The legacy of A. V. Hill's Nobel Prize winning work on muscle energetics

Barclay, Christopher John; Curtin, N. A.

doi:10.1113/jp281556

Cited by 5 publications

(4 citation statements)

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“…The definition of a Hill-type model has been continuously refined and extended since Hill’s preliminary Nobel prize-winning works (Hill, 1922; Hill, 1938; Barclay & Curtin, 2022), as detailed in SM1. A Hill-type model refers today, consistently with the terminology proposed in milestone reviews in the field (Zajac, 1989; Winters, Jack M., 1990; Epstein, 1998), to any rheological arrangement of an active force generator (FG), which builds the active muscle force, and in-series and in-parallel MT passive elements, which passively transmit force through the stretch-resisting dynamics of their constitutive material.…”

Section: Methodsmentioning

confidence: 99%

Hill-type models of skeletal muscle and neuromuscular actuators: a systematic review

Caillet

Phillips

Carty

et al. 2022

Preprint

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Backed by a century of research and development, Hill-type muscle-tendon models are extensively used for countless applications. Lacking recent reviews, the field of Hill-type modelling is however dense and hard-to-explore, with detrimental consequences on knowledge transmission, inter-study consistency, and innovation. Here we present the first systematic review of the field of Hill-type muscle-tendon modelling. It aims to clarify the literature by detailing its contents and proposing updated terminology and definitions, and discussing the state-of-the-art by identifying the latest advances, current gaps, and potential improvements in modelling muscle properties. To achieve this aim, fifty-five criteria-abiding studies were extracted using a systematic search and their Hill-type models assessed according to a completeness evaluation, which identified the modelled muscle-tendon properties, and a modelling evaluation, which considered the level of validation and reusability of the model, and attention given to its modelling strategy and calibration. It is concluded that most models (1) do not significantly advance the dated gold standards in muscle modelling and do not build upon more recent advances, (2) overlook the importance of parameter identification and tuning, (3) are not strongly validated, and (4) are not reusable in other studies. Besides providing a convenient tool supported by extensive supplementary material for understanding the literature, the results of this review open a discussion on the necessity for global recommendations in Hill-type modelling and more frequent reviews to optimize inter-study consistency, knowledge transmission and model reusability.

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Section: Methodsmentioning

confidence: 99%

Hill-type models of skeletal muscle and neuromuscular actuators: a systematic review

Caillet

Phillips

Carty

et al. 2022

Preprint

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“…The 1938 paper wasn’t Hill’s last word on the topic. After time spent on war-related activities (for descriptions, see Barclay and Curtin 2022 ; Katz 1978 ; Rall 2017 ), Hill returned to science in the late 1940s. Following further developments of his heat-measuring apparatus (Hill 1949a ), Hill showed that more energy, as both heat and work, was produced in twitches with shortening (Hill 1949b , 1953 ), correcting an earlier anomalous result (Hartree and Hill 1928a ).…”

Section: A V Hill’s Ultimate Response: Empirical Confirmation Of Fenn...mentioning

confidence: 99%

A century of exercise physiology: key concepts in muscle energetics

Barclay

2022

Eur J Appl Physiol

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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.

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“…Contemporary estimates for mitochondrial efficiency are closer to 80%, whereas that of the cross‐bridge efficiency seems to greatly depend on species and fibre type (Barclay 2017). However, in any case, and when considering the additional energy used for ion transport, the maximum overall efficiency values for human muscle are expected to be well below 30% (Barclay, 2017, 2019; Barclay & Curtin, 2022). Here, it may be emphasized that these are maximum theoretical values, that is, the maximum efficiency possible under optimal experimental conditions, which probably do not occur during whole‐body tasks such as cycling (Barclay et al., 2010).…”

Section: Introductionmentioning

confidence: 99%

Efficiency of cycling exercise: Understanding the physiology

MacDougall,

MacIntosh

2024

The Journal of Physiology

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The legacy of A. V. Hill's Nobel Prize winning work on muscle energetics

Abstract: support-information-section).

Cited by 5 publications

References 123 publications

Hill-type models of skeletal muscle and neuromuscular actuators: a systematic review

Hill-type models of skeletal muscle and neuromuscular actuators: a systematic review

A century of exercise physiology: key concepts in muscle energetics

Efficiency of cycling exercise: Understanding the physiology

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