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Progress in Biophysics and Molecular... 2000Contractile and energetic properties of human skeletal muscle have been studied for many years in vivo in the body. It has been, however, difficult to identify the... (Review)
Review
Contractile and energetic properties of human skeletal muscle have been studied for many years in vivo in the body. It has been, however, difficult to identify the specific role of muscle fibres in modulating muscle performance. Recently it has become possible to dissect short segments of single human muscle fibres from biopsy samples and make them work in nearly physiologic conditions in vitro. At the same time, the development of molecular biology has provided a wealth of information on muscle proteins and their genes and new techniques have allowed analysis of the protein isoform composition of the same fibre segments used for functional studies. In this way the histological identification of three main human muscle fibre types (I, IIA and IIX, previously called IIB) has been followed by a precise description of molecular composition and functional and biochemical properties. It has become apparent that the expression of different protein isoforms and therefore the existence of distinct muscle fibre phenotypes is one of the main determinants of the muscle performance in vivo. The present review will first describe the mechanisms through which molecular diversity is generated and how fibre types can be identified on the basis of structural and functional characteristics. Then the molecular and functional diversity will be examined with regard to (1) the myofibrillar apparatus; (2) the sarcolemma and the sarcoplasmic reticulum; and (3) the metabolic systems devoted to producing ATP. The last section of the review will discuss the advantage that fibre diversity can offer in optimizing muscle contractile performance.
Topics: Calcium; Electrophysiology; Humans; Ion Channels; Models, Biological; Muscle Fibers, Skeletal; Muscle, Skeletal; Protein Isoforms; Temperature
PubMed: 10958931
DOI: 10.1016/s0079-6107(00)00006-7 -
Scientific Reports Jan 2021Physiological cross-sectional area (PCSA), an important biomechanical variable, is an estimate of a muscle's contractile force potential and is derived from dividing...
Physiological cross-sectional area (PCSA), an important biomechanical variable, is an estimate of a muscle's contractile force potential and is derived from dividing muscle mass by the product of a muscle's average fascicle length and a theoretical constant representing the density of mammalian skeletal muscle. This density constant is usually taken from experimental studies of small samples of several model taxa using tissues collected predominantly from the lower limbs of adult animals. The generalized application of this constant to broader analyses of mammalian myology assumes that muscle density (1) is consistent across anatomical regions and (2) is unaffected by the aging process. To investigate the validity of these assumptions, we studied muscles of rabbits (Oryctolagus cuniculus) in the largest sample heretofore investigated explicitly for these variables, and we did so from numerous anatomical regions and from three different age-cohorts. Differences in muscle density and histology as a consequence of age and anatomical region were evaluated using Tukey's HSD tests. Overall, we observed that older individuals tend to have denser muscles than younger individuals. Our findings also demonstrated significant differences in muscle density between anatomic regions within the older cohorts, though none in the youngest cohort. Approximately 50% of the variation in muscle density can be explained histologically by the average muscle fiber area and the average percent fiber area. That is, muscles with larger average fiber areas and a higher proportion of fiber area tend to be denser. Importantly, using the age and region dependent measurements of muscle density that we provide may increase the accuracy of PCSA estimations. Although we found statistically significant differences related to ontogeny and anatomical region, if density cannot be measured directly, the specific values presented herein should be used to improve accuracy. If a single muscle density constant that has been better validated than the ones presented in the previous literature is preferred, then 1.0558 and 1.0502 g/cm would be reasonable constants to use across all adult and juvenile muscles respectively.
Topics: Age Factors; Aging; Animals; Biomechanical Phenomena; Female; Forelimb; Head; Hindlimb; Male; Models, Biological; Muscle Fibers, Skeletal; Muscle, Skeletal; Rabbits; Torso
PubMed: 33483576
DOI: 10.1038/s41598-021-81489-w -
NMR in Biomedicine Mar 2017The mechanical functions of muscles involve the generation of force and the actuation of movement by shortening or lengthening under load. These functions are... (Review)
Review
The mechanical functions of muscles involve the generation of force and the actuation of movement by shortening or lengthening under load. These functions are influenced, in part, by the internal arrangement of muscle fibers with respect to the muscle's mechanical line of action. This property is known as muscle architecture. In this review, we describe the use of diffusion tensor (DT)-MRI muscle fiber tracking for the study of muscle architecture. In the first section, the importance of skeletal muscle architecture to function is discussed. In addition, traditional and complementary methods for the assessment of muscle architecture (brightness-mode ultrasound imaging and cadaver analysis) are presented. Next, DT-MRI is introduced and the structural basis for the reduced and anisotropic diffusion of water in muscle is discussed. The third section discusses issues related to the acquisition of skeletal muscle DT-MRI data and presents recommendations for optimal strategies. The fourth section discusses methods for the pre-processing of DT-MRI data, the available approaches for the calculation of the diffusion tensor and the seeding and propagating of fiber tracts, and the analysis of the tracking results to measure structural properties pertinent to muscle biomechanics. Lastly, examples are presented of how DT-MRI fiber tracking has been used to provide new insights into how muscles function, and important future research directions are highlighted. Copyright © 2016 John Wiley & Sons, Ltd.
Topics: Algorithms; Animals; Diffusion Tensor Imaging; Forecasting; Humans; Image Enhancement; Image Interpretation, Computer-Assisted; Muscle Fibers, Skeletal; Muscle, Skeletal; Reproducibility of Results; Sensitivity and Specificity
PubMed: 27257975
DOI: 10.1002/nbm.3563 -
Biological Reviews of the Cambridge... Aug 2022The size and arrangement of fibres play a determinate role in the kinetic and energetic performance of muscles. Extrapolations between fibre architecture and performance... (Review)
Review
The size and arrangement of fibres play a determinate role in the kinetic and energetic performance of muscles. Extrapolations between fibre architecture and performance underpin our understanding of how muscles function and how they are adapted to power specific motions within and across species. Here we provide a synopsis of how this 'fibre to function' paradigm has been applied to understand muscle design, performance and adaptation in animals. Our review highlights the widespread application of the fibre to function paradigm across a diverse breadth of biological disciplines but also reveals a potential and highly prevalent limitation running through past studies. Specifically, we find that quantification of muscle architectural properties is almost universally based on an extremely small number of fibre measurements. Despite the volume of research into muscle properties, across a diverse breadth of research disciplines, the fundamental assumption that a small proportion of fibre measurements can accurately represent the architectural properties of a muscle has never been quantitatively tested. Subsequently, we use a combination of medical imaging, statistical analysis, and physics-based computer simulation to address this issue for the first time. By combining diffusion tensor imaging (DTI) and deterministic fibre tractography we generated a large number of fibre measurements (>3000) rapidly for individual human lower limb muscles. Through statistical subsampling simulations of these measurements, we demonstrate that analysing a small number of fibres (n < 25) typically used in previous studies may lead to extremely large errors in the characterisation of overall muscle architectural properties such as mean fibre length and physiological cross-sectional area. Through dynamic musculoskeletal simulations of human walking and jumping, we demonstrate that recovered errors in fibre architecture characterisation have significant implications for quantitative predictions of in-vivo dynamics and muscle fibre function within a species. Furthermore, by applying data-subsampling simulations to comparisons of muscle function in humans and chimpanzees, we demonstrate that error magnitudes significantly impact both qualitative and quantitative assessment of muscle specialisation, potentially generating highly erroneous conclusions about the absolute and relative adaption of muscles across species and evolutionary transitions. Our findings have profound implications for how a broad diversity of research fields quantify muscle architecture and interpret muscle function.
Topics: Animals; Computer Simulation; Diffusion Tensor Imaging; Muscle Fibers, Skeletal; Muscle, Skeletal; Running
PubMed: 35388613
DOI: 10.1111/brv.12856 -
Anatomical Record (Hoboken, N.J. : 2007) Jun 2022Kangaroo rats (Dipodomys spp.) use specialized bipedal hopping like that of kangaroos. In contrast to kangaroos that have elastic tendons capable of storing energy,...
Kangaroo rats (Dipodomys spp.) use specialized bipedal hopping like that of kangaroos. In contrast to kangaroos that have elastic tendons capable of storing energy, kangaroo rats have inelastic tendons that are unable to store large amounts of energy. Thus, the musculature of the ankle joint provides the greatest power contribution to kangaroo rat hopping. Skeletal muscle can be characterized by several fiber types, including slow twitch (Type I) and fast twitch (Type II) fibers. Fast fibers are found in higher concentration in muscles that perform quick, dynamic movements, whereas slow fibers are found in higher proportion in muscles that perform slow, endurant movements. Using fiber type specific antibodies, we identified four pure (Types I, IIA, IIB, and IIX) and two hybrid (Types I/IIA and IIA/IIX) fiber types in six hindlimb muscles from three kangaroo rats (Dipodomys merriami) to investigate the relationship between fiber composition and hindlimb muscle function. Hindlimb muscles (except soleus) were dominated by Type IIB fibers, which were largest in cross-sectional area, and are known to be best suited for rapid and explosive movements. Oxidative Type IIA and Type IIX fibers were found at moderate concentrations and likely function in maintaining continual saltatory locomotion. Thus, kangaroo rats can use these two fiber type populations as "gears" for both endurant and explosive behaviors.
Topics: Animals; Dipodomys; Hindlimb; Immunohistochemistry; Locomotion; Muscle Fibers, Fast-Twitch; Muscle Fibers, Skeletal; Muscle Fibers, Slow-Twitch; Muscle, Skeletal; Potoroidae
PubMed: 34605198
DOI: 10.1002/ar.24791 -
Journal of Cachexia, Sarcopenia and... Aug 2017As muscle capillarization is related to the oxidative capacity of the muscle and the size of muscle fibres, capillary rarefaction may contribute to sarcopenia and... (Comparative Study)
Comparative Study
BACKGROUND
As muscle capillarization is related to the oxidative capacity of the muscle and the size of muscle fibres, capillary rarefaction may contribute to sarcopenia and functional impairment in older adults. Therefore, it is important to assess how ageing affects muscle capillarization and the interrelationship between fibre capillary supply with the oxidative capacity and size of the fibres.
METHODS
Muscle biopsies from healthy recreationally active young (22 years; 14 men and 5 women) and older (74 years; 22 men and 6 women) people were assessed for muscle capillarization and the distribution of capillaries with the method of capillary domains. Oxidative capacity of muscle fibres was assessed with quantitative histochemistry for succinate dehydrogenase (SDH) activity.
RESULTS
There was no significant age-related reduction in muscle fibre oxidative capacity. Despite 18% type II fibre atrophy (P = 0.019) and 23% fewer capillaries per fibre (P < 0.002) in the old people, there was no significant difference in capillary distribution between young and old people, irrespective of sex. The capillary supply to a fibre was primarily determined by fibre size and only to a small extent by oxidative capacity, irrespective of age and sex. Based on SDH, the maximal oxygen consumption supported by a capillary did not differ significantly between young and old people.
CONCLUSIONS
The similar quantitative and qualitative distribution of capillaries within muscle from healthy recreationally active older people and young adults indicates that the age-related capillary rarefaction, which does occur, nevertheless maintains the coupling between skeletal muscle fibre size and capillarization during healthy ageing.
Topics: Adult; Aged; Aging; Biopsy; Capillaries; Cell Size; Female; Healthy Aging; Humans; Male; Muscle Fibers, Skeletal; Muscle, Skeletal; Oxygen Consumption; Young Adult
PubMed: 28382740
DOI: 10.1002/jcsm.12194 -
The Journal of Experimental Biology Apr 2022Muscle is highly hierarchically organized, with functions shaped by genetically controlled expression of protein ensembles with different isoform profiles at the...
Muscle is highly hierarchically organized, with functions shaped by genetically controlled expression of protein ensembles with different isoform profiles at the sarcomere scale. However, it remains unclear how isoform profiles shape whole-muscle performance. We compared two mouse hindlimb muscles, the slow, relatively parallel-fibered soleus and the faster, more pennate-fibered tibialis anterior (TA), across scales: from gene regulation, isoform expression and translation speed, to force-length-velocity-power for intact muscles. Expression of myosin heavy-chain (MHC) isoforms directly corresponded with contraction velocity. The fast-twitch TA with fast MHC isoforms had faster unloaded velocities (actin sliding velocity, Vactin; peak fiber velocity, Vmax) than the slow-twitch soleus. For the soleus, Vactin was biased towards Vactin for purely slow MHC I, despite this muscle's even fast and slow MHC isoform composition. Our multi-scale results clearly identified a consistent and significant dampening in fiber shortening velocities for both muscles, underscoring an indirect correlation between Vactin and fiber Vmax that may be influenced by differences in fiber architecture, along with internal loading due to both passive and active effects. These influences correlate with the increased peak force and power in the slightly more pennate TA, leading to a broader length range of near-optimal force production. Conversely, a greater force-velocity curvature in the near-parallel fibered soleus highlights the fine-tuning by molecular-scale influences including myosin heavy and light chain expression along with whole-muscle characteristics. Our results demonstrate that the individual gene, protein and whole-fiber characteristics do not directly reflect overall muscle performance but that intricate fine-tuning across scales shapes specialized muscle function.
Topics: Animals; Mice; Muscle Contraction; Muscle Fibers, Fast-Twitch; Muscle Fibers, Slow-Twitch; Muscle, Skeletal; Myosin Heavy Chains; Myosins; Protein Isoforms; Sarcomeres
PubMed: 35288729
DOI: 10.1242/jeb.243630 -
Acta Biomaterialia Oct 2021During growth there are serious changes in the skeletal muscles to compensate for the changed requirements in terms of body weight and size. In this study, the...
During growth there are serious changes in the skeletal muscles to compensate for the changed requirements in terms of body weight and size. In this study, the age-dependent (between 21 and 100 days) mechanical and microstructural properties of rabbit soleus muscle tissue were investigated. For this purpose, morphological properties (animal mass, soleus muscle mass, tibial length) were measured at 5 different times during aging. On the other hand, fibre orientation-dependent axial and semi-confined compression experiments were realised. In addition, the essential components (muscle fibres, extracellular matrix, remaining components), dominating the microstructure of muscle tissue, were analysed. While the mechanical results show hardly any age-dependent differences, the morphological and microstructural results show clear age-dependent differences. All morphological parameters increase significantly (animal mass by 839.2%, muscle mass 1050.6%, tibial length 233.6%). In contrast, microstructural parameters change differently. The percentage of fibres (divided into slow-twitch (ST) and fast-twitch (FT) fibres) increases significantly (137.6%), while the proportions of the extracellular matrix and the remaining components (48.2% and 46.1%) decrease. At the same time, the cross-sectional area of the fibres increases significantly (697.9%). The totality of this age-dependent information provides a deeper understanding of age-related changes in muscle structure and function and may contribute to successful development and validation of growth models in the future. STATEMENT OF SIGNIFICANCE: This article reports the first comprehensive data set on age-dependent morphological (animal mass, soleus muscle mass, tibial length), mechanical (axial and semi-confined compression), and microstructural (muscle fibres, extracellular matrix, remaining components) properties of the rabbit soleus muscle. On the one hand, the results of this study contribute to the understanding of muscle mechanics and thus to understanding of load transfer mechanisms inside the muscle tissue during growth. On the other hand, these results are relevant to the fields of constitutive formulation of age-dependent muscle tissue.
Topics: Aging; Animals; Muscle Contraction; Muscle Fibers, Skeletal; Muscle, Skeletal; Rabbits
PubMed: 34343717
DOI: 10.1016/j.actbio.2021.07.066 -
Acta Biomaterialia May 2022Skeletal muscle tissue shows a clear asymmetry with regard to the passive stresses under tensile and compressive deformation, referred to as tension-compression...
Skeletal muscle tissue shows a clear asymmetry with regard to the passive stresses under tensile and compressive deformation, referred to as tension-compression asymmetry (TCA). The present study is the first one reporting on TCA at different length scales, associated with muscle tissue and muscle fibres, respectively. This allows for the first time the comparison of TCA between the tissue and one of its individual components, and thus to identify the length scale at which this phenomenon originates. Not only the passive stress-stretch characteristics were recorded, but also the volume changes during the axial tension and compression experiments. The study reveals clear differences in the characteristics of TCA between fibres and tissue. At tissue level TCA increases non-linearly with increasing deformation and the ratio of tensile to compressive stresses at the same magnitude of strain reaches a value of approximately 130 at 13.5% deformation. At fibre level instead it initially drops to a value of 6 and then rises again to a TCA of 14. At a deformation of 13.5%, the tensile stress is about 6 times higher. Thus, TCA is about 22 times more expressed at tissue than fibre scale. Moreover, the analysis of volume changes revealed little compressibility at tissue scale whereas at fibre level, especially under compressive stress, the volume decreases significantly. The data collected in this study suggests that the extracellular matrix has a distinct role in amplifying the TCA, and leads to more incompressible tissue behaviour. STATEMENT OF SIGNIFICANCE: This article analyses and compares for the first time the tension-compression asymmetry (TCA) displayed by skeletal muscle at tissue and fibre scale. In addition, the volume changes of tissue and fibre specimens with application of passive tensile and compressive loads are studied. The study identifies a key role of the extracellular matrix in establishing the mechanical response of skeletal muscle tissue: It contributes significantly to the passive stress, it is responsible for the major part of tissue-scale TCA and, most probably, prevents/balances the volume changes of muscle fibres during deformation. These new results thus shed light on the origin of TCA and provide new information to be used in microstructure-based approaches to model and simulate skeletal muscle tissue.
Topics: Biomechanical Phenomena; Muscle Fibers, Skeletal; Muscle, Skeletal; Pressure; Stress, Mechanical
PubMed: 35339701
DOI: 10.1016/j.actbio.2022.03.034 -
Experimental Physiology Apr 2024Changes in myonuclear architecture and positioning are associated with exercise adaptations and ageing. However, data on the positioning and number of myonuclei...
Changes in myonuclear architecture and positioning are associated with exercise adaptations and ageing. However, data on the positioning and number of myonuclei following exercise are inconsistent. Additionally, whether myonuclear domains (MNDs; i.e., the theoretical volume of cytoplasm within which a myonucleus is responsible for transcribing DNA) and myonuclear positioning are altered with age remains unclear. The aim of this investigation was to investigate relationships between age and activity status and myonuclear domains and positioning. Vastus lateralis muscle biopsies from younger endurance-trained (YT) and older endurance-trained (OT) individuals were compared with age-matched untrained counterparts (YU and OU; OU samples were acquired during surgical operation). Serial, optical z-slices were acquired throughout isolated muscle fibres and analysed to give three-dimensional coordinates for myonuclei and muscle fibre dimensions. The mean cross-sectional area (CSA) of muscle fibres from OU individuals was 33%-53% smaller compared with the other groups. The number of nuclei relative to fibre CSA was 90% greater in OU compared with YU muscle fibres. Additionally, scaling of MND volume with fibre size was altered in older untrained individuals. The myonuclear arrangement, in contrast, was similar across groups. Fibre CSA and most myonuclear parameters were significantly associated with age in untrained individuals, but not in trained individuals. These data indicate that regular endurance exercise throughout the lifespan might better preserve the size of muscle fibres in older age and maintain the relationship between fibre size and MND volumes. Inactivity, however, might result in reduced muscle fibre size and altered myonuclear parameters.
Topics: Humans; Aged; Muscle Fibers, Skeletal; Aging; Cell Nucleus; Quadriceps Muscle; Exercise Therapy; Muscle, Skeletal
PubMed: 38461483
DOI: 10.1113/EP091567