

In the mid-nineteenth century, the concept of muscle behaving like a stretched spring was developed. This elastic model of contraction predicted that the energy available to perform work was established at the start of a contraction. Despite several studies showing evidence inconsistent with the elastic model, it persisted into the twentieth century. In 1923, W. O. Fenn published a paper in which he presented evidence that appeared to clearly refute the elastic model. Fenn showed that when a muscle performs work it produces more heat than when contracting isometrically. He proposed that energy for performing work was only made available in a muscle as and when that work was performed. However, his ideas were not adopted and it was only after 15 years of technical developments that in 1938 A. V. Hill performed experiments that conclusively disproved the elastic model and supported Fenn’s conclusions. Hill showed that the rate of heat production increased as a muscle made the transition from isometric to working contraction. Understanding the basis of the phenomenon observed by Fenn and Hill required another 40 years in which the processes that generate force and work in muscle and the associated scheme of biochemical reactions were established. Demonstration of the biochemical equivalent of Hill’s observations—changes in rate of ATP splitting when performing work—in 1999 was possible through further technical advances. The concept that the energy, from ATP splitting, required to perform work is dynamically modulated in accord with the loads a muscle encounters when contracting is key to understanding muscle energetics.

Linking Muscle Mechanics to the Metabolic Cost of Human Hopping

“…The mechanical requirements of ankle and knee musculature differed across conditions and were indicative of changes in metabolic power. The factors that are likely to contribute to increases in metabolic rate include increased average muscle force (i.e., activation requirements), and increased fascicle shortening and fascicle shortening velocity (i.e., work requirements) (Barclay, 2023;Homsher, 1972;Smith, 1972;Woledge et al, 1985). Below we explore potential contributors to changes in metabolic power with hop height and hop frequency.…”

“…Whilst we know a considerable amount about the mechanisms that drive energy expenditure in muscles during contraction (Barclay, 2023; Brooks, 2012; Woledge et al, 1985), direct measurements of muscle mechanics are essential for understanding muscle energetics during gross movements because of variability that can be attributed to the elastic function of in-series tendinous tissue. Movements that more effectively utilise tendon to recycle the work that is done upon muscle by body weight can minimise muscle activation and work requirements, which is energetically favourable (Fukunaga et al, 2001; Hof et al, 2002; Lichtwark and Wilson 2005a,b; Roberts et al, 1997).…”

Validation of a musculoskeletal model for simulating muscle mechanics and energetics during diverse human hopping tasks

“…Simulated fascicle lengths were normalized to the same values as the experimental data (L M ), and fascicle shortening and shortening velocity was calculated the same way mentioned previously. We took specific interest in the magnitudes of fascicle shortening and fascicle shortening velocity because these are what predominantly drive increases in muscle metabolic cost [30][31][32]. As per the process of normalizing the experimental EMG, simulated muscle activations were normalized to the mean simulated muscle activation within their respective session-this meant that our analysis could be performed independent of scaling factors (i.e.…”

Linking muscle mechanics to the metabolic cost of human hopping

“…Whilst we know a considerable amount about the mechanisms that drive energy expenditure in muscles during contraction ( Barclay, 2023 ; Brooks, 2012 ; Woledge et al, 1985 ), direct measurements of muscle mechanics are essential for understanding muscle energetics during gross movements because of variability that can be attributed to the elastic function of in-series tendinous tissue. Movements that more effectively utilise tendon to recycle the work that is done upon muscle by body weight can minimise muscle activation and work requirements, which is energetically favourable ( Fukunaga et al, 2001 ; Hof et al, 2002 ; Lichtwark and Wilson, 2005a , b ; Roberts et al, 1997 ).…”

“…Specifically, the function of tendon can reduce muscle activation by reducing the length change and velocity requirements of muscle contractions. Furthermore, reducing muscle shortening velocity can also further reduce the required metabolic rate associated with work production (known as the Fenn effect; Barclay, 2023 ).…”