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Muscle Structural Assembly and Functional Consequences Marco Narici1,*, Martino Franchi1 and Constantinos Maganaris2

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Muscle Structural Assembly and Functional Consequences Marco Narici1,*, Martino Franchi1 and Constantinos Maganaris2 © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 276-284 doi:10.1242/jeb.128017 REVIEW Muscle structural assembly and functional consequences Marco Narici1,*, Martino Franchi1 and Constantinos Maganaris2 ABSTRACT appointed Professor of Surgery and Anatomy at the University The relationship between muscle structure and function has been a of Padua. Just 6 years after his appointment at Padua University, matter of investigation since the Renaissance period. Extensive use Vesalius published his treatise De Humani Corporis Fabrica of anatomical dissections and the introduction of the scientific method (1543) in seven books (Libri Septem) (Fig. 1A). In his treatise, enabled early scholars to lay the foundations of muscle physiology Vesalius gives a highly detailed description of each muscle of and biomechanics. Progression of knowledge in these disciplines led the human body, through a series of artistic illustrations of ‘ ’ ’ to the current understanding that muscle architecture, together with muscle men (Fig. 1B), attributed to Titian s pupil Jan Stephen ’ muscle fibre contractile properties, has a major influence on muscle van Calcar. Vesalius drawings and descriptions provided mechanical properties. Recently, advances in laser diffraction, optical accurate anatomical details of muscle insertions, position and microendoscopy and ultrasonography have enabled in vivo actions but not of the arrangement of muscle fibres because the investigations into the behaviour of human muscle fascicles and technique he used of engraving on woodblocks followed by printing sarcomeres with varying joint angle and muscle contraction intensity. probably did not enable him to achieve sufficient accuracy to With these technologies it has become possible to identify the length illustrate muscle fibres. region over which fascicles and sarcomeres develop maximum Such details were instead provided almost a century later (1627) isometric force in vivo as well as the operating ranges of fascicles and by Casserius (Giulio Cesare Casseri; Fig. 2A), pupil of Hieronymus ’ sarcomeres during real-life activities such as walking. Also, greater Fabricius (Girolamo Fabrici d Acquapendente), through the use of a insights into the remodelling of muscle architecture in response to different drawing technique: engraving on copper plates. Working at ’ overloading and unloading, and in ageing, have been obtained by the the Universita d Artista, at the time a branch of Padua University, use of ultrasonography; these have led to the identification of clinical Casserius was able to produce drawings based on his copper biomarkers of disuse atrophy and sarcopenia. Recent evidence also engravings that clearly showed the arrangement of muscle fibres shows that the pattern of muscle hypertrophy in response to chronic (Fig. 2B) in situ. loading is contraction-mode dependent (eccentric versus concentric), Even greater morphological details of individual muscles were as similar gains in muscle mass, but through differing addition of provided by the illustrations of the British architect Sir Christopher ’ sarcomeres in series and in parallel (as indirectly inferred from Wren, who is best known for having designed St Paul s Cathedral in ’ changes in fascicle length and pennation angle), have been found. London. In 1670 in Willis treatise De Motu Musculari,Wren These innovative observations prompted a new set of investigations produced highly detailed anatomical drawings clearly illustrating into the molecular mechanisms regulating this contraction-specific the architectural features of different muscles of the body, muscle growth. differentiating between parallel-fibred, uni-pennate, bi-pennate and multi-pennate muscles (Fig. 3). KEY WORDS: Skeletal muscle, Hypertrophy, Atrophy, Sarcopenia, However, appreciation of the functional meaning of different Muscle contraction muscle fibre arrangements seems to start only with the work of the Danish scientist Nicolaus Steno(nis) who, working under the court Introduction of the Duke of Florence, Ferdinand II de’ Medici, published in 1667 The relationship between muscle structure and function has been a the treatise Elementorum Mythologiae Specimen (Fig. 4). Steno matter of interest to anatomists and physiologists since the used geometric models to represent muscles as parallelepiped Renaissance. This period represented a new era for medical integrations of fibres and was the first to describe changes in muscle science as the fine details of the human body were revealed architecture with muscle contraction as follows: ‘dum contrabitur through the use of anatomical dissections. This enabled great musculus, anguli eius acuti siunt ampliores’ (with muscle advancement in medical knowledge as, before this period, contraction, angles that are acute become greater) (Fig. 5). A understanding of human anatomy was based on Galen’s contemporary of Steno, who was probably inspired by his work as dissection work on animals (Barbary macaques), as human well as by that of Galileo, was the Neapolitan mathematician, dissections were forbidden in ancient Rome. Many of Galen’s physicist and physiologist Giovanni Alfonso Borelli (1608–1679), assumptions on the anatomy of the human body were proved wrong often described as the father of biomechanics. In his De Motu by Andreas Vesalius, one of the greatest contemporary scholars of Animalium (1680), he applied to biology the rigorous analytical the time, who shortly after obtaining his doctorate in 1537 was methods introduced by Galileo in the field of mechanics. Borelli was the first to estimate the forces of fusiform and pennate muscles required for equilibrium in various joints and demonstrated that the 1University of Nottingham, Division of Medical Sciences and Graduate Entry levers of the musculoskeletal system magnify motion rather than Medicine, School of Medicine, Faculty of Medicine and Health Sciences, MRC- force, requiring muscles to produce forces much greater than those ARUK Centre of Excellence for Musculoskeletal Ageing Research, Derby Royal Hospital, Derby DE22 3DT, UK. 2Research Institute for Sport and Exercise opposing motion (Fig. 6). Sciences, Faculty of Science, Liverpool John Moores University, Liverpool However, the mathematical relationship between muscle L3 3AF, UK. dimensions and mechanical output was actually formalized two *Author for correspondence ([email protected]) centuries later by the German physiologist Ernst H. Weber, in his Journal of Experimental Biology 276 REVIEW Journal of Experimental Biology (2016) 219, 276-284 doi:10.1242/jeb.128017 ABFig. 1. De Humani Corporis Fabrica. (A) Portrait of the 28 year old Andreas Vasalius, taken from De Humani Corporis Fabrica (1543). (B) Illustration from this treatise showing details of the muscular system of the human body. Individual muscles are accurately represented though details of muscle fibre arrangement are missing. Reproduced as public domain images from: http:// catalogue.museogalileo.it/biography/NielsSteensen NicolasSteno.html. book titled Handwörterbuch der Physiologie (Weber, 1846), but not to all muscle fibres of pennate muscles) measured in which reports one of the very first calculations (0.836 kg cm−2)of cadavers (Haxton, 1944). Despite this limitation, the real novelty human muscle maximum isometric force normalized to cross- of Haxton’s study was that of relating the maximum force of a sectional area (estimated as volume/muscle length in cadavers). In muscle to its PCSA; this ratio is now referred to as ‘specific force’, 1944, Haxton refined the estimate of force (F) per cross-sectional a quantity that represents the intrinsic force-generating potential of area (CSA) (F/CSA, specific force) of human skeletal muscle muscle independent of muscle size. As in the plantarflexors, by correcting for moment arms, accounting for pennation, and PCSA is about 1.3-fold greater than ACSA; the average value by accurately measuring the physiological cross-sectional area of F/CSA obtained by Haxton (38.2 N cm−2)issimilarto (PCSA, i.e. the area of the cross-section of a muscle perpendicular that reported by Close (1972) for mammalian muscles to all its fibres) of the plantarflexor muscles obtained by inclusion (15–30 N cm−2). of all fibres along the muscle length (Fig. 7). Although Haxton’s Although the pioneering work of these early scholars has been measurement of PCSA in the cadaveric specimens of his study is fundamental for identifying differences in muscle structural design correct, as it accounts for the cross-section of all muscle fibres, the and for relating this to the ability to generate force and movement, PCSA of his living subjects was estimated by multiplying the information on muscle structure in living humans could only be anatomical cross-sectional area for the ratio of physiological to obtained through inference from anatomical dissections and from anatomical CSA (ACSA, which is orthogonal to the muscle belly observations on animal muscle. ABFig. 2. Tabulae Anatomicae. (A) Portrait of Giulio Cesare Casseri. (B) Illustration of a copper engraving from Casseri’s Tabulae Anatomicae showing the fine details of muscle anatomy. Contrary to Vesalius’ drawings, the technique used by Casseri enabled illustration of muscle fibres and their orientation. Reproduced as public domain images from: https:// commons.wikimedia.org/wiki/Category:Giulio_Cesare_ Casseri#/media/File:Giulio_Casserio._Line_engraving_ by_G._van_Veen._Wellcome_V0001024.jpg. Journal of Experimental
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