The passive mechanical properties of muscle
2018; American Physiological Society; Volume: 126; Issue: 5 Linguagem: Inglês
10.1152/japplphysiol.00966.2018
ISSN8750-7587
AutoresRob Herbert, Simon C. Gandevia,
Tópico(s)Prosthetics and Rehabilitation Robotics
ResumoEditorialPassive Properties of MuscleThe passive mechanical properties of muscleR. D. Herbert and S. C. GandeviaR. D. HerbertNeuroscience Research Australia (NeuRA), Sydney, AustraliaUniversity of New South Wales, Sydney, Australia and S. C. GandeviaNeuroscience Research Australia (NeuRA), Sydney, AustraliaUniversity of New South Wales, Sydney, AustraliaPublished Online:16 May 2019https://doi.org/10.1152/japplphysiol.00966.2018This is the final version - click for previous versionMoreSectionsPDF (58 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat The most remarkable property of muscles is that they can contract. So it is not surprising that most muscle physiologists study the behavior of contracting muscles. The focus on muscle contraction has meant that research into the mechanical properties of relaxed muscle has been relatively neglected.There is, however, much to be gained from studying the mechanical properties of relaxed skeletal muscles. That is because the passive properties of muscles have a central role in a diverse range of physiological and pathophysiological processes. To list just a few: Passive muscle tension resists joint motion so it places fundamental constraints on movement and motor control systems. The capacity of muscles to generate active forces is modulated by passive muscle forces. The way in which muscles deform under both passive and active conditions influences the sensitivity of muscle spindles and Golgi tendon organs to joint movement and muscle force. Passive and active muscle forces influence the behavior of mechanosensitive cells that regulate muscle growth. Excessive passive and active loading of muscles can cause tendinopathies, contusion injuries, and pressure ulcers. Muscle contracture—an abnormal increase in the passive stiffness of muscles—is a major cause of physical disability in people with common conditions such as stroke, spinal cord injury, and cerebral palsy. Interest in these phenomena and others has motivated research into the passive mechanical properties of skeletal muscles.Here we introduce a series of nine minireviews to be published in the Highlighted Topic "Passive Properties of Muscle" in this and upcoming issues of the Journal of Applied Physiology. Each minireview addresses an aspect of the passive mechanical properties of skeletal muscles. Topics include passive changes in muscle length (8), contemporary image-based methods for measuring passive mechanical properties of skeletal muscles in vivo (1), epimuscular force transmission under passive conditions (15), passive force enhancement (9), properties of titin (6), muscle thixotropy (13), mechanical properties and physiological behavior of tendon (4), adaptations of the passive properties of skeletal muscle to altered patterns of use (2), and muscle contracture in cerebral palsy (14).In the following paragraphs we explain the context from which these topics have emerged and identify important directions for research into the passive mechanical properties of skeletal muscles.ContextBy the end of the 19th century, muscle physiologists had carefully investigated the elastic properties of relaxed muscle (i.e., the relationship between passive muscle tension and muscle length) (3). Under both quasi-static and dynamic loading conditions, the relationship between passive tension and muscle length closely approximated a simple exponential function. Subsequently, with the development of single-fiber preparations early in the 20th century, it was established that single muscle fibers also have exponential passive length-tension curves (5).Even in the early days of muscle physiology it was apparent that muscles do not behave purely as elastic materials—they also exhibit viscous behaviors such as stress relaxation, creep, and hysteresis. Many attempts have been made to model these behaviors, notably using quasi-linear viscoelastic models (7), but there has been limited success in modeling the changes in passive force which accompany physiological changes in muscle length (17).A longstanding question concerns the structural basis of the elastic and viscous properties of relaxed muscle. That question appeared to have been largely answered when, in 1985, Magid and Law (16) showed that relaxed single fibers and skinned fibers from frog muscles displayed quantitatively similar material properties to relaxed whole frog muscles, a finding that implied the elastic properties of relaxed muscles are conferred by intracellular structures. An immediate suspect was titin, which forms extensible filaments that span the gaps between thick filaments and adjacent z-lines. In one of the minireviews, Freundt and Linke (6) summarize what is known about the elastic properties of the titin molecule. Freundt and Linke describe several mechanisms that can modulate the force generated by stretched titin molecules and argue that titin is ideally placed to serve as a sensor of the muscle's mechanical environment under passive and active conditions.In another minireview, Lieber and Fridén (14) challenge the view that titin is the primary determinant of the mechanical properties of relaxed skeletal muscles. They argue that the passive mechanical properties of mammalian skeletal muscles are conferred primarily by intramuscular connective tissues. If confirmed, this hypothesis would have far-reaching implications. It suggests that the intramuscular connective tissues, often considered a nuisance by physiologists studying muscle contraction, deserve greater attention.Single-fiber preparations have proved very useful in the study of mechanisms of muscle contraction. Isolation of single muscle cells removes the need to consider forces generated by adjacent cells. Perhaps that is why muscle physiologists have been inclined, at least implicitly, to assume that the tensile forces generated inside muscle cells propagate along muscle cells to tendons. One of the first serious threats to that view was provided by a series of fascinating experiments conducted by Street (18) in 1983. She demonstrated that muscle forces are transmitted from muscle cells to tendons through complex, distributed pathways. The many implications of this finding have barely begun to be investigated.Subsequently Huijing and others extended this idea to epimuscular force transmission. Huijing (12) hypothesized that forces are transmitted between muscles and adjacent structures through myofascial connections. Much of the research into epimuscular force transmission has considered the transmission of actively generated muscle forces. The minireview by Maas (15) is the first to focus specifically on epimuscular transmission of passively generated muscle forces. Maas tentatively concludes there may be functionally significant epimuscular force transmission under passive conditions.Relaxed skeletal muscles exhibit nonlinear, history-dependent behaviors in response to small perturbations. For example, D.K. Hill showed, in 1968, that when resting muscles are stretched they initially demonstrate a short-range elastic response that is followed by yielding (11). Large-amplitude stretch and release of the muscle reduces muscle stiffness, but stiffness recovers rapidly if the muscle is allowed to rest. This history dependence of muscle stiffness is referred to by physiologists as thixotropy. In their minireview, Lakie and Campbell (13) speculate that thixotropy may be conferred by several mechanisms, possibly including both mechanisms related to cross-bridge cycling and mechanisms that are independent of cross bridges.Another history-dependent phenomenon exhibited by muscle is passive force enhancement. Passive force enhancement refers to the observation that a muscle which contracts while it is stretched to a particular length subsequently exerts a higher passive force at that length than if it was passively stretched to the same length. The phenomenon must have been familiar to early muscle physiologists, but it was first systematically investigated by Herzog and colleagues (10) in 2002. Passive force enhancement is intriguing because it shows that the active and passive properties of muscles are not independent; structures that generate active force also modulate passive force. In his minireview, Herzog (9) argues that the best current explanation of residual force enhancement is that it is caused by titin bonding with actin.When muscles contract, they bulge. Less obviously, muscles also undergo changes in shape with changes in muscle length. Changes in the shape of muscles—muscle deformation—may be functionally important. The minireview by Herbert and colleagues (8) considers how muscles deform when they lengthen and shorten, and how muscle deformation can contribute to changes in muscle length. The authors speculate that fascicle shear may contribute substantially to passive changes in muscle length under physiological conditions. Fascicle shear uncouples muscle length and muscle fiber length.It is not only muscle tissue that deforms when muscles change their length. Tendons also deform, even under passive loads. The minireview by Bojsen-Møller and Magnusson (4) focuses on deformations of extramuscular tendon and aponeuroses that occur at macro- and nanostructural levels.Ultimately, we will only be able to understand the mechanisms by which architecturally complex muscles deform and undergo changes in length by integrating information about the architecture and material properties of muscles and tendons into computational models (2a, 7a, 16a).Computational models of skeletal muscles are data hungry—models must be fed data on the architecture and material properties of muscle and tendinous tissue. Contemporary muscle imaging methods can be useful here: methods such as diffusion tensor imaging can be used to reconstruct the internal architecture of whole muscles in exquisite detail, and dynamic MRI methods can be used to map how muscles deform when they change length or contract. Surprisingly, imaging methods such as elastography can also be used to estimate the material properties of muscle tissue. In their minireview, Bilston and colleagues (1) provide an overview of available methods. Data obtained using these methods will be essential for the construction and validation of continuum models of muscles.Muscles are among the most adaptable of all organs. In his minireview, Blazevich (2) draws together the findings of many experimental studies which have examined how the passive mechanical properties of muscles adapt in response to stretch and exercise. Then, in the last of the minireviews in this series, Lieber (14) discusses the maladaptations of passive properties of muscles which manifest as muscle contracture in children with cerebral palsy. He presents three seminal findings from his own laboratory: muscles with contracture contain sarcomeres that are abnormally long, the increase in stiffness of muscles with contracture is due to increases in the stiffness of the extracellular matrix, and muscles with contracture have fewer satellite cells than normal muscle.DirectionsDespite the progress highlighted in these nine minireviews, there remain important gaps in the current understanding of the passive mechanical properties of skeletal muscle. We still do not have a model that can satisfactorily predict the anisotropic viscoelastic responses of relaxed muscles to the complex small- and large-amplitude strain histories that occur under physiological conditions. An equally fundamental problem is that we still do not know whether, or under what circumstances, or how much, these behaviors are determined by intracellular structures such as cross bridges or titin filaments, or by intramuscular and extramuscular (myofascial) connective tissues. Multiscale computational models may provide a framework within which emerging experimental data can be interpreted.Relaxed muscles demonstrate an array of history-dependent behaviors. It is not known to what degree these phenomena share common mechanisms. It may be that a single mechanism could explain, for example, thixotropy and passive force enhancement and the length- and contraction-dependence of muscle fascicle slack lengths. It would be very pleasing to see some sort of unification or consolidation of the diverse history-dependent behaviors exhibited by skeletal muscle.Some of the hardest remaining problems concern how muscles adapt to their mechanical environments. What are the mechanical events that initiate these adaptations? What are the signaling pathways? Why do muscles become pathologically stiff in people with muscle contractures? These questions will provide a challenge to the next generation of researchers investigating the passive mechanical properties of muscles.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the authors.AUTHOR CONTRIBUTIONSR.D.H. drafted manuscript; R.D.H. and S.C.G. edited and revised manuscript; R.D.H. and S.C.G. approved final version of manuscript.REFERENCES1. Bilston LE, Bolsterlee B, Nordez A, Sinha S. Contemporary image-based methods for measuring passive mechanical properties of skeletal muscles in vivo. J Appl Physiol (1985). doi:10.1152/japplphysiol.00672.2018. Link | ISI | Google Scholar2. Blazevich AJ. Adaptations in the passive mechanical properties of skeletal muscle to altered patterns of use. J Appl Physiol (1985). doi:10.1152/japplphysiol.00700.2018. 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Science 230: 1280–1282, 1985. doi:10.1126/science.4071053. Crossref | PubMed | ISI | Google Scholar16a. Nash MP, Hunter PJ. Computational mechanics of the heart. From tissue structure to ventricular function. J Elasticity 61: 113–141, 2000.Crossref | ISI | Google Scholar17. Quaia C, Ying HS, Optican LM. The viscoelastic properties of passive eye muscle in primates. III: force elicited by natural elongations. PLoS One 5: e9595, 2010. doi:10.1371/journal.pone.0009595. Crossref | PubMed | ISI | Google Scholar18. Street SF. Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol 114: 346–364, 1983. doi:10.1002/jcp.1041140314. Crossref | PubMed | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: R. D. Herbert, NeuRA, Barker St., Randwick NSW 2031, Australia (e-mail: r.[email protected]edu.au). 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D. Herbert, B. Bolsterlee, and S. C. Gandevia16 May 2019 | Journal of Applied Physiology, Vol. 126, No. 5 More from this issue > Volume 126Issue 5May 2019Pages 1442-1444 Copyright & PermissionsCopyright © 2019 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00966.2018PubMed30412027History Received 2 November 2018 Accepted 7 November 2018 Published online 16 May 2019 Published in print 1 May 2019 Metrics
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