Mechanical and morphological properties of human quadriceps femoris and triceps surae muscle-tendon unit in relation to aging and running

The purpose of this study was to examine the effects of aging and endurance running on the mechanical and morphological properties of different muscle-tendon units (MTUs) in vivo. The investigation was conducted on 30 elderly and 19 young adult males. For the analysis of possible MTU adaptation in response to endurance running the subjects were divided into two subgroups: non-active vs. endurance-runners. All subjects performed isometric maximal voluntary plantarflexion and knee extension contractions on a dynamometer. The distal aponeurosis of the gastrocnemius medialis (GM) and vastus lateralis (VL) during plantarflexion and knee extensions and the muscle architecture of the GM and VL were visualized by ultrasonography. The maximal knee and ankle joint moment were higher for the young compared to the elderly population (p<0.05). No identifiable differences in muscle architecture between young and elderly subjects were detected in VL and GM. Aging results in a reduced (p<0.05) normalized stiffness of the quadriceps femoris tendon and aponeurosis, which were not identifiable for the triceps surae. In contrast, the properties of both MTUs showed no major differences between endurance-runners and the non-active group (p>0.05). Only pennation angle at the GM were higher for the runners compared to the non-active group (p<0.05). The present results indicate that tendon changes related to aging do not occur proportionally in different MTUs. Furthermore, it seems that the extra stress and load imposed on high-load-bearing MTUs during endurance running may not be sufficient to produce significant adaptative processes in the mechanical parameters analyzed.     

Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo.

Load-strain characteristics of tendinous tissues (Achilles tendon and aponeurosis) were determined in vivo for human medial gastrocnemius (MG) muscle. Seven male subjects exerted isometric plantar flexion torque while the elongation of tendinous tissues of MG was determined from the tendinous movements by using ultrasonography. The maximal strain of the Achilles tendon and aponeurosis, estimated separately from the elongation data, was 5.1 +/- 1.1 and 5.9 +/- 1.6%, respectively. There was no significant difference in strain between the Achilles tendon and aponeurosis. In addition, no significant difference in strain was observed between the proximal and distal regions of the aponeurosis. The results indicate that tendinous tissues of the MG are homogeneously stretched along their lengths by muscle contraction, which has functional implications for the operation of the human MG muscle-tendon unit in vivo.     

Effects of repeated Achilles tendon vibration on triceps surae force production

Many studies reported benefits of whole-body vibration (WBV) on muscle force production. Therefore, WBV may be an important technique for muscle re-education. However vibrating platforms are heavy tools that cannot be easily used by all patients. Thus, we propose to apply vibrations directly to the Achilles tendon at rest with a portable vibrator. We investigated whether 14 days of such a vibration program would enhance triceps surae force production in healthy subjects. If successful, such a protocol could be utilized to prevent deleterious effects of hypo-activity. Twenty-nine healthy students participated in this study. The electrical evoked twitch and maximal voluntary contraction (MVC) in plantar-flexion, and electromyograms (EMG) were quantified before and at the end of the program. The vibration program consisted of 14 days of daily vibration applied at rest (duration: 1 h; frequency: 50 Hz). After the program, there was an increase in MVC associated with greater EMG of the TS. No sign of hypertrophy were found on the twitch parameters and the EMG–torque relationships. Repeated vibrations of the Achilles tendon lead to an increase in plantar-flexor activation and thus to greater force developed in voluntary conditions whilst the contractile properties assessed by the twitch are not modified. This program could be beneficial to persons with hypo-activity who are not candidates for WBV.     

Mechanical properties of aponeurosis and tendon of the cat soleus muscle during whole-muscle isometric contractions

Recent studies have suggested that the mechanical properties of aponeurosis are not similar to the properties of external tendon. In the present study, the lengths of aponeurosis, tendon, and muscle fascicles were recorded individually, using piezoelectric crystals attached to the surface of each structure during isometric contractions in the cat soleus muscle. We used a surgical microscope to observe the surface of the aponeurosis, which revealed a confounding effect on measures of aponeurosis length due to sliding of a thin layer of epimysium over the proximal aponeurosis. After correcting for this artifact, the stiffness computed for aponeurosis was similar to tendon, with both increasing from around 8 F₀/L_c (F₀ is maximum isometric force and L_c is tissue length) at 0.1 F₀ to 30 F₀/L_c at forces greater than 0.4 F₀. At low force levels only (0.1 F₀), aponeurotic stiffness increased somewhat as fascicle length increased. There was a gradient in the thickness of the aponeurosis along its length: its thickness was minimal at the proximal end and maximal at the distal end, where it converged to form the external tendon. This gradient in thickness appeared to match the gradient in tension transmitted along this structure. We conclude that the specific mechanical properties of aponeurosis are similar to those of tendon. © 1995 Wiley-Liss, Inc.     

The effects of Achilles tendon compliance on triceps surae mechanics and energetics in walking

Achilles tendon (AT) compliance can affect the generation and transmission of triceps surae muscle forces, and thus has important biomechanical consequences for walking performance. However, the uniarticular soleus (SOL) and the biarticular (GAS) function differently during walking, with in vivo evidence suggesting that their associated fascicles and tendinous structures exhibit unique kinematics during walking. Given the strong association between muscle fiber length, velocity and force production, we conjectured that SOL and GAS mechanics and energetic behavior would respond differently to altered AT compliance. To test this, we characterized GAS and SOL muscle and tendon mechanics and energetics due to systematic changes in tendon compliance using musculoskeletal simulations of walking. Increased tendon compliance enlarged GAS and SOL tendon excursions, shortened fiber operation lengths and affected muscle excitation patterns. For both muscles, an optimal tendon compliance (tendon strains of approximately 5% with maximum isometric force) existed that minimized metabolic energy consumption. However, GAS muscle-tendon mechanics and energetics were significantly more sensitive to changes in tendon compliance than were those for SOL. In addition, GAS was not able to return stored tendon energy during push-off as effectively as SOL, particularly for larger values of tendon compliance. These fundamental differences between GAS and SOL sensitivity to altered tendon compliance seem to arise from the biarticular nature of GAS. These insights are potentially important for understanding the functional consequences of altered Achilles tendon compliance due to aging, injury, or disease.     

Spontaneous activity of passive muscle spindles of the cat triceps surae muscle

The hypothesis that one possible cause of the spontaneous discharge of muscle spindles in the totally relaxed and de-efferented triceps surae muscle, with its tendon divided, is the mechanical factor due to extrafusal-intrafusal interaction was tested in experiments on anesthetized cats. Responses of spontaneously active units were similar with respect to many indices to responses of silent receptors capable of generating a long discharge in response to an increase in static length of the muscle. Isotonic contraction of the relaxed muscle during direct or indirect stimulation was accompanied by a pause in spontaneous activity. The prolonged increase in discharge frequency sometimes arising as a result of pressure on the muscle in the region of the receptor also was abolished by weak isotonic contraction of the muscle. If a long posttetanic sensory discharge was induced in a spontaneously active receptor by intensive tetanization of the nerve to the muscle, and it was then abolished by short stretching of the muscle, the initial spontaneous discharge frequency was restored. The dynamic thresholds of spontaneously active receptors were lower than for silent receptors. In some spontaneously active receptors an initial slowing of the discharge was observed during linear or stepwise stretching of the muscle. It is suggested that the ability of sensory endings to generate a long spontaneous discharge is due to initial stretching of the spindle inside the relaxed muscle.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 10, No. 3, pp. 287–294, May–June, 1978.     

Electrically evoked isometric and isokinetic properties of the triceps surae in young male subjects

The relationship between electrically evoked isometric and isokinetic properties of the triceps surae have been studied in 11 healthy male subjects. The results showed that the time to peak tension (TPT) and half relaxation time (1/2 RT) of the maximal twitch were 110 +/- 11 ms and 82 +/- 11 ms respectively, and the peak rates of rise of contraction (delta P50, delta P200) and relaxation (delta PR50, delta PR200) at 50 and 200 Hz were 0.36 +/- 0.07, 0.48 +/- 0.08 and 1.27 +/- 0.33, 1.25 +/- 0.27% Po ms-1 respectively. The decline in force during a fatigue test was significantly (P less than 0.02) associated with the decrease in maximal relaxation rate (r = 0.79). The TPT was significantly (P less than 0.05) and inversely related to delta P50 and delta P200. The mean angle specific torque-velocity relationship for the 11 subjects was adequately described by the empirical exponential equation of the form: V = 16.5 (e-P/30.8-e-84.3/30.8) where V = velocity (rads s-1) and P = torque (Nm). The only significant association found between the isometric and isokinetic properties of the muscle was between delta PR200 and the torque expressed at a given velocity of 4 rads s-1. This lack of association between the two variables is difficult to explain with certainty but it is suggested that it may be due to the differential effects of Ca2+ release and uptake and cross-bridge turnover rate in the two situations.     

Mechanical properties of rat tail tendon in relation to proximal-distal sampling position and age

The mechanical properties of 3, 15 and 25 month-old rat tail tendons were investigated in relation to proximal-distal sampling location along the fibre length. For the 15 and 25 month-old tendons maximum load as well as collagen content per mm fibre length (unit collagen) increased markedly from the proximal to the distal location. A linear regression analysis of the collagen content and mechanical parameters (maximum load, maximum slope of the load-strain curve and energy absorption) showed that these parameters were linearly correlated to the collagen content. However, normalization of the mechanical parameters with regard to the collagen content did not cancel the dependency of the parameters on proximal-distal sampling location. Normalized load and energy values for the 3 month-old tendons and normalized slope values for the 15 and 25 month-old tendons were found to decrease from proximal to distal location. These findings showed that tail tendons are heterogeneous along their length in respect to mechanical strength. The regression analysis also indicated the existence of an inverse relationship between unit collagen and mechanical quality of the collagen. Alternatively, the mechanical properties of tendon fibres might be influenced by other components than collagen.     

Mechanical properties of the gastrocnemius aponeurosis in wild turkeys

In many muscles, the tendinous structures include both an extramuscular free tendon as well as a sheet-like aponeurosis. In both free tendons and aponeuroses the collagen fascicles are oriented primarily longitudinally, along the muscle's line of action. It is generally assumed that this axis represents the direction of loading for these structures. This assumption is well founded for free tendons, but aponeuroses undergo a more complex loading regime. Unlike free tendons, aponeuroses surround a substantial portion of the muscle belly and are therefore loaded both parallel (longitudinal) and perpendicular (transverse) to a muscle's line of action when contracting muscles bulge to maintain a constant volume. Given this biaxial loading pattern, it is critical to understand the mechanical properties of aponeuroses in both the longitudinal and transverse directions. In this study, we use uniaxial testing of isolated tissue samples from the aponeurosis of the lateral gastrocnemius of wild turkeys to determine mechanical properties of samples loaded longitudinally (along the muscle's line of action) and transversely (orthogonal to the line of action). We find that the aponeurosis has a significantly higher Young's modulus in the longitudinal than in the transverse direction. Our results also show that aponeuroses can behave as efficient springs in both the longitudinal and transverse directions, losing little energy to hysteresis. We also test the failure properties of aponeuroses to quantify the likely safety factor with which these structures operate during muscular force production. These results provide an essential foundation for understanding the mechanical function of aponeuroses as biaxially loaded biological springs.     

Twitch contractile adaptations are not dependent on the intensity of isometric exercise in the human triceps surae

Ultrastructural and twitch contractile characteristics of the human triceps surae were determined in six healthy but very sedentary subjects before and after 16 weeks of isometric training at 30% maximal voluntary contraction (MVC). Following training, twitch contraction time was approximately 16% shorter, although no differences were observed in one-half relaxation time or peak twitch torque. Percent fibre type was not changed by training. The mean area of type I and type II fibres in the soleus increased by approximately 30% but only type II fibres showed an increase in area in the lateral gastrocnemius (30%). Despite such changes in fibre area the volume density of the sarcoplasmic reticulum-transverse tubular network averaged 3.2 +/- 0.6% and 5.9 +/- 0.9% in type I and type II fibres respectively, before and after training in the two heads of the gastrocnemius. The results indicate that contractile adaptations to isometric training at 30% MVC were limited to twitch contraction time and were not directly related to changes in percent fibre distribution or the volume of sarcoplasmic reticulum and transverse tubules in either type I or type II fibres. The data further demonstrate that substantial fibre hypertrophy is achieved by training with low-intensity contractions.     

Voluntary activation of the triceps surae in prepubertal children

The activation capacities and neuromuscular efficiency (NME) of the triceps surae (TS) of prepubescent children (7–11 years) and adults were evaluated during submaximal and maximal (MVC) isometric plantarflexion to determine whether they varied with age. TS-EMG were obtained by summing-up the rectified electromyograms of the soleus and gastrocnemii muscles; these data were quantified using a sliding average method and normalized with reference to the TS maximal compound action potential (TS-M-wave).

The maximal EMG increased significantly with age in the children, but less than MVC, what led to a significant increase in NME_Max (MVC/TS-EMG_max ratio). The EMG–torque relationship indicated an age-related overactivation of TS at low torque, what led to a lower NME_Sub-max (inverse of the slope of the EMG–torque relationship) for the youngest children. The overactivation of TS was accompanied by contraction of the TA, which decreased with age. The youngest children were also less able to maintain a target torque and muscle activation. Finally, the twitch interpolated method revealed an age-dependant activation deficit. We conclude that central mechanisms are the main cause of the lower torques developed by children and they appear to vary with age in prepubertal children.     

Peak triceps surae muscle activity is not specific to knee flexion angles during MVIC

There is limited research on peak activity of the separate triceps surae muscles in select knee flexion (KF) positions during a maximum voluntary isometric contraction (MVIC) used to normalize EMG signals. The aim of this study was to determine how frequent peak activity occurred during an MVIC for soleus (SOL), gastrocnemius medialis (GM), and gastrocnemius lateralis (GL) in select KF positions, and if these peaks were recorded in similar KF positions. Forty-eight healthy individuals performed unilateral plantar-flexion MVIC in standing with 0°KF and 45°KF, and in sitting with 90°KF. Surface EMG of SOL, GM, and GL were collected and processed in 250 ms epochs to determine peak root-mean-square amplitude. Peak activity was most frequently captured in standing and rarely in sitting, with no position selective to SOL, GM or GL activity. Peak GM and GL activity was more frequent in 0°KF than 45°KF, and more often in similar KF positions than not. Peak SOL activity was just as likely in 45°KF as 0°KF, and more in positions similar to GM, but not GL. The EMG amplitudes were at least 20% greater in positions that captured peak activity over those that did not. The overall findings support performing an MVIC in more than one KF position to normalize triceps surae EMG. It is emphasized that no KF position is selective to SOL, GM, or GL alone.     

Mechanical and morphological properties of the triceps surae muscle-tendon unit in old and young adults and their interaction with a submaximal fatiguing contraction.

The purposes of this study were to examine (a) whether the morphological properties of the muscle gastrocnemius medialis (GM) contribute to the known enhanced muscle fatigue resistance during submaximal sustained isometric plantar flexion contraction of old compared to young adults and (b) whether a submaximal fatiguing contraction differently affects the mechanical properties of the GM tendon and aponeurosis of old and young adults. Fourteen old and 12 young male subjects performed maximal voluntary isometric plantar flexions (MVC) on a dynamometer before and after a submaximal fatiguing task (40% MVC). Moments and EMG signals from the gastrocnemius medialis and lateralis, soleus and tibialis anterior muscles were measured. The elongation of the GM tendon and aponeurosis and the morphological properties of its contractile element were examined by means of ultrasonography. The old adults showed lower maximal ankle joint moment, stiffness and fascicle length in both tested conditions. The submaximal fatiguing contraction did not affect the force-strain relationship of the GM tendon and aponeurosis of either young or old adults. The time to task failure was longer for the old adults and was strongly correlated with the fascicle length (r(2)=0.50, P<0.001). This provides evidence on that the lower ratio of the active muscle volume to muscle force for the old adults might be an additional mechanism contributing to the known age related increase in muscle fatigue resistance.     

Heterogeneity of muscle activation in relation to force direction: A multi-channel surface electromyography study on the triceps surae muscle

Several skeletal muscles can be divided into sub-modules, called neuromuscular compartments (NMCs), which are thought to be controlled independently and to have distinct biomechanical functions. We looked for distinct muscle activation patterns in the triceps surae muscle (TS) using surface electromyography (EMG) during voluntary contraction. Nine subjects performed isometric and isotonic plantar flexions combined with forces along pre-defined directions. Besides the forces under the ball of the foot, multi-channel surface EMG was measured with electrodes homogeneously distributed over the entire TS. Using principal component analysis, common (global) components were omitted from the EMG signals, thereby estimating muscle activity sufficiently accurate to track fine fluctuations of force during an isotonic contraction (r = 0.80 ± 0.09). A subsequent cluster analysis showed a topographical organization of co-activated parts of the muscle that was different between subjects. Low and negative correlations between the EMG activity within clusters were found, indicating a substantial heterogeneity of TS activation. The correlations between cluster time series and forces at the foot in specific directions differed substantially between clusters, showing that the differentially activated parts of the TS had specific biomechanical functions.     

A model of the human triceps surae muscle-tendon complex applied to jumping

The purpose of this study was to gain more insight into the behavior of the muscle-tendon complex of human m. triceps surae in jumping. During one-legged vertical jumps of ten subjects ground reaction forces as well as cinematographic data were registered, and electromyograms were recorded from m. soleus and m. gastrocnemius. A model was developed of m. triceps surae, incorporating assumptions concerning dimensions, architecture, force-length and force-velocity relationships of muscle fibers, as well as assumptions concerning dimensions and elastic behavior of tendinous tissue in series with the muscle fibers. The velocity with which origin approaches insertion (V OI) was calculated for m. soleus and m. gastrocnemius using cine film data, and served as input of the model. During the last part of the push-off phase EMG-levels were found to be more or less constant, V OI of m. soleus and m. gastrocnemius rapidly increased, and the plantar flexing moment obtained by solving equations concerning a free body diagram of the foot rapidly declined. A similar decline was observed in the plantar flexing moment obtained by multiplying force calculated with help of the model by estimated moment arm at the ankle. As a result of the decline of exerted force tendon length decreases. According to the model the shortening velocity of tendon reaches higher values than that of muscle fibers. The results of a kinetic analysis demonstrate that during the last part of the push-off phase a combination of high angular velocities with relatively large plantar flexing moments is required. It is concluded that without a compliant tendon m. triceps surae would not be able to satisfy this requirement.     

Contractile adaptations in the human triceps surae after isometric exercise

Ultrastructural and twitch contractile characteristics of the human triceps surae were determined in seven healthy but very sedentary subjects before and after 16 wk of unilateral isometric training at 100% maximal voluntary contraction. After training, twitch contraction time decreased by approximately 20%. One-half relaxation time, peak twitch torque, and percent fiber type in any of the muscles of the triceps surae complex were not changed by training. Type I and type II fiber areas increased in the soleus by approximately 30%, but only type II fibers showed an increased in area in the lateral gastrocnemius (40%). Despite such changes in fiber area, the volume density of the sarcoplasmic reticulum-transverse tubular (SR) network averaged 3.2 +/- 0.6 and 5.9 +/- 0.9% in type I and type II fibers, respectively, before and after training in the two heads of the gastrocnemius. Type I SR fraction increased to 3.5 +/- 1.2% after training in the soleus; however, correlations were not significant between the change in the volume density of SR and the change in twitch contraction time (R = 0.46, P = 0.45) or the change in one-half relaxation time (R = -0.68, P = 0.08). The results demonstrate that isometric training at 100% maximal voluntary contraction induced changes in twitch contraction time that were not directly related to changes in the volume density of SR in fibers of the triceps surae.     

Ethnic differences in triceps surae muscle-tendon complex and walking economy

The purposes of this study were to (a) determine whether structural differences in triceps surae muscle-tendon complex and walking economy exist between 14 African American and 19 Caucasian sedentary women and (b) determine whether muscle-tendon parameters are associated with walking economy. African American and Caucasian subjects were matched on body weight, height, and body composition. Muscle-tendon parameters were determined by magnetic resonance imaging and walking economy was evaluated at 4.8 km.h(-1). Medial gastrocnemius and total triceps surae muscle shape were different across ethnicity despite no ethnic differences in plantar flexion strength or in maximal cross-sectional area for any triceps surae muscles. African American women had shorter gastrocnemius muscles and longer tendons and performed walking more economically. Tendon length was the only variable related to walking economy. No ethnic differences were observed in walking economy after adjusting for tendon length. Data show gastrocnemius tendon length is related to level walking and longer gastrocnemius tendons may partly explain more economical walking in African American women. These preliminary findings indicate the structure of the muscle-tendon complex could be a factor partially accounting for reported ethnic differences in certain types of athletic-related performance.     

Influence of knee flexion angle and age on triceps surae muscle activity during heel raises

ABSTRACT: Hébert-Losier, K, Schneiders, AG, García, JA, Sullivan, SJ, and Simoneau, GG. Influence of knee flexion angle and age on triceps surae muscle activity during heel raises. J Strength Cond Res 26(11): 3124-3133, 2012-Triceps surae and Achilles tendon injuries are frequent in sports medicine, particularly in middle-aged adults. Muscle imbalances and weakness are suggested to be involved in the etiology of these conditions, with heel-raise testing often used to assess and treat triceps surae (TS) injuries. Although heel raises are recommended with the knee straight for gastrocnemius and bent for soleus (SOL), the extent of muscle selectivity in these positions is not clear. This study aimed to determine the influence of knee angle and age on TS muscle activity during heel raises. Forty-eight healthy men and women were recruited from a younger-aged (18-25 years) and middle-aged (35-45 years) population. All the subjects performed unilateral heel raises in 0° and 45° knee flexion (KF). Soleus, gastrocnemius medialis (GM) and gastrocnemius lateralis (GL) surface electromyography signals were processed to compute root-mean-square amplitudes, and data were analyzed using mixed-effects models and stepwise regression. The mean TS activity during heel raises was 23% of maximum voluntary isometric contraction when performed in 0° KF and 21% when in 45°. Amplitudes were significantly different between TS muscles (p < 0.001) and KF angles (p < 0.001), with a significant interaction (p < 0.001). However, the age of the population did not influence the results (p = 0.193). The findings demonstrate that SOL activity was 4% greater when tested in 45° compared with 0° KF and 5% lower in the GM and GL. The results are consistent with the recommended use of heel raises in select knee positions for assessing, training, and rehabilitating the SOL and gastrocnemius muscles; however, the 4-5% documented change in activity might not be enough to significantly influence clinical outcome measures or muscle-specific benefits. Contrary to expectations, TS activity did not distinguish between middle-aged and younger-aged adults, despite the higher injury prevalence in middle age.