Length-force characteristics of the aponeurosis in the passive and active muscle condition and in the isolated condition

doi:10.1016/0021-9290(94)90020-5

Journal of Biomechanics

Volume 27, Issue 4, April 1994, Pages 445-453

https://doi.org/10.1016/0021-9290(94)90020-5 Get rights and content

Abstract

Length behaviour of the entire and designated parts of the proximal aponeurosis of the unipennate gastrocnemius medialis (GM) muscle of the rat was examined at muscle lengths ranging form muscle slack length to 4 mm above muscle optimum length in the passive and active (isometric contractions) muscle condition (n = 13). In addition, length-force characteristics of the aponeurosis in the isolated condition were determined (n = 6). Going from muscle slack length to 4 mm above muscle optimum length, the relative extension (relative to the length at muscle slack length) yielded the following results: 14.3% for the entire aponeurosis, 9.8% for the most proximal 25% of the aponeurosis, 3–5% for the middle 50% of the aponeurosis and 52.3% for the most distal 25% of the aponeurosis. Aponeurosis length as a function of aponeurosis force was significantly shorter in the active compared to the passive or isolated condition for force values within the range of force encountered in all three conditions (0.3–1.0 N); no significant difference was observed between the passive or isolated condition. It is concluded that the extension of the aponeurosis is heterogeneously distributed along its length. Differences in aponeurosis length-force curves between the conditions may be explained in terms of a heterogeneous force distribution within the muscle.

References (32)

M.G. Banus et al.
The relation of isometric tension to length in skeletal muscle
J. Cell. Comp. Physiol.
(1938)
D.L. Butler et al.
C. Casella
Tensile force in total striated muscle, isolated fibre and sarcolemma
Acta Physiol. Scand.
(1950)
G.J.C. Ettema
Series elastic properties and architecture of skeletal muscle in isometric and dynamic contractions
G.J.C. Ettema et al.
Properties of the tendinous structures and series elastic component of EDL muscle-tendon complex of the rat
J. Biomechanics
(1989)
G.J.C. Ettema et al.
The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions
J. exp. Biol.
(1990)
R.I. Griffiths
Shortening of muscle fibres during stretch of the active medial gastrocnemius muscle: the role of tendon compliance
J. Physiol.
(1991)
J.W. Heslinga et al.
Effects of growth on architecture and functional characteristics of adult rat gastrocnemius muscle
J. Morphol.
(1990)
A.V. Hill
The series elastic component of muscle
J.A. Hoffer et al.
Roles of muscle activity and load on the relationship between spindle length and whole muscle length in the freely walking cat

R. Horowits et al.

A physiological role for titin and nebulin in skeletal muscle

Nature

(1986)

P.A. Huijing et al.

Length-force characteristics of aponeurosis in passive muscle and during isometric and slow dynamic contractions of rat gastrocnemius muscle

Acta Morphol. Neerl.-Scand.

(1988/1989)

J.L. van Leeuwen

Muscle function in locomotion

R.L. Lieber et al.

Frog semitendinosus tendon load-strain and stress-strain properties during passive loading

Am. J. Physiol.

(1991)

A. Magid et al.

Myofibrils bear most of the resting tension in frog skeletal muscle

Science

(1985)

D.L. Morgan et al.

Measuring the compliance of intact tendon: a comparison of methods

Cited by (113)

Influence of muscle length on the three-dimensional architecture and aponeurosis dimensions of rabbit calf muscles
2024, Journal of the Mechanical Behavior of Biomedical Materials
The function of a muscle is highly dependent on its architecture, which is characterized by the length, pennation, and curvature of the fascicles, and the geometry of the aponeuroses. During in vivo function, muscles regularly undergo changes in length, thereby altering their architecture. During passive muscle lengthening, fascicle length (FL) generally increases and the angle of fascicle pennation (FP) and the fascicle curvature (FC) decrease, while the aponeuroses increase in length but decrease in width.
Muscles are differently structured, making their change during muscle lengthening complex and multifaceted. To obtain comprehensive data on architectural changes in muscles during passive length, the present study determined the three-dimensional fascicle geometry of rabbit M. gastrocnemius medialis (GM), M. gastrocnemius lateralis (GL), and M. plantaris (PLA). For this purpose, the left and right legs of three rabbits were histologically fixed at targeted ankle joint angles of 95° (short muscle length [SML]) and 60° (long muscle length [LML]), respectively, and the fascicles were tracked by manual three-dimensional digitization. In a second set of experiments, the GM aponeurosis dimensions of ten legs from five rabbits were determined at varying muscle lengths via optical marker tracking.
The GM consisted of a uni-pennated compartment, whereas the GL and PLA contained multiple compartments of differently pennated fascicles. In the LML compared to the SML, the GM, GL, and PLA had on average a 41%, 29%, and 41% increased fascicle length, and a 30%, 25%, and 33% decrease in fascicle pennation and a 32%, 11%, and 35% decrease in fascicle curvature, respectively. Architectural properties were also differentiated among the different compartments of the PLA and GL, allowing for a more detailed description of their fascicle structure and changes. It was shown that the compartments change differently with muscle length. It was also shown that for each degree of ankle joint angle reduction, the proximal GM aponeurosis length increased by 0.11%, the aponeurosis width decreased by 0.22%, and the area was decreased by 0.20%. The data provided improve our understanding of muscles and can be used to develop and validate muscle models.
Aponeurosis structure-function properties: Evidence of heterogeneity and implications for muscle function
2023, Acta Biomaterialia
Aponeurosis is a sheath-like connective tissue that aids in force transmission from muscle to tendon and can be found throughout the musculoskeletal system. The key role of aponeurosis in muscle-tendon unit mechanics is clouded by a lack of understanding of aponeurosis structure-function properties. This work aimed to determine the heterogeneous material properties of porcine triceps brachii aponeurosis tissue with materials testing and evaluate heterogeneous aponeurosis microstructure with scanning electron microscopy. We found that aponeurosis may exhibit more microstructural collagen waviness in the insertion region (near the tendon) compared to the transition region (near the muscle midbelly) (1.20 versus 1.12, p = 0.055), which and a less stiff stress-strain response in the insertion versus transition regions (p < 0.05). We also showed that different assumptions of aponeurosis heterogeneity, specifically variations in elastic modulus with location can alter the stiffness (by more than 10x) and strain (by approximately 10% muscle fiber strain) of a finite element model of muscle and aponeurosis. Collectively, these results suggest that aponeurosis heterogeneity could be due to variations in tissue microstructure and that different approaches to modeling tissue heterogeneity alters the behavior of computational models of muscle-tendon units.
Aponeurosis is a connective tissue found in many muscle tendon units that aids in force transmission, yet little is known about the specific material properties of aponeurosis. This work aimed to determine how the properties of aponeurosis tissue varied with location. We found that aponeurosis exhibits more microstructural waviness near the tendon compared to near the muscle midbelly, which was associated with differences in tissue stiffness. We also showed that different variations in aponeurosis modulus (stiffness) can alter the stiffness and stretch of a computer model of muscle tissue. These results show that assuming uniform aponeurosis structure and modulus, which is common, may lead to inaccurate models of the musculoskeletal system.
Muscle-tendon unit design and tuning for power enhancement, power attenuation, and reduction of metabolic cost
2023, Journal of Biomechanics
The contractile elements in skeletal muscle fibers operate in series with elastic elements, tendons and potentially aponeuroses, in muscle–tendon units (MTUs). Elastic strain energy (ESE), arising from either work done by muscle fibers or the energy of the body, can be stored in these series elastic elements (SEEs). MTUs vary considerably in their design in terms of the relative lengths and stiffnesses of the muscle fibers and SEEs, and the force and work generating capacities of the muscle fibers. However, within an MTU it is thought that contractile and series elastic elements can be matched or tuned to maximize ESE storage. The use of ESE is thought to improve locomotor performance by enhancing contractile element power during activities such as jumping, attenuating contractile element power during activities such as landing, and reducing the metabolic cost of movement during steady-state activities such as walking and running. The effectiveness of MTUs in these potential roles is contingent on factors such as the source of mechanical energy, the control of the flow of energy, and characteristics of SEE recoil. Hence, we suggest that MTUs specialized for ESE storage may vary considerably in the structural, mechanical, and physiological properties of their components depending on their functional role and required versatility.
The non-intuitive, in-vivo behavior of aponeuroses in a unipennate muscle
2023, Journal of Biomechanics
Citation Excerpt :
Our observations support the theory of Epstein et al. (2006) who described a gradient of longitudinal forces along the aponeuroses of unipennate muscles reducing from maximal force at the thick end of aponeuroses (at the insertion into the free tendon) to essentially zero force at the thin ends embedded in the muscle. These variable aponeurosis forces, combined with the structural changes along the long axis of the aponeuroses, may partly explain the non-uniform longitudinal strains observed in some aponeuroses (Zuurbier et al. 1994; Scott et al. 1995; Finni et al. 2003; Arellano et al. 2016). In a recent in-vitro investigation on isolated aponeurosis properties, it was concluded that differences in aponeurosis thickness along its length are indeed the reason for site-dependent differences in stiffness rather than a reduction in material properties (Shan et al. 2019).
Experimental observations and theoretical models suggest that the loading of muscular aponeuroses is complex, causing strain patterns that are not reconcilable with the frequently assumed mechanical “in series” arrangement of aponeuroses with muscles and tendons. The purpose of this work was to measure the in-vivo longitudinal strains of the distal and proximal aponeuroses and force of the unipennate Medial Gastrocnemius (MG) muscle during locomotor activities. Sonomicrometry crystals and a force buckle transducer were implanted to measure aponeurosis strains and MG forces in the left hindlimb of four healthy female sheep while walking at different speeds and inclination angles on a motorized treadmill. The resulting aponeurosis strains versus the corresponding muscle forces resulted in a complex interaction that is not reconcilable with a mechanical “in series” arrangement of aponeuroses with either the free tendon or muscle, as has frequently been assumed when trying to determine the storage and release of mechanical energy in muscles or the stiffness and elastic modulus of in-vivo aponeurosis tissues. We conclude that the interaction of muscle tissue with aponeuroses in the sheep MG allows for elongation of the aponeuroses at low forces in the passive muscle, while elongation in the active muscle is greatly reduced possibly due to the complex shear forces and pressures produced when the muscle is activated. It is likely that the observed aponeurosis mechanics are similar in other unipennate skeletal muscles, but the current study was limited to a single muscle and therefore does not allow for such extrapolation at this time.
The effects of an activation-dependent increase in titin stiffness on whole muscle properties using finite element modeling
2021, Journal of Biomechanics
Citation Excerpt :
Any collection of three muscle elements in series represents a muscle fascicle. Aponeurosis elements have identical mechanical properties, but increasing cross-sectional area toward the tendon (Zuurbier et al., 1994) is accounted for. The reference model accounts for the passive state titin properties for also the active state, whereas the extended models distinguish and represent the principles of two possible components to titin's stiffness increase upon activation: a direct calcium-titin interaction (Labeit et al., 2003; active state titin-I), and a titin-actin interaction that reduces the free spring length (Nishikawa et al., 2012; active state titin-II).
Active state titin’s effects have been studied predominantly in sarcomere or muscle fiber segment level and an understanding of its functional effects in the context of a whole muscle, and the mechanism of those is lacking. By representing experimentally observed calcium induced stiffening and actin-titin interaction induced reduced free spring length effects of active state titin in our linked fiber-matrix mesh finite element model, our aim was to study the mechanism of effects and particularly to determine the functionally more effective active state titin model. Isolated EDL muscle of the rat was modeled and three cases were studied: passive state titin (no change in titin constitutive equation in the active state), active state titin-I (constitutive equation involves a higher stiffness in the active state) and active state titin-II (constitutive equation also involves a strain shift coefficient accounting for titin’s reduced free spring length). Isometric muscle lengthening was imposed (initial to long length, l_m = 28.7 mm to 32.7 mm). Compared to passive state titin, (i) active state titin-I and II elevates muscle total (l_m = 32.7 mm: 14% and 29%, respectively) and active (l_m = 32.7 mm: 37.5% and 77.4%, respectively) forces, (ii) active state titin-II also shifts muscle’s optimum length to a longer length (l_m = 29.6 mm), (iii) active state titin-I and II limits sarcomere shortening (l_m = 32.7 mm: up to 10% and 20%, respectively). Such shorter sarcomere effect characterizes active state titin’s mechanism of effects. These effects become more pronounced and functionally more effective if not only calcium induced stiffening but also a reduced free spring length of titin is accounted for.
A simple geometrical model accounting for 3D muscle architectural changes across muscle lengths
2020, Journal of Biomechanics
Citation Excerpt :
Concluding, there is no method that yields the complete three-dimensional muscle architecture at different muscle lengths. When a muscle changes in length passively, most of the deformations occur within the muscle's fascicles while the aponeurosis retains its form to a large extent (Azizi and Roberts, 2009; Zuurbier et al., 1994 see also supplementary video). This is because the aponeurosis is stiff compared to passive muscle fascicles (Zuurbier et al., 1994).
Muscle architecture parameters change when the muscle changes in length. This has multiple effects on the function of the muscle, e.g. on force production and on contraction velocity. Here we present a versatile geometrical model that predicts changes in muscle architecture as a consequence of length changes of the muscle on the basis of the known architecture at a given muscle length. The model accounts for small changes in aponeuroses’ dimensions relative to changes in fascicle length and keeps muscle volume constant. We evaluate the model on the rabbit soleus muscle by comparing model predictions of fascicle lengths and pennation angles with experimental data. For this, we determined the internal architecture of the soleus muscle at different muscle belly lengths (67.8 mm at 35° ankle angle and 59.3 mm at 80° ankle angle). The long and the short soleus muscle exhibited mean fascicle lengths and pennation angles of 20.8 ± 1.3 mm, 4 ± 2° and 13.5 ± 1 mm, 10 ± 4°, respectively. The model predicted reasonable mean fascicle lengths and pennation angles for the long and short soleus that differed only by 1 mm and 1° from the measured data, respectively. Differences between predicted and measured distributions seem to stem from interindividual variability in muscle architecture. Even if the proposed approach has been used for the soleus muscle, which is relatively simple in architecture, it is not restricted to homogeneous unipennate architectures.

View all citing articles on Scopus

View full text

Length-force characteristics of the aponeurosis in the passive and active muscle condition and in the isolated condition

Abstract

The relation of isometric tension to length in skeletal muscle

J. Cell. Comp. Physiol.

Tensile force in total striated muscle, isolated fibre and sarcolemma

Acta Physiol. Scand.

Series elastic properties and architecture of skeletal muscle in isometric and dynamic contractions

Properties of the tendinous structures and series elastic component of EDL muscle-tendon complex of the rat

J. Biomechanics

The role of series elastic structures in prestretch-induced work enhancement during isotonic and isokinetic contractions

J. exp. Biol.

Shortening of muscle fibres during stretch of the active medial gastrocnemius muscle: the role of tendon compliance

J. Physiol.

Effects of growth on architecture and functional characteristics of adult rat gastrocnemius muscle

J. Morphol.

The series elastic component of muscle

Roles of muscle activity and load on the relationship between spindle length and whole muscle length in the freely walking cat