scholarly journals Evidence of a tunable biological spring: elastic energy storage in aponeuroses varies with transverse strain in vivo

2019 ◽  
Vol 286 (1900) ◽  
pp. 20182764 ◽  
Author(s):  
Christopher J. Arellano ◽  
Nicolai Konow ◽  
Nicholas J. Gidmark ◽  
Thomas J. Roberts

Tendinous structures are generally thought of as biological springs that operate with a fixed stiffness, yet recent observations on the mechanical behaviour of aponeuroses (broad, sheet-like tendons) have challenged this general assumption. During in situ contractions, aponeuroses undergo changes in both length and width and changes in aponeuroses width can drive changes in longitudinal stiffness. Here, we explore if changes in aponeuroses width can modulate elastic energy (EE) storage in the longitudinal direction. We tested this idea in vivo by quantifying muscle and aponeuroses mechanical behaviour in the turkey lateral gastrocnemius during landing and jumping, activities that require rapid rates of energy dissipation and generation, respectively. We discovered that when aponeurosis width increased (as opposed to decreased), apparent longitudinal stiffness was 34% higher and the capacity of aponeuroses to store EE when stretched in the longitudinal direction was 15% lower. These data reveal that biaxial loading of aponeuroses allows for variation in tendon stiffness and energy storage for different locomotor behaviours.

1990 ◽  
Vol 259 (2) ◽  
pp. R223-R230 ◽  
Author(s):  
R. L. Marsh

The kinetic properties of muscle that could influence locomotor frequency include rate of activation, rate of cross-bridge "attachment", intrinsic shortening velocity, and rate of deactivation. The latter two mechanisms are examined using examples from high-speed running in lizards and escape swimming in scallops. During running, inertial loading and elastic energy storage probably mitigate the effects of thermal alterations in intrinsic muscle shortening velocity. The result is a rather low thermal dependence of stride frequency over a 15-20 degree C temperature range. However, at lower temperatures, the longer times required for deactivation cause the thermal dependence of frequency to increase greatly. Scallops use a single muscle to swim by jet propulsion. In vivo shortening velocity in these animals also shows a low thermal dependence. As with high-speed running, the mechanics of jet propulsion may limit the effects of thermally induced changes in intrinsic shortening velocity. The largest thermal effect during swimming is on the initial phase of valve opening. The effects of temperature on the rate of deactivation of the adductor muscle could play an important role in limiting reextension of the muscle, which is dependent on elastic energy storage in the hinge ligament. These examples illustrate that the relative importance of various intrinsic contractile properties in controlling locomotor performance depends on the mechanics of the movements.


1990 ◽  
Vol 68 (3) ◽  
pp. 1033-1040 ◽  
Author(s):  
R. E. Shadwick

We investigated the possibility that tendons that normally experience relatively high stresses and function as springs during locomotion, such as digital flexors, might develop different mechanical properties from those that experience only relatively low stresses, such as digital extensors. At birth the digital flexor and extensor tendons of pigs have identical mechanical properties, exhibiting higher extensibility and mechanical hysteresis and lower elastic modulus, tensile strength, and elastic energy storage capability than adult tendons. With growth and aging these tendons become much stronger, stiffer, less extensible, and more resilient than at birth. Furthermore, these alterations in elastic properties occur to a significantly greater degree in the high-load-bearing flexors than in the low-stress extensors. At maturity the pig digital flexor tendons have twice the tensile strength and elastic modulus but only half the strain energy dissipation of the corresponding extensor tendons. A morphometric analysis of the digital muscles provides an estimate of maximal in vivo tendon stresses and suggests that the muscle-tendon unit of the digital flexor is designed to function as an elastic energy storage element whereas that of the digital extensor is not. Thus the differences in material properties between mature flexor and extensor tendons are correlated with their physiological functions, i.e., the flexor is much better suited to act as an effective biological spring than is the extensor.


1994 ◽  
Vol 266 (3) ◽  
pp. R1022-R1031 ◽  
Author(s):  
C. M. Pollock ◽  
R. E. Shadwick

This paper considers the structural properties of muscle-tendon units in the hindlimbs of mammals as a function of body mass. Morphometric analysis of the ankle extensors, digital flexors, and digital extensors from 35 quadrupedal species, ranging in body mass from 0.04 to 545 kg, was carried out. Tendon dimensions scale nearly isometrically, as does muscle mass. The negative allometry of muscle fiber length results in positive allometric scaling of muscle cross-sectional areas in all but digital extensors. Maximum muscle forces are predicted to increase allometrically, with mass exponents as high as 0.91 in the plantaris, but nearly isometrically (0.69) in the digital extensors. Thus the maximum amount of stress a tendon may experience in vivo, as indicated by the ratio of muscle and tendon cross-sectional areas, increases with body mass in digital flexors and ankle extensors. Consequently, the capacity for elastic energy storage scales with positive allometry in these tendons but is isometric in the digital extensors, which probably do not function as springs in normal locomotion. These results suggest that the springlike tendons of large mammals can potentially store more elastic strain energy than those of smaller mammals because their disproportionately stronger muscles can impose higher tendon stresses.


Author(s):  
Brooke A. Christensen ◽  
David C. Lin ◽  
M. Janneke Schwaner ◽  
Craig P. McGowan

Small bipedal hoppers, including kangaroo rats, are thought to not benefit from substantial elastic energy storage and return during hopping. However, recent species-specific material properties research suggests that, despite relative thickness, the ankle extensor tendons of these small hoppers are considerably more compliant than had been assumed. With faster locomotor speeds demanding higher forces, a lower tendon stiffness suggests greater tendon deformation and thus a greater potential for elastic energy storage and return with increasing speed. Using the elastic modulus values specific to kangaroo rat tendons, we sought to determine how much elastic energy is stored and returned during hopping across a range of speeds. In vivo techniques were used to record tendon force in the ankle extensors during steady-speed hopping. Our data support the hypothesis that the ankle extensor tendons of kangaroo rats store and return elastic energy in relation to hopping speed, storing more at faster speeds. Despite storing comparatively less elastic energy than larger hoppers, this relationship between speed and energy storage offer novel evidence of a functionally similar energy storage mechanism, operating irrespective of body size or tendon thickness, across the distal muscle-tendon units of both small and large bipedal hoppers.


Author(s):  
Paul Hulme ◽  
Sabina Bruehlmann ◽  
Neil A. Duncan

The intervertebral disc (IVD) is a “hydrostatic load-bearing structure” [1], found between the vertebral bodies of the spine. The IVD is composed of the inner and outer annulus fibrosus and a gelatinous center, the nucleus pulposus. Fluid is the largest component of the IVD. Swelling affects the macroscopic mechanical response of the tissue, as well as the microscopic nutrient and solute transport to the cells of the IVD. Previous studies describing the macroscopic swelling behaviour of the annulus fibrosus have been uniaxial in nature [2,3]. However, the behaviour of the annulus is markedly affected by its geometry [3]. By examining a biaxial section of annulus fibrosus with a portion of the bone attachment present, the structure of the annular test section will be maintained and by inference so should its function [4]. Therefore, the objective of this study was to develop an apparatus to investigate simultaneously both the macroscopic and microscopic swelling behaviour of the annulus fibrosus subjected to realistic biaxial loading. The biaxial loading device should maintain the annulus fibrosus in vivo geometry and environment, monitor stress and control tissue strain, while positioning the tissue in a manner that allows for in situ visualization of the cells.


1986 ◽  
Vol 250 (1) ◽  
pp. R56-R64 ◽  
Author(s):  
J. G. Tidball ◽  
T. L. Daniel

The capability of heavy meromyosin (HMM) to store energy in reversible deformations has been investigated previously; yet, whether HMM is the site of most elastic energy storage in skeletal muscle cells has not been established. We conducted dynamic loading tests on single rigored muscle cells over the physiological range of sarcomere lengths. These tests enabled us to calculate the energy stored in reversible deformations or dissipated in the cell during each cycle of oscillation. Our findings show that these cells are capable of storing approximately 0.5 J . kg-1 of elastic energy during the last 50 ms of passive extension in vivo by agonists and before their own active contraction. Possible sites of this energy storage are HMM subunit 2, the proximal portion of HMM subunit 1, and parallel structures. However, energy storage increases monotonically as myofilament overlap decreases in the physiological range. This negative correlation suggests that HMM subunits are not the primary sites of elastic energy storage. Our electron-microscopic observations show that collagen fibrils at the cell's surface become oriented parallel to the cell's long axis over the range of sarcomere lengths where energy storage increases. This provides a mechanism for the observed increases in elastic energy storage.


1995 ◽  
Vol 198 (9) ◽  
pp. 1829-1841 ◽  
Author(s):  
A Biewener ◽  
R Baudinette

In order to evaluate the role of elastic energy recovery in the hopping of macropodids, in vivo measurements of muscle­tendon forces using buckle force transducers attached to the tendons of the gastrocnemius (G), plantaris (PL) and flexor digitorum longus (FDL) of tammar wallabies were made as the animals hopped on a treadmill at speeds ranging from 2.1 to 6.3 m s-1. These muscles and tendons constitute the main structures that are most important in energy storage and recovery. Electromyographic recordings from the lateral gastrocnemius and plantaris muscles, together with high-speed films (200 frames s-1) and video (60 fields s-1), were also used to correlate muscle activation and kinematic patterns of limb movement with force development. On the basis of in situ calibrations of the buckle transducers, we found that muscle forces and elastic energy storage increased with increased hopping speed in all three muscle­tendon units. Elastic energy recovery reached a maximum of 25 % of metabolic energy expenditure at 6.3 m s-1 and is probably greater than this at higher speeds. Force sharing among the three muscles was consistently maintained over this range of speeds in terms of recruitment. Although forces and stresses were generally comparable within the gastrocnemius and plantaris muscles, maximal tendon stresses were considerably greater in the gastrocnemius, because of its smaller cross-sectional area (peak muscle stress: 227 versus 262 kPa; peak tendon stress: 36 versus 32 MPa, G versus PL). As a result, energy storage was greatest in the gastrocnemius tendon despite its much shorter length, which limits its volume and, hence, energy storage capacity, compared with PL and FDL tendons. Forces and stresses (17 MPa maximum) developed within the FDL tendon were consistently much lower than those for the other two tendons. Peak stresses in these three tendons indicated safety factors of 3.0 for G, 3.3 for PL and 6.0 for FDL. The lower stresses developed within the tendons of the plantaris and, especially, the flexor digitorum longus may indicate the need to maintain sufficient stiffness for phalangeal control of foot placement, at the expense of reduced strain energy recovery.


Author(s):  
D. Reis ◽  
B. Vian ◽  
J. C. Roland

Wall morphogenesis in higher plants is a problem still open to controversy. Until now the possibility of a transmembrane control and the involvement of microtubules were mostly envisaged. Self-assembly processes have been observed in the case of walls of Chlamydomonas and bacteria. Spontaneous gelling interactions between xanthan and galactomannan from Ceratonia have been analyzed very recently. The present work provides indications that some processes of spontaneous aggregation could occur in higher plants during the formation and expansion of cell wall.Observations were performed on hypocotyl of mung bean (Phaseolus aureus) for which growth characteristics and wall composition have been previously defined.In situ, the walls of actively growing cells (primary walls) show an ordered three-dimensional organization (fig. 1). The wall is typically polylamellate with multifibrillar layers alternately transverse and longitudinal. Between these layers intermediate strata exist in which the orientation of microfibrils progressively rotates. Thus a progressive change in the morphogenetic activity occurs.


Author(s):  
Greg V. Martin ◽  
Ann L. Hubbard

The microtubule (MT) cytoskeleton is necessary for many of the polarized functions of hepatocytes. Among the functions dependent on the MT-based cytoskeleton are polarized secretion of proteins, delivery of endocytosed material to lysosomes, and transcytosis of integral plasma membrane (PM) proteins. Although microtubules have been shown to be crucial to the establishment and maintenance of functional and structural polarization in the hepatocyte, little is known about the architecture of the hepatocyte MT cytoskeleton in vivo, particularly with regard to its relationship to PM domains and membranous organelles. Using an in situ extraction technique that preserves both microtubules and cellular membranes, we have developed a protocol for immunofluorescent co-localization of cytoskeletal elements and integral membrane proteins within 20 µm cryosections of fixed rat liver. Computer-aided 3D reconstruction of multi-spectral confocal microscope images was used to visualize the spatial relationships among the MT cytoskeleton, PM domains and intracellular organelles.


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