Morphometry of Macaca mulatta forelimb. I. Shoulder and elbow muscles and segment inertial parameters

The present study examined the morphometric properties of the forelimb, including the inertial properties of the body segments and the morphometric parameters of 21 muscles spanning the shoulder and/or elbow joints of six Macaca mulatta and three M. fascicularis. Five muscle parameters are presented: optimal fascicle length (L(0)(M)), tendon slack length (L(S)(T)), physiological cross-sectional area (PCSA), pennation angle (alpha(0)), and muscle mass (m). Linear regressions indicate that muscle mass, and to a lesser extent PCSA, correlated with total body weight. Segment mass, center-of-mass, and the moment of inertia of the upper arm, forearm, and hand are also presented. Our data indicate that for some segments, radius of gyration (rho) predicts segment moment of inertia better than linear regressions based on total body weight. Key differences between the monkey and human forelimb are highlighted.     

Pennation angles of the intrinsic muscles of the foot

As mathematical models of the musculoskeletal system become increasingly detailed and precise, they require more accurate information about the architectural parameters of the individual muscles. These muscles are typically represented as Hill-type models, which require data on fiber length, physiological cross-sectional area (PCSA) and pennation angle. Most of this information for lower limb muscles has been published, except for data on the pennation angle of the intrinsic muscles of the foot. Each (n=20) intrinsic muscle of three human feet was dissected free. The dorsal and plantar surfaces were photographed and a digitized color image was imported into Abobe Photoshop. The muscles were divided into "anatomical units". For each anatomical unit (n=26), a line was drawn along the tendon axis and a number of other lines were drawn along individual muscle fibers. The angle between the tendon line and each fiber line was defined as the pennation angle of that fiber. By visual inspection, an effort was made to take measurements such that they represented the distribution of fibers in various parts of the muscle. Although some individual muscles had higher or lower pennation angles, when averaged for all specimens, the second dorsal interosseous had the smallest pennation angle (6.7+/-6.81 degrees) while the abductor digiti minimi had the largest (19.1+/-11.19 degrees). Since the cosines of the angles range from 0.9932 to 0.9449, the effect of the pennation angle on the force generated by the muscle was not great.     

Inevitable joint angular rotation affects muscle architecture during isometric contraction

The purpose of this study was to quantify the influence of inevitable ankle joint motion during an isometric contraction on the measured change of the gastrocnemius medialis muscle (GM) architecture in vivo during the loading and the unloading phase. Sitting on a dynamometer subjects performed isometric maximal voluntary contractions as well as contractions induced by electrostimulation. Synchronous joint angular motion, plantarflexion moment, foot’s centre of pressure and real-time ultrasonography of muscle architecture changes of the GM were obtained. During the contraction the ankle joint position altered and significantly affected the change in muscle architecture. At maximal tendon force (1094 ± 323 N), the measured fascicle length overestimated the change in fascicle length due to the tendon force by 1.53 cm, while the measured pennation angle overestimated the change in pennation angle due to the tendon force by 5.5°. At the same tendon force the measured fascicle length and pennation angle were significantly different between loading and unloading conditions. After correcting the values for the change in ankle joint angle no differences between the loading and the unloading phase at the same tendon force were found. Concerning the estimation of GM fascicle length–force and pennation angle–force curves during the loading and unloading phase of an isometric contraction, these findings indicate that not accounting for ankle joint motion will produce unreliable results.     

In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men.

Sarcopenia and muscle weakness are well-known consequences of aging. The aim of the present study was to ascertain whether a decrease in fascicle force (Ff) could be accounted for entirely by muscle atrophy. In vivo physiological cross-sectional area (PCSA) and specific force (Ff/PCSA) of the lateral head of the gastrocnemius (GL) muscle were assessed in a group of elderly men [EM, aged 73.8 yr (SD 3.5), height 173.4 cm (SD 4.4), weight 78.4 kg (SD 8.3); means (SD)] and for comparison in a group of young men [YM, aged 25.3 yr (SD 4.4), height 176.4 cm (SD 7.7), weight 79.1 kg (SD 11.9)]. GL muscle volume (Vol) and Achilles tendon moment arm length were evaluated using magnetic resonance imaging. Pennation angle and fiber fascicle length (Lf) were measured using B-mode ultrasonography during isometric maximum voluntary contraction of the plantar flexors. PCSA was estimated as Vol/Lf. GL Ff was calculated by dividing Achilles tendon force by the cosine of theta, during the interpolation of a supramaximal doublet, and accounting for antagonist activation level (assessed using EMG), Achilles tendon moment arm length, and the relative PCSA of the GL within the plantar flexor group. Voluntary activation of the plantar flexors was lower in the EM than in the YM (86 vs. 98%, respectively, P < 0.05). Compared with the YM, plantar flexor maximal voluntary contraction torque and Ff of the EM were lower by 47 and 40%, respectively (P < 0.01). Both Vol and PCSA were smaller in the EM by 28% (P < 0.01) and 16% (P < 0.05), respectively. Also, pennation angle was 12% smaller in the EM, whereas there was no significant difference in Lf between the YM and EM. After accounting for differences in agonists and antagonists activation, the Ff/PCSA of the EM was 30% lower than that of the YM (P < 0.01). These findings demonstrate that the loss of muscle strength with aging may be explained not only by a reduction in voluntary drive to the muscle, but mostly by a decrease in intrinsic muscle force. This phenomenon may possibly be due to a reduction in single-fiber specific tension.     

American Society of Biomechanics Journal of Biomechanics Award 2017: High-acceleration training during growth increases optimal muscle fascicle lengths in an avian bipedal model

Sprinters have been found to possess longer muscle fascicles than non-sprinters, which is thought to be beneficial for high-acceleration movements based on muscle force-length-velocity properties. However, it is unknown if their morphology is a result of genetics or training during growth. To explore the influence of training during growth, thirty guinea fowl (Numida meleagris) were split into exercise and sedentary groups. Exercise birds were housed in a large pen and underwent high-acceleration training during their growth period (age 4–14 weeks), while sedentary birds were housed in small pens to restrict movement. Morphological analyses (muscle mass, PCSA, optimal fascicle length, pennation angle) of a hip extensor muscle (ILPO) and plantarflexor muscle (LG), which differ in architecture and function during running, were performed post-mortem. Muscle mass for both ILPO and LG was not different between the two groups. Exercise birds were found to have ∼12% and ∼14% longer optimal fascicle lengths in ILPO and LG, respectively, than the sedentary group despite having ∼3% shorter limbs. From this study we can conclude that optimal fascicle lengths can increase as a result of high-acceleration training during growth. This increase in optimal fascicle length appears to occur irrespective of muscle architecture and in the absence of a change in muscle mass. Our findings suggest high-acceleration training during growth results in muscles that prioritize adaptations for lower strain and shortening velocity over isometric strength. Thus, the adaptations observed suggest these muscles produce higher force during dynamic contractions, which is beneficial for movements requiring large power outputs.     

The isometric functional capacity of muscles that cross the elbow

We hypothesized that muscles crossing the elbow have fundamental differences in their capacity for excursion, force generation, and moment generation due to differences in their architecture, moment arm, and the combination of their architecture and moment arm. Muscle fascicle length, sarcomere length, pennation angle, mass, and tendon displacement with elbow flexion were measured for the major elbow muscles in 10 upper extremity specimens. Optimal fascicle length, physiological cross-sectional area (PCSA), moment arm, operating range on the force-length curve, and moment-generating capacity were estimated from these data. Brachioradialis and pronator teres had the longest (17.7cm) and shortest (5.5cm) fascicles, respectively. Triceps brachii (combined heads) and brachioradialis had the greatest (14.9cm(2)) and smallest (1.2cm(2)) PCSAs, respectively. Despite a comparable fascicle length, long head of biceps brachii operates over a broader range of the force-length curve (length change=56% of optimal length, 12.8cm) than the long head of triceps brachii (length change=28% of optimal length, 12. 7cm) because of its larger moment arm (4.7cm vs. 2.3cm). Although brachioradialis has a small PCSA, it has a relatively large moment-generating capacity (6.8cm(3)) due to its large moment arm (average peak=7.7cm). These results emphasize the need to consider the interplay of architecture and moment arm when evaluating the functional capabilities of a muscle.     

Validity of architectural properties of the hamstring muscles: Correlation of ultrasound findings with cadaveric dissection

The purpose of this study was to compare the architectural parameters of the long head of biceps femoris (BFlh) and semitendinosus (ST) muscles by comparing measurements from ultrasound (US) with those obtained from direct dissection. The BFlh and ST architectures were examined bilaterally in 6 legs from 3 male cadavers. The fascicle length, pennation angle, muscle thickness and muscle and tendon length were obtained from direct measurement and US scans along each muscle. Intraclass correlation coefficients between the two methods ranged from 0.905 to 0.913 for the BFlh variables and from 0.774 to 0.974 for the ST parameters. Compared with the direct measurements, the US method showed a mean typical error of 0.09–0.14 cm for muscle thickness, 1.01–1.31° for the pennation angle, 0.92–1.71 cm for fascicle length and muscle–tendon length measurements. The US method is a valid alternative tool for assessing basic architectural parameters of ST and BFlh components of the hamstring muscles.     

Fascicle length of gastrocnemius muscles in monozygous twins

A large inter-individual variation is seen in muscle fascicle length of the athletes but the reasons for this phenomenon are unclear. The purpose of this study was to determine whether genetic factors contribute to the variances in muscle architectural characteristics. Nine monozygous twin pairs (3 males and 6 females), mean age 23 years (range 17-40) were studied. Fascicle length, pennation angle, and muscle thickness of the medial (MG) and lateral (LG) gastrocnemius muscles were measured in vivo by B-mode ultrasound. In the LG muscle intrapair resemblance (P < 0.01) for fascicle length (r = 0.98), pennation angle (r = 0.94) and muscle thickness (r = 0.86) were observed. In MG muscle, however, there was no intrapair resemblance for fascicle length (r = 0.66, P > 0.05), although pennation angle (r = 0.73, P < 0.05) and muscle thickness (r = 0.86, P < 0.01) were significant. Mean percent intrapair difference in LG and MG muscles were 1.8% and 5.1% for fascicle length, 11.3% and 12.3% for pennation angle and 12.4% and 9.9% for muscle thickness, respectively. There is intrapair difference between muscle thickness and pennation angle in both MG (r = 0.69, P < 0.05) and LG (r = 0.70, P < 0.05) muscles. However, no significant correlation was observed for intrapair difference between muscle thickness and fascicle length in both muscles (MG, r = 0.46; LG, r = 0.40). It appears that genetic predisposition is the predominant factor for the determination of muscle fascicle length. However, a lack of intrapair resemblance in MG fascicle length raises the possibility that fascicle length may be further influenced by external environmental factors such as physical training.     

Ultrasound-based subject-specific parameters improve fascicle behaviour estimation in Hill-type muscle model

The estimation of muscle fascicle behaviour is decisive in a Hill-type model as they are related to muscle force by the force–length–velocity relationship and the tendon force–strain relationship. This study was aimed at investigating the influence of subject-specific tendon force–strain relationship and initial fascicle geometry (IFG) on the estimation of muscle forces and fascicle behaviour during isometric contractions. Ultrasonography was used to estimate the in vivo muscle fascicle behaviour and compare the muscle fascicle length and pennation angle estimated from the Hill-type model. The calibration–prediction process of the electromyography-driven model was performed using generic or subject-specific tendon definition with or without IFG as constraint. The combination of subject-specific tendon definition and IFG led to muscle fascicle behaviour closer to ultrasound data and significant lower forces of the ankle dorsiflexor and plantarflexor muscles compared to the other conditions. Thus, subject-specific ultrasound measurements improve the accuracy of Hill-type models on muscle fascicle behaviour.     

Optimal pennation angle of the primary ankle plantar and dorsiflexors: variations with sex, contraction intensity, and limb

Ultrasonography was used to measure the pennation angle of the human tibialis anterior (TA), lateral gastrocnemius (LG), medial gastrocnemius (MG), and soleus (Sol). The right and left legs of 8 male and 8 female subjects were tested at rest and during maximum voluntary contraction (MVC). Joint angles were chosen to control muscle tendon lengths so that the muscles were near their optimal length within the length-tension relationship. No differences in pennation angle were detected between the right and left legs. Another consistent finding was that the pennation angle at MVC was significantly greater than at rest for all muscles tested. Optimal pennation angles for the TA, MG, and Sol were significantly greater for the men than for the women. Optimal pennation angles for the TA, LG, MG, and Sol for the male subjects were 14.3 degrees, 23.7 degrees, 34.6 degrees, and 40.1 degrees respectively, whereas values of 12.1 degrees, 16.3 degrees, 27.3 degrees, and 26.3 degrees were recorded for the female subjects. The results of this study suggest the following: (1) similar values for pennation angle can be used for the right and left TA, LG, MG, and Sol; (2) pennation angle is significantly greater at MVC than at rest for all muscles tested; and (3) sex-specific values for optimal pennation angle should be used when modeling the force-generating potential of the primary muscles responsible for ankle plantar and dorsiflexion.     

Determination of fascicle length and pennation in a contracting human muscle in vivo

Fukunaga, Tetsuo, Yoshiho Ichinose, Masamitsu Ito, YasuoKawakami, and Senshi Fukashiro. Determination of fascicle lengthand pennation in a contracting human muscle in vivo.J. Appl. Physiol. 82(1): 354-358, 1997.We have developed a technique to determine fascicle length inhuman vastus lateralis muscle in vivo by using ultrasonography. Whenthe subjects had the knee fully extended passively from a position of110° flexion (relaxed condition), the fascicle length decreasedfrom 133 to 97 mm on average. During static contractions at 10% ofmaximal voluntary contraction strength (tensed condition), fascicleshortening was more pronounced (from 126 to 67 mm), especially when theknee was closer to full extension. Similarly, as the knee was extended, the angle of pennation (fascicle angle, defined as the angle between fascicles and aponeurosis) increased (relaxed, from 14 to 18°; tensed, from 14 to 21°), and a greater increase in the pennation angle was observed in the tensed than in the relaxed condition when theknee was close to extension (<40°). We conclude that there aredifferences in fascicle lengths and pennation angles when the muscle isin a relaxed and isometrically tensed conditions and that thedifferences are affected by joint angles, at least at thesubmaximal contraction level.

     

Reproducibility of gastrocnemius medialis muscle architecture during treadmill running

The purpose of this study was to assess the reproducibility of fascicle length (FL) and pennation angle (PA) of gastrocnemius medialis (GM) muscle during running in vivo. Twelve male recreational long distance runners (mean ± SD; age: 24 ± 3 years, mass: 76 ± 7 kg) ran on a treadmill at a speed of 3.0 m/s, wearing their own running shoes, for two different 10 min sessions that were at least 2 days apart. For each test day 10 acceptable trials were recorded. Ankle and knee joint angle data were recorded by a Vicon 624 system with three cameras operating at 120 Hz. B-mode ultrasonography was used to examine fascicle length and pennation angle of gastrocnemius medialis muscle. The ultrasound probe was firmly secured on the muscle belly using a lightweight foam fixation. The results indicated that fascicle length and pennation angle demonstrated high reproducibility values during treadmill running both for within and between test days. The root mean square scores between the repeated waveforms of pennation angle and fascicle length were small (∼2° and ∼3.5 mm, respectively). However, ∼14 trials for pennation angle and ∼9 trials for fascicle length may be required in order to record accurate data from muscle architecture parameters. In conclusion, ultrasound measurements may be highly reproducible during dynamic movements such as treadmill running, provided that a proper fixation is used in order to assure the constant location and orientation of the ultrasound probe throughout the movement.     

Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running

Ultrasound imaging has recently been used to distinguish the length changes of muscle fascicles from those of the whole muscle tendon complex during real life movements. The complicated three-dimensional architecture of pennate muscles can however cause heterogeneity in the length changes along the length of a muscle. Here we use ultrasonography to examine muscle fascicle length and pennation angle changes at proximal, distal and midbelly sites of the human gastrocnemius medialis (GM) muscle during walking (4.5 km/h) and running (7.5 km/h) on a treadmill. The results of this study have shown that muscle fascicles perform the same actions along the length of the human GM muscle during locomotion. However the distal fascicles tend to shorten more and act at greater pennation angles than the more proximal fascicles. Muscle fascicles acted relatively isometrically during the stance phase during walking, however during running the fascicles shortened throughout the stance phase, which corresponded to an increase in the strain of the series elastic elements (SEEs) (consisting of the Achilles tendon and aponeurosis). Measurement of the fascicle length changes at the midbelly level provided a good approximation of the average fascicle length changes across the length of the muscle. The compliance of the SEE allows the muscle fascicles to shorten at a much slower speed, more concomitant with their optimal speed for maximal power output and efficiency, with high velocity shortening during take off in both walking and running achieved by recoil of the SEE.     

Effect of resistance training on skeletal muscle-specific force in elderly humans.

This study assessed muscle-specific force in vivo following strength training in old age. Subjects were assigned to training (n = 9, age 74.3 +/- 3.5 yr; mean +/- SD) and control (n = 9, age 67.1 +/- 2 yr) groups. Leg-extension and leg-press exercises (2 sets of 10 repetitions at 80% of the 5 repetition maximum) were performed three times/wk for 14 wk. Vastus lateralis (VL) muscle fascicle force was calculated from maximal isometric voluntary knee extensor torque with superimposed stimuli, accounting for the patella tendon moment arm length, ultrasound-based measurements of muscle architecture, and antagonist cocontraction estimated from electromyographic activity. Physiological cross-sectional area (PCSA) was calculated from the ratio of muscle volume to fascicle length. Specific force was calculated by dividing fascicle force by PCSA. Fascicle force increased by 11%, from 847.9 +/- 365.3 N before to 939.3 +/- 347.8 N after training (P < 0.05). Due to a relatively greater increase in fascicle length (11%) than muscle volume (6%), PCSA remained unchanged (pretraining: 30.4 +/- 8.9 cm(2); posttraining: 29.1 +/- 8.4 cm(2); P > 0.05). Activation capacity and VL muscle root mean square electromyographic activity increased by 5 and 40%, respectively, after training (P < 0.05), indicating increased agonist neural drive, whereas antagonist cocontraction remained unchanged (P > 0.05). The VL muscle-specific force increased by 19%, from 27 +/- 6.3 N/cm(2) before to 32.1 +/- 7.4 N/cm(2) after training (P < 0.01), highlighting the effectiveness of strength training for increasing the intrinsic force-producing capacity of skeletal muscle in old age.     

Relationship between sprint performance and muscle fascicle length in female sprinters

The purpose of this study was to investigate the relationship between sprint performance and architectural characteristics of leg muscles in 26 female 100-m sprinters. Pennation angle and muscle thickness of the vastus lateralis (VL) and gastrocnemius medialis (GM) and lateralis (GL) muscles were measured by B-mode ultrasonography, and fascicle length was estimated. Sprinters had a significantly lower VL pennation angle, but GM and GL pennation angle was similar between sprinters and female control subjects (N = 22). There was no significant correlation between pennation angle and 100-m personal best performance. Sprinters had significantly greater absolute fascicle length in VL and GL than controls, which significantly correlated to 100-m best-record (r = -0.51 and r = -0.44, respectively). Relative fascicle length (VL and GL) were also significantly greater in sprinters than controls. However, there were no significant correlation between relative fascicle length and 100-m best-record (r = -0.36 and r = -0.29, respectively). No relationship was found between the sprint performance and fat-free mass (r = -0.26) or body mass index (r = -0.03). However, there was a significant correlation between percent (%) body fat and 100-m best-record (r = 0.62, p < 0.01). Adjusting the confounding effect of % fat, significant correlations were seen between relative fascicle length and 100-m best-record (VL; r = -0.39 and GL; r = -0.40). Absolute and relative fascicle length were similar in elite female sprinters compared with previous reported values for elite male sprinters (Kumagai et al., 2000). It was concluded that longer fascicle length is associated with greater sprinting performance in sprinters, but there is no gender differences in fascicle length for elite sprinters.     

A comparison of three muscle pennation assumptions and their effect on isometric and isotonic force

Three different pennation angle assumptions are compared to experimental data from Huijing and Woittiez (Neth. J. Zool. 34, 21-32, 1984) that relate fibre length to angle of pennation changes. The assumptions tested are: (1) neglecting pennation; (2) assuming a fixed pennation; and (3) assuming a constant muscle volume and thickness resulting in pennation angle being dependent on fibre length. Each assumption is compared by transforming fibre force/length and force/velocity characteristics to muscle properties. In general, the fixed pennation assumption provides the worst estimate of muscle force output with a peak error of 0.31 Fo during isometric contractions at small muscle lengths. A better estimate of muscle force output was provided by neglecting pennation entirely. The assumption that the pennation angle changed with fibre length maintained an error of less than 0.05 Fo for most lengths and velocities tested and provided the best estimate of muscle force output.     

Sprint performance is related to muscle fascicle length in male 100-m sprinters.

The purpose of this study was to investigate the relationship between muscle fascicle length and sprint running performance in 37 male 100-m sprinters. The sample was divided into two performance groups by the personal-best 100-m time: 10.00-10.90 s (S10; n = 22) and 11.00-11.70 s (S11; n = 15). Muscle thickness and fascicle pennation angle of the vastus lateralis and gastrocnemius medialis and lateralis muscles were measured by B-mode ultrasonography, and fascicle length was estimated. Standing height, body weight, and leg length were similar between groups. Muscle thickness was similar between groups for vastus lateralis and gastrocnemius medialis, but S10 had a significantly greater gastrocnemius lateralis muscle thickness. S10 also had a greater muscle thickness in the upper portion of the thigh, which, given similar limb lengths, demonstrates an altered "muscle shape." Pennation angle was always less in S10 than in S11. In all muscles, S10 had significantly greater fascicle length than did S11, which significantly correlated with 100-m best performance (r values from -0.40 to -0.57). It is concluded that longer fascicle length is associated with greater sprinting performance.     

Comparison of fascicle behaviors between superficial and deeper muscles of triceps brachii during isometric contractions

PurposeWe assessed fascicle behaviors of the upper extremities during isometric contractions at different joint angles in this study.MethodsThirteen healthy men and women performed isometric elbow extension tasks at 50% and 75% of maximal voluntary contraction (MVC) at 60°, 90°, and 120° of elbow extension (full extension = 180°). Extended field-of-view B-mode ultrasonography was used to obtain sagittal plane panoramic images of the long head (TB-Long) and medial head (TB-Med) of the triceps brachii at rest and during contraction; fascicle length and pennation angle were measured.ResultsIn the TB-Long, significant fascicle shortening from rest was found during 50% and 75%MVC at 60° and during 75%MVC at 90° of extension. There was no significant fascicle shortening in the TB-Med muscle under any conditions. There was no significant pennation angle change from rest in either muscle. The pennation angle of the TB-Long was significantly greater than that of the TB-Med under all conditions.ConclusionsThese results suggest that fascicle shortening in the TB-Long muscle occurs in flexion; however, no change was found in the TB-Med. In the upper extremity muscle–tendon complex, the superficial and deeper muscles may have different force-transmission efficiency at flexed joint angles.     

A novel method of studying fascicle architecture in relaxed and contracted muscles

A muscle’s architecture, described by geometric variables such as fascicle pennation angles or lengths, plays a crucial role in its functionality. Usually, single parameters are used to estimate force vectors or lengthening rates, thereby assuming that they represent the architecture properly and are constant during contraction. To describe muscle architecture in more detail and compare relaxed and contracted states, we developed and validated a new approach. The m. soleus of the laboratory rat was shock-frozen while relaxed and under isometric contraction, reconstructed three-dimensionally from histological sections, and fascicle lengths, curvatures and pennation angles, as well as the shape of the aponeuroses were analysed. Remarkable differences in volume distribution and the shapes of the aponeuroses as well as locally varying changes in the fascicle architecture were observed. While the mean pennation angle increased by only 2° due to contraction, local changes of up to 4° were observed. Fascicle curvature increased in the distal but remained unchanged in the proximal parts. Our approach may help to identify functional subunits within the muscle, i.e., regions with homogeneous architectural properties. Our results are discussed regarding the input parameters essential for realistic muscle modelling and challenge maximum isometric force estimations that are based on the physiological cross-sectional area or the Hill-model.