Incompressible fluid plays a mechanical role in the development of passive muscle tension

Sleboda, David A.; Roberts, Thomas J.

doi:10.1098/rsbl.2016.0630

Cited by 47 publications

(47 citation statements)

References 18 publications

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“…Changes in muscle volume may alter the force generating potential of muscle. Studies on isolated muscles have demonstrated an increase in passive muscle tension with increased muscle fluid volume (Sleboda & Roberts, 2017). Passive muscle force at a given length changes in proportion to volume change, and a measurable change in force can be observed with volume changes as small as 5% in isolated muscles (Sleboda, Wold, & Roberts, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…In skeletal muscle, for example, fluid flows are crucial in the regulation of ion concentrations and pH, which affect muscle contraction and hence force development during exercise (Sjogaard & Saltin, 1982). In addition to the importance of muscle fluids for the biochemistry of muscle contraction, recent studies suggest that fluid plays important mechanical roles within muscle, influencing passive force development during stretch (Gindre, Takaza, Moerman, & Simms, 2013; Sleboda & Roberts, 2017), work production during active contraction (Azizi, Deslauriers, Holt, & Eaton, 2017), and dynamic changes in muscle shape that influence muscle speed and force (Azizi, Brainerd, & Roberts, 2008; Eng, Azizi, & Roberts, 2018).…”

Section: Introductionmentioning

confidence: 99%

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The time course of calf muscle fluid volume during prolonged running

et al. 2020

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Muscle fluid is essential for the biochemistry and the biomechanics of muscle contraction. Here, we provide evidence that muscle fluid volumes undergo significant changes during 75 min of moderate intensity (2.7 ± 0.4 m/s) running. Using MRI measurements at baseline and after 2.5, 5, 10, 15, 45 and 75 min, we found that the volumes of calf muscles (quantified through average cross‐sectional area) in 18 young recreational runners increase (up to 9% in the gastrocnemii) at the beginning and decrease (below baseline levels) at later stages of running. However, the intensity of changes varied between analyzed muscles. We speculate that these changes are induced by muscle activity and dehydration‐related changes in osmotic pressure gradients between intramuscular and extramuscular spaces. These findings highlight the complex nature of muscle fluid shifts during prolonged running exercise.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The time course of calf muscle fluid volume during prolonged running

et al. 2020

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“…How energy is stored during cocking remains unclear. We suspect stretching of elastic elements in muscle [31] and tendon or flexing of propodal cuticle as in stomatopod raptorial limbs [2].…”

Section: Muscle Insertion and Power Amplificationmentioning

confidence: 97%

Parallel Saltational Evolution of Ultrafast Movements in Snapping Shrimp Claws

et al. 2018

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How do stunning functional innovations evolve from unspecialized progenitors? This puzzle is particularly acute for ultrafast movements of appendages in arthropods as diverse as shrimps [1], stomatopods [2], insects [3-6], and spiders [7]. For example, the spectacular snapping claws of alpheid shrimps close so fast (∼0.5 ms) that jetted water creates a cavitation bubble and an immensely powerful snap upon bubble collapse [1]. Such extreme movements depend on (1) an energy-storage mechanism (e.g., some kind of spring) and (2) a latching mechanism to release stored energy quickly [8]. Clearly, rapid claw closure must have evolved before the ability to snap, but its evolutionary origins are unknown. Unearthing the functional mechanics of transitional stages is therefore essential to understand how such radical novel abilities arise [9-11]. We reconstructed the evolutionary history of shrimp claw form and function by sampling 114 species from 19 families, including two unrelated families within which snapping evolved independently (Alpheidae and Palaemonidae) [12, 13]. Our comparative analyses, using micro-computed tomography (microCT) and confocal imaging, high-speed video, and kinematic experiments with select 3D-printed scale models, revealed a previously unrecognized "slip joint" in non-snapping shrimp claws. This slip joint facilitated the parallel evolution of a novel energy-storage and cocking mechanism-a torque-reversal joint-an apparent precondition for snapping. Remarkably, these key functional transitions between ancestral (simple pinching) and derived (snapping) claws were achieved by minute differences in joint structure. Therefore, subtle changes in form appear to have facilitated wholly novel functional change in a saltational manner. VIDEO ABSTRACT.

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“…More recent work suggests that a drop in the force capacity of a muscle during transverse loading may relate more to changes in internal pressure resulting in changes in the lattice spacing of myofibrils (Siebert et al 2016). In addition, the development of fluid pressure inside a muscle has been shown to interact with surrounding collagen fibers to contribute to longitudinal forces (Sleboda and Roberts 2017). Continued focus on transverse loading will advance our understanding of how structures like intramuscular connective tissues, aponeuroses, adjacent muscles, or skeletal elements may influence muscle performance.…”

Section: Discussionmentioning

confidence: 99%

“…This radial expansion requires a contracting muscle fiber to interact with the collagenous network of the ECM (Purslow 1989). Recent work has also shown that an increase in muscle volume resulting in radial expansion facilitates a mechanical interaction between intramuscular fluid and the ECM, thereby contributing to the development of passive force (Sleboda and Roberts 2017). Similarly, models have shown that the radial loading of helically oriented collagen fibers of the fibers of the ECM can directly influence longitudinal force (Gindre et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Resistance to radial expansion limits muscle strain and work

Azizi

Deslauriers

Holt

et al. 2017

Biomech Model Mechanobiol

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The collagenous extracellular matrix (ECM) of skeletal muscle functions to transmit force, protect sensitive structures, and generate passive tension to resist stretch. The mechanical properties of the ECM change with age, atrophy, and neuromuscular pathologies, resulting in an increase in the relative amount of collagen and an increase in stiffness. Although numerous studies have focused on the effect of muscle fibrosis on passive muscle stiffness, few have examined how these structural changes may compromise contractile performance. Here we combine a mathematical model and experimental manipulations to examine how changes in the mechanical properties of the ECM constrain the ability of muscle fibers and fascicles to radially expand and how such a constraint may limit active muscle shortening. We model the mechanical interaction between a contracting muscle and the ECM using a constant volume, pressurized, fiber-wound cylinder. Our model shows that as the proportion of a muscle cross section made up of ECM increases, the muscle’s ability to expand radially is compromised, which in turn restricts muscle shortening. In our experiments, we use a physical constraint placed around the muscle to restrict radial expansion during a contraction. Our experimental results are consistent with model predictions and show that muscles restricted from radial expansion undergo less shortening and generate less mechanical work under identical loads and stimulation conditions. This work highlights the intimate mechanical interaction between contractile and connective tissue structures within skeletal muscle and shows how a deviation from a healthy, well-tuned relationship can compromise performance.

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Incompressible fluid plays a mechanical role in the development of passive muscle tension

Cited by 47 publications

References 18 publications

The time course of calf muscle fluid volume during prolonged running

The time course of calf muscle fluid volume during prolonged running

Parallel Saltational Evolution of Ultrafast Movements in Snapping Shrimp Claws

Resistance to radial expansion limits muscle strain and work

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