Training-induced changes in muscle architecture and specific tension

Five men underwent unilateral resistance training of elbow extensor (triceps brachii) muscles for 16 weeks. Before and after training, muscle layer thickness and fascicle angles of the long head of the triceps muscle were measured in vivo using B-mode ultrasound, and fascicle lengths were estimated. Series anatomical cross-sectional areas (ACSA) of the triceps brachii muscle were measured by magnetic resonance imaging, from which muscle volume (Vm) was determined and physiological cross-sectional area (PCSA) was calculated. Elbow extension strength (isometric; concentric and eccentric at 30, 90 and 180°·s^–1) was measured using an isokinetic dynamometer to determine specific tension. Muscle volumes, ACSA, PCSA, muscle layer thickness and fascicle angles increased after training and their relative changes were similar, while muscle and fascicle length did not change. Muscle strength increased at all velocities; however, specific tension decreased after training. Increase in fascicle angles, which would be the result of increasedV _m and PCSA, would seem to imply the occurrence of changes in muscle architecture. This might have given a negative effect on the force-generating properties of the muscles.     

Visualization and Quantification of Digitally Dissected Muscle Fascicles in the Masticatory Muscles of Callithrix jacchus Using Nondestructive DiceCT

The organization and length of a muscle's fascicles imparts its contractile properties. Longer fascicles permit increased muscle excursion, whereas changes in fascicle orientation relate to the overall vector of contractile force. Collecting data on fascicle architecture has traditionally involved destructive and irreversible gross dissection. In recent years, however, new imaging modalities have permitted muscles and their fascicles to be visualized nondestructively. Here, we present data from a primate (Callithrix jacchus), in which, for the first time, individual muscle fascicles are digitally “dissected” (segmented and reconstructed) using nondestructive, high-resolution diffusible iodine-based contrast-enhanced computed tomography (DiceCT) techniques. We also present quantitative data on the length and orientation of these fascicles within 10 muscle divisions of the jaw adductor and abductor musculature (superficial, deep, and zygomatic portions of temporalis and masseter; medial and lateral pterygoid; anterior and posterior digastric) and compare these digitally measured lengths to fascicular lengths measured using traditional gross and chemical dissection. Digitally derived fascicle lengths correspond well to their dissection-derived counterparts. Moreover, our analyses of changes in fascicle orientation across the adductor complex enable us to visualize previously uncharacterized levels of detail and highlight significant variation between adjacent muscle layers within muscle groups (e.g., between superficial, deep, and zygomatic portions of masseter and temporalis). We conclude that this technique offers great potential to future research, particularly for questions centered around the visualization and quantification of obscured and often-overlooked muscles such as the pterygoid and digastric muscles, and for deriving more accurate models of the masticatory system as a whole. Anat Rec, 302:1891–1900, 2019. © 2019 American Association for Anatomy     

Behaviour of vastus lateralis muscle–tendon during high intensity SSC exercises in vivo

Aims: The interaction between fascicle and tendinous tissue of human vastus lateralis muscle was investigated during varying intensity stretch–shortening cycle (SSC) jumps performed on a sledge apparatus. Methods: Eight subjects performed single leg squat (SJ) and drop jumps (DJ) from a constant dropping height but to different rebound heights. The fascicle length of the vastus lateralis muscle (VL) was determined from real‐time ultrasonography during the movement. Tendon length changes were calculated by subtracting the horizontal part of the fascicle length from the muscle–tendon unit (MTU) length. Simultaneously, kinematic, kinetic and electromyographic data were recorded from leg muscles. In addition, the in vivo patella tendon force was measured from one subject during the trials. Results: In all DJs, where MTU was stretched prior to shortening, the fascicle and tendinous tissue of the VL also underwent a SSC. The fascicle lengths decreased and the recoil of tendinous tissue increased with increased rebound intensities (P < 0.05). The force–velocity curves obtained from the MTU showed the expected force–velocity relationship for SSC activities, demonstrating performance enhancement. However, the increased MTU power during the shortening phase of the movement was due primarily to the enhancement of the tendon compartment. Conclusion: The results of this study show that, at higher rebound intensities, the fascicle is controlled during the braking phase in a distinct manner so that the effective recoil of the tendon is possible during the final push‐off phase. In addition, the results suggest that the behaviour of fascicle length change depends on the muscle in question in addition to the movement intensity.     

Electromyographical study of the iliocostalis lumborum, longissimus thoracis and spinalis thoracis muscles in various positions and movements

The iliocostalis lumborum, longissimus thoracis and spinalis thoracis muscles were studied electromyographically in six male individuals between 18 and 23 years old. They were connected to co-axial needle electrodes while in orthostatic, kneeling and sitting positions performing movements of flexing, extending and rotating the trunk. In the total flexing of the trunk the muscles did not present any action potential. The results showed intense potential for action while flexing the trunk 45 degrees, extending the trunk beginning at 45 degrees of flexing and in homolateral rotation for the muscles analyzed in the orthostatic position, emphasizing the iliocostalis lumborum muscle in the extension of the trunk which registered very strong action potentials in all individuals. There were similar results for movements of flexing and extending the trunk in the kneeling position, emphasizing the longissimus thoracis muscle in the movement of hyperextension. In the sitting position the more intense potentials were for the movements of extension, flexing with rotation and homolateral rotation of the trunk, emphasizing the longissimus thoracis muscle with strong potentials.     

Behaviour of vastus lateralis muscle-tendon during high intensity SSC exercises in vivo

AIMS: The interaction between fascicle and tendinous tissue of human vastus lateralis muscle was investigated during varying intensity stretch-shortening cycle (SSC) jumps performed on a sledge apparatus. METHODS: Eight subjects performed single leg squat (SJ) and drop jumps (DJ) from a constant dropping height but to different rebound heights. The fascicle length of the vastus lateralis muscle (VL) was determined from real-time ultrasonography during the movement. Tendon length changes were calculated by subtracting the horizontal part of the fascicle length from the muscle-tendon unit (MTU) length. Simultaneously, kinematic, kinetic and electromyographic data were recorded from leg muscles. In addition, the in vivo patella tendon force was measured from one subject during the trials. RESULTS: In all DJs, where MTU was stretched prior to shortening, the fascicle and tendinous tissue of the VL also underwent a SSC. The fascicle lengths decreased and the recoil of tendinous tissue increased with increased rebound intensities (P<0.05). The force-velocity curves obtained from the MTU showed the expected force-velocity relationship for SSC activities, demonstrating performance enhancement. However, the increased MTU power during the shortening phase of the movement was due primarily to the enhancement of the tendon compartment. CONCLUSION: The results of this study show that, at higher rebound intensities, the fascicle is controlled during the braking phase in a distinct manner so that the effective recoil of the tendon is possible during the final push-off phase. In addition, the results suggest that the behaviour of fascicle length change depends on the muscle in question in addition to the movement intensity.     

Neural compensation within the human triceps surae during prolonged walking

During human walking, muscle activation strategies are approximately constant across consecutive steps over a short time, but it is unknown whether they are maintained over a longer duration. Prolonged walking may increase tendinous tissue (TT) compliance, which can influence neural activation, but the neural responses of individual muscles have not been investigated. This study investigated the hypothesis that muscle activity is up- or down-regulated in individual triceps surae muscles during prolonged walking. Thirteen healthy subjects walked on a treadmill for 60 min at 4.5 km/h, while triceps surae muscle activity, maximal muscle compound action potentials, and kinematics were recorded every 5 min, and fascicle lengths were estimated at the beginning and end of the protocol using ultrasound. After 1 h of walking, soleus activity increased by 9.3 ± 0.2% (P < 0.05) and medial gastrocnemius activity decreased by 9.3 ± 0.3% (P < 0.01). Gastrocnemius fascicle length at ground contact shortened by 4.45 ± 0.99% (P < 0.001), whereas soleus fascicle length was unchanged (P = 0.988). Throughout the stance phase, medial gastrocnemius fascicle lengthening decreased by 44 ± 13% (P < 0.001), whereas soleus fascicle lengthening amplitude was unchanged (P = 0.650). The data suggest that a compensatory neural strategy exists between triceps surae muscles and that changes in muscle activation are generally mirrored by changes in muscle fascicle length. These findings also support the notion of muscle-specific changes in TT compliance after prolonged walking and highlight the ability of the CNS to maintain relatively constant movement patterns in spite of neuromechanical changes in individual muscles.     

Determination of three-dimensional muscle architectures: validation of the DTI-based fiber tractography method by manual digitization

In the last decade, diffusion tensor imaging (DTI) has been used increasingly to investigate three-dimensional (3D) muscle architectures. So far there is no study that has proved the validity of this method to determine fascicle lengths and pennation angles within a whole muscle. To verify the DTI method, fascicle lengths of m. soleus as well as their pennation angles have been measured using two different methods. First, the 3D muscle architecture was analyzed in vivo applying the DTI method with subsequent deterministic fiber tractography. In a second step, the muscle architecture of the same muscle was analyzed using a standard manual digitization system (MicroScribe MLX). Comparing both methods, we found differences for the median pennation angles (P < 0.001) but not for the median fascicle lengths (P = 0.216). Despite the statistical results, we conclude that the DTI method is appropriate to determine the global fiber orientation. The difference in median pennation angles determined with both methods is only about 1.2° (median pennation angle of MicroScribe: 9.7°; DTI: 8.5°) and probably has no practical relevance for muscle simulation studies. Determining fascicle lengths requires additional restriction and further development of the DTI method.     

A survey of in situ sarcomere extension in mouse skeletal muscle

The giant molecule titin/connectin was demonstrated to connect the ends of thick filaments with the Z-disks and thus to provide an elastic connection that seems to be responsible for passive tension in striated muscle. To investigate the physiological limits of I-band titin extension in skeletal muscle, we have measured sarcomere lengths of a number of mouse postural and clonal muscles in situ under the constraints imposed by the skeletal, ligamentous and tendinous components of the motile apparatus. These values now give upper limits for the extension of the I-band and therefore for the maximal degree of titin extension under physiological constraints. We find that I-band extension in all muscles investigated does not exceed a factor of 2.5 in situ, which is well below values obtainable in isolated fibre preparations. Approach to the yield-point is therefore prevented by extramuscular mechanisms. Sarcomere lengths near the tendinous junction and within the muscle are virtually identical in extended muscle, suggesting that a major function of titin in intact muscle is to ensure uniform sarcomere lengths over the entire muscle length and thus to prevent localized myofibril overstretch during isometric contraction     

Effects of prolonged walking on neural and mechanical components of stretch responses in the human soleus muscle

After repeated passive stretching, tendinous tissue compliance increases in the human soleus (SOL) muscle–tendon unit. During movement, such changes would have important consequences for neural and mechanical stretch responses. This study examined the existence of such effects in response to a 75 min walking intervention. Eleven healthy subjects walked on a treadmill at 4 km h⁻¹ with a robotic stretch device attached to the left leg. Ultrasonography was used to measure SOL fascicle lengths, and surface EMG activity was recorded in the SOL and tibialis anterior (TA) muscles. Perturbations of 6 deg were imposed at three different measurement intervals: Pre (immediately before the walking intervention), Mid (after approximately 30 min of walking) and Post (immediately after the intervention). Between the Pre–Mid and Mid–Post intervals, subjects walked for 30 min at a gradient of 3%. After the intervention, the amplitude and velocity of fascicle stretch both decreased (by 46 and 59%, respectively; P < 0.001) in response to a constant external perturbation, as did short (33%; P < 0.01) and medium (25%; P < 0.01) latency stretch reflex amplitudes. A faster perturbation elicited at the end of the protocol resulted in a recovery of fascicle stretch velocities and short latency reflex amplitudes to the pre-exercise values. These findings suggest that repeated stretching and shortening of a muscle–tendon unit can induce short-term structural changes in the tendinous tissues during human walking. The data also highlight the effect of these changes on neural feedback from muscle sensory afferents.     

Muscle–tendon interaction and EMG profiles of world class endurance runners during hopping

The present study examined the muscle–tendon interaction of ten international level Kenyan runners. Ultrasonography and kinematics were applied together with EMG recordings of lower limb muscles during repetitive hopping performed at maximal level. The ten Kenyans had longer gastro Achilles tendon at rest (p < 0.01) as compared with ten control subjects matched in height. Conversely, the stretching and shortening amplitudes of the tendinous tissues of the medial gastrocnemius (MG) muscle were significantly smaller in the Kenyans than in controls during the contact phase of hopping. This applied also to the fascicle length changes, which were smaller and more homogeneous among Kenyans. These limited musculo-tendinous changes resulted in higher maximal hopping height and in larger power despite their reduced body weight. The associated finding of a greater shortening to stretching ratio of the MG tendinous tissues during contact could imply that the Kenyan MG muscle–tendon unit is optimized to favor efficient storage and recoil of elastic energy, while operating at optimal muscle fascicle working range (plateau region).     

Trunk extensor endurance and its relationship to electromyogram parameters

Summary The present study was designed to investigate the relationship between muscle performance and electromyogram (EMG) parameters of the trunk extensor muscles in the development of fatigue. Nine subjects performed continuous isometric trunk extensions at 25% and 40% maximal voluntary contraction. The EMG signals of the longissimus thoracis, iliocostalis lumborum, multifidus and latissimus dorsi muscles were recorded. The EMG amplitude (RA-EMG) appeared to increase consistently during the contractions in all muscles, whereas the mean power frequency (MPF) showed a fairly consistent decrease during the contractions. The time constants of the exponential change of the RA-EMG and of the MPF were related to the endurance time. The prediction of endurance based on both EMG parameters appeared to yield better results than the prediction based on the relative force. In particular the time constants of the MPF changes of the multifidus and longissimus muscles appeared to be good predictors of endurance time. The consistency of the spectrum shift of EMG appeared to coincide with a reduced variability of the activation of the muscle involved.     

Comparative functional anatomy of the epaxial musculature of dogs (Canis familiaris) bred for sprinting vs. fighting

The axial musculoskeletal system of quadrupedal mammals is not currently well understood despite its functional importance in terms of facilitating postural stability and locomotion. Here we examined the detailed architecture of the muscles of the vertebral column of two breeds of dog, the Staffordshire bull terrier (SBT) and the racing greyhound, which have been selectively bred for physical combat and high speed sprint performance, respectively. Dissections of the epaxial musculature of nine racing greyhounds and six SBTs were carried out; muscle mass, length, and fascicle lengths were measured and used to calculate muscle physiological cross‐sectional area (PCSA), and to estimate maximum muscle potential for force, work and power production. The longissimus dorsi muscle was found to have a high propensity for force production in both breeds of dog; however, when considered in combination with the iliocostalis lumborum muscle it showed enhanced potential for production of power and facilitating spinal extension during galloping gaits. This was particularly the case in the greyhound, where the m. longissimus dorsi and the m. iliocostalis lumborum were estimated to have the potential to augment hindlimb muscle power by ca. 12%. Breed differences were found within various other muscles of the axial musculoskeletal system, particularly in the cranial cervical muscles and also the deep muscles of the thorax which insert on the ribs. These may also highlight key functional adaptations between the two breeds of dog, which have been selectively bred for particular purposes. Additionally, in both breeds of dog, we illustrate specialisation of muscle function by spinal region, with differences in both mass and PCSA found between muscles at varying levels of the axial musculoskeletal system, and between muscle functional groups.     

Functional anatomy and muscle moment arms of the pelvic limb of an elite sprinting athlete: the racing greyhound (Canis familiaris)

We provide quantitative anatomical data on the muscle-tendon architecture and geometry of the pelvic limb of an elite sprint athlete, the racing greyhound. Specifically, muscle masses, muscle lengths, fascicle lengths, pennation angles and muscle moment arms were measured. Maximum isometric force and power of muscles, the maximum muscle torque at joints and tendon stress and strain were estimated. We compare data with that published for a generalized breed of canid, and other cursorial mammals such as the horse and hare. The pelvic limb of the racing greyhound had a relatively large volume of hip extensor muscle, which is likely to be required for power production. Per unit body mass, some pelvic limb muscles were relatively larger than those in less specialized canines, and many hip extensor muscles had longer fascicle lengths. It was estimated that substantial extensor moments could be created about the tarsus and hip of the greyhound allowing high power output and potential for rapid acceleration. The racing greyhound hence possesses substantial specializations for enhanced sprint performance.     

Age-related changes in glucose utilization and fatty acid oxidation

The optimal utilization of energy substrates in muscle fibers is of primary importance for muscle contraction and whole body physiology. This study aimed to investigate the age-related changes in some indicators of glucose catabolism and fatty acid oxidation in muscles of growing rabbits. Longissimus lumborum (fast-twitch, LL) and semimembranosus proprius (slow-twitch, SMP) muscles were collected at 10 or 20 weeks of age (n = 6 per age). Glucose transporter GLUT4 content was investigated by immunoblot assay. Activity levels of five enzymes were measured: lactate dehydrogenase (LDH) and phosphofructokinase (PFK) for glycolysis; citrate synthase (CS), isocitrate dehydrogenase (ICDH) and -3-hydroxyacyl-coenzyme A dehydrogenase (HAD) for oxidation. Mitochondrial and peroxisomal oxidation rates were assessed on fresh homogenates using [1-¹⁴C]-oleate as substrate. At both ages, mitochondrial and peroxisomal oxidations rates, as well as activities of oxidative enzymes were higher in SMP than in LL. In both muscles, the apparent rate of fatty acid oxidation by the mitochondria did not differ between the two ages. However, a decrease in the activities of the three oxidative enzymes was observed in LL, whereas activities of CS and HAD and peroxisomal oxidation rate of oleate increased between the two ages in SMP muscle. In both muscles, LDH activity increased between 10 and 20 weeks, without variations in glucose uptake (GLUT4 transporter content) and in the first step of glucose utilization (PFK activity). In conclusion, mitochondrial oxidation rate of fatty acids and activities of selected mitochondrial enzymes were largely unrelated. Moreover, regulation of energy metabolism with advancing age differed between muscle types. This revised version was published online in July 2006 with corrections to the Cover Date.     

Muscle�Ctendon structure and dimensions in adults and children

Muscle performance is closely related to the architecture and dimensions of the muscle–tendon unit and the effect of maturation on these architectural characteristics in humans is currently unknown. This study determined whether there are differences in musculo‐tendinous architecture between adults and children of both sexes. Fascicle length and pennation angle were measured from ultrasound images at three sites along the length of the vastus intermedius, vastus lateralis, vastis medialis and rectus femoris muscles. Muscle volume and muscle–tendon length were measured from magnetic resonance images. Muscle physiological cross‐sectional area (PCSA) was calculated as the ratio of muscle volume to optimum fascicle length. Fascicle length was greater in the adult groups than in children (P < 0.05) but pennation angle did not differ between groups (P > 0.05). The ratios between fascicle and muscle length and between fascicle and tendon length were not different (P > 0.05) between adults and children for any quadriceps muscle. Quadriceps volume and PCSA of each muscle were greater in adults than children (P < 0.01) but the relative proportion of each head to the total quadriceps volume was similar in all groups. However, the difference in PCSA between adults and children (men ～ 104% greater than boys, women ～ 57% greater than girls) was greater (P < 0.05) than the difference in fascicle length (men ～ 37% greater than boys, women ～ 10% greater than girls). It is concluded that the fascicle, muscle and tendon lengthen proportionally during maturation, thus the muscle–tendon stiffness and excursion range are likely to be similar in children and adults but the relatively greater increase in PCSA than fascicle length indicates that adult muscles are better designed for force production than children’s muscles.     

The role of the extrinsic thoracic limb muscles in equine locomotion

Muscles have two major roles in locomotion: to generate force and to absorb/generate power (do work). Economical force generation is achieved by short-fibred pennate muscle while the maximum power output of a muscle is architecture independent. In this study we tested the hypothesis that there is an anatomical and structural separation between the force-generating anti-gravity muscles and the propulsive (limb/trunk moving) muscles of the equine forelimb. Muscle mass and fascicle length measurements were made on the thoracic limb extrinsic muscles of six fresh horse cadavers. Physiological cross-sectional area and maximum isometric force were then estimated. Maximum power was estimated from muscle volume and published contraction velocity data. The majority of extrinsic forelimb muscles were large with long fascicles arranged in parallel to the long axis of the muscle. Muscles arranged in this way are optimised for doing work. The architecture of serratus ventralis thoracis (SVT) was unique. It had short (48 +/- 17 mm) fascicles, arranged at about 45 degrees to the long axis of the muscle, which would suggest a force-generating, anti-gravity role. The muscle belly of SVT was sandwiched between two broad, thick sheets of aponeurosis. Hence, SVT could make a significant contribution to the overall elastic properties of the thoracic limb.     

The role of the extrinsic thoracic limb muscles in equine locomotion

Muscles have two major roles in locomotion: to generate force and to absorb/generate power (do work). Economical force generation is achieved by short-fibred pennate muscle while the maximum power output of a muscle is architecture independent. In this study we tested the hypothesis that there is an anatomical and structural separation between the force-generating anti-gravity muscles and the propulsive (limb/trunk moving) muscles of the equine forelimb. Muscle mass and fascicle length measurements were made on the thoracic limb extrinsic muscles of six fresh horse cadavers. Physiological cross-sectional area and maximum isometric force were then estimated. Maximum power was estimated from muscle volume and published contraction velocity data. The majority of extrinsic forelimb muscles were large with long fascicles arranged in parallel to the long axis of the muscle. Muscles arranged in this way are optimised for doing work. The architecture of serratus ventralis thoracis (SVT) was unique. It had short (48 +/- 17 mm) fascicles, arranged at about 45 degrees to the long axis of the muscle, which would suggest a force-generating, anti-gravity role. The muscle belly of SVT was sandwiched between two broad, thick sheets of aponeurosis. Hence, SVT could make a significant contribution to the overall elastic properties of the thoracic limb.     

Monitoring muscle over three orders of magnitude: Widespread positive allometry among locomotor and body support musculature in the pectoral girdle of varanid lizards (Varanidae)

There is a functional trade-off in the design of skeletal muscle. Muscle strength depends on the number of muscle fibers in parallel, while shortening velocity and operational distance depend on fascicle length, leading to a trade-off between the maximum force a muscle can produce and its ability to change length and contract rapidly. This trade-off becomes even more pronounced as animals increase in size because muscle strength scales with area (length²) while body mass scales with volume (length³). In order to understand this muscle trade-off and how animals deal with the biomechanical consequences of size, we investigated muscle properties in the pectoral girdle of varanid lizards. Varanids are an ideal group to study the scaling of muscle properties because they retain similar body proportions and posture across five orders of magnitude in body mass and are highly active, terrestrially adapted reptiles. We measured muscle mass, physiological cross-sectional area, fascicle length, proximal and distal tendon lengths, and proximal and distal moment arms for 27 pectoral girdle muscles in 13 individuals across 8 species ranging from 64 g to 40 kg. Standard and phylogenetically informed reduced major axis regression was used to investigate how muscle architecture properties scale with body size. Allometric growth was widespread for muscle mass (scaling exponent >1), physiological cross-sectional area (scaling exponent >0.66), but not tendon length (scaling exponent >0.33). Positive allometry for muscle mass was universal among muscles responsible for translating the trunk forward and flexing the elbow, and nearly universal among humeral protractors and wrist flexors. Positive allometry for PCSA was also common among trunk translators and humeral protractors, though less so than muscle mass. Positive scaling for fascicle length was not widespread, but common among humeral protractors. A higher proportion of pectoral girdle muscles scaled with positive allometry than our previous work showed for the pelvic girdle, suggesting that the center of mass may move cranially with body size in varanids, or that the pectoral girdle may assume a more dominant role in locomotion in larger species. Scaling exponents for physiological cross-sectional area among muscles primarily associated with propulsion or with a dual role were generally higher than those associated primarily with support against gravity, suggesting that locomotor demands have at least an equal influence on muscle architecture as body support. Overall, these results suggest that larger varanids compensate for the increased biomechanical demands of locomotion and body support at higher body sizes by developing larger pectoral muscles with higher physiological cross-sectional areas. The isometric scaling rates for fascicle length among locomotion-oriented pectoral girdle muscles suggest that larger varanids may be forced to use shorter stride lengths, but this problem may be circumvented by increases in limb excursion afforded by the sliding coracosternal joint.