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.     

Functional specialisation of the thoracic limb of the hare (Lepus europeus)

We provide quantitative anatomical data on the muscle-tendon architecture of the hare thoracic limb (specifically muscle mass, fascicle length, pennation angle, tendon mass and length). In addition, moment arms of major thoracic limb muscles were measured. Maximum isometric force and power of muscles, the moment of force about a joint, and tendon stress and strain were estimated. Data are compared with those from other cursorial mammals. The thoracic limb of the hare consists predominantly of extrinsic musculature with long parallel fascicles, specialised for generating force over a large range. A large shoulder flexor/elbow extensor muscle mass is present, in particular Triceps brachii. The pennate nature of the long head of this muscle suggests it has an important role in stabilising the elbow joint during stance, whilst moment arm curves suggest that it may also play a role in initiating shoulder flexion. In addition, Supraspinatus and Infraspinatus are capable of generating high forces, potentially to stabilise the shoulder joint during the stance phase of locomotion. Supraspinatus may in addition play an important role in forelimb protraction. The Subscapularis muscle was capable of generating surprisingly high forces, suggesting that the hare must be able to withstand/produce high forces during activities that need medio-lateral stability, such as turning. Distally, tendons were relatively short, showing little potential for elastic energy storage when compared with both their pelvic limb counterparts and their equivalents in the horse thoracic limb. Thus, a 'stiffer' thoracic limb may be beneficial in terms of behaving like a strut, simply supporting and deflecting the body during high-speed running. This more distal/less proximal distribution of limb mass is also likely to be important in retaining the manipulative/adaptive/non-locomotor capabilities of the limb.     

Functional specialisation of pelvic limb anatomy in horses (Equus caballus)

We provide quantitative anatomical data on the muscle-tendon units of the equine pelvic limb. Specifically, we recorded muscle mass, fascicle length, pennation angle, tendon mass and tendon rest length. Physiological cross sectional area was then determined and maximum isometric force estimated. There was proximal-to-distal reduction in muscle volume and fascicle length. Proximal limb tendons were few and, where present, were relatively short. By contrast, distal limb tendons were numerous and long in comparison to mean muscle fascicle length, increasing potential for elastic energy storage. When compared with published data on thoracic limb muscles, proximal pelvic limb muscles were larger in volume and had shorter fascicles. Distal limb muscle architecture was similar in thoracic and pelvic limbs with the exception of flexor digitorum lateralis (lateral head of the deep digital flexor), the architecture of which was similar to that of the pelvic and thoracic limb superficial digital flexors, suggesting a functional similarity.     

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

We provide quantitative muscle–tendon architecture and geometry data for the racing greyhound thoracic limb. Muscle mass, belly length, fascicle lengths, pennation angles and moment arms were measured, as were tendon masses and lengths. Maximum isometric force and maximum power were estimated for muscles, and maximum stress and strain were estimated for tendons. Results are compared with other fast quadrupedal runners, and to previously published data in mixed‐breed dogs. The implications of the functional adaptations of the greyhound thoracic limb for sprinting performance are discussed. The thoracic limb was found to benefit from a similar proportion of locomotor muscle mass to the pelvic limb, suggesting that it may be used to some extent in propulsion, or alternatively that stabilisation is very important in this animal. Extrinsic muscles, especially latissimus dorsi and pectoralis profundus, were predicted to be powerful and important for generating net positive work during accelerations. Proximal biarticular muscles show specialisation toward preventing collapse of the shoulder and elbow joints to enable strut‐like limb function, or some form of dynamic control. Distal muscles did not appear specialised for elastic energy storage, a functional difference to pelvic limb muscles, and the equivalents in horse thoracic limbs. The greyhound thoracic limb appears to possess substantial differences from both that of more ‘sub‐maximal specialist’ quadrupeds, and from the greyhound pelvic limb.     

The Arrangement of Fascicles in Whole Muscle

The architecture of the muscle fascicles, here meaning their lengths and their arrangement relative to one another, has important implications for the force a muscle can produce. Therefore, quantifying this architectural arrangement and understanding the implications of the architecture are important for understanding muscle function in vivo. There were two purposes of this study: (1) to assess, via blunt dissection, the number and the length of all the fascicles comprising the First Dorsal Interosseous (FDI) muscle and (2) to visually identify, via magnetic resonance imaging (MRI), the arrangement of the fascicles comprising the FDI. Simple blunt dissection of all the fascicles comprising four FDI muscles and their subsequent measurement demonstrated that the fascicles comprising the whole muscle were not as long as the muscle belly from which they were extracted. Muscle fascicles are surrounded by connective tissue hence the paths of the fascicles in two whole FDI muscles were identified via MRI by tracking the connective tissue surrounding the fascicles. The fascicles had a spiral pattern along the length of each muscle, within both muscles many of the fascicles were arranged in series with other fascicles. These architectural features of the fascicles of the FDI have important implications for the force–length and force–velocity properties of the whole muscle. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.     

Morphological analysis of the hindlimb in apes and humans. I. Muscle architecture

We present quantitative data on the hindlimb musculature of Pan paniscus, Gorilla gorilla gorilla, Gorilla gorilla graueri, Pongo pygmaeus abelii and Hylobates lar and discuss the findings in relation to the locomotor habits of each. Muscle mass and fascicle length data were obtained for all major hindlimb muscles. Physiological cross-sectional area (PCSA) was estimated. Data were normalized assuming geometric similarity to allow for comparison of animals of different size/species. Muscle mass scaled closely to (body mass)(1.0) and fascicle length scaled closely to (body mass)(0.3) in most species. However, human hindlimb muscles were heavy and had short fascicles per unit body mass when compared with non-human apes. Gibbon hindlimb anatomy shared some features with human hindlimbs that were not observed in the non-human great apes: limb circumferences tapered from proximal-to-distal, fascicle lengths were short per unit body mass and tendons were relatively long. Non-human great ape hindlimb muscles were, by contrast, characterized by long fascicles arranged in parallel, with little/no tendon of insertion. Such an arrangement of muscle architecture would be useful for locomotion in a three dimensionally complex arboreal environment.     

Functional anatomy of the gibbon forelimb: adaptations to a brachiating lifestyle

It has been shown that gibbons are able to brachiate with very low mechanical costs. The conversion of muscle activity into smooth, purposeful movement of the limb depends on the morphometry of muscles and their mechanical action on the skeleton. Despite the gibbon's reputation for excellence in brachiation, little information is available regarding either its gross musculoskeletal anatomy or its more detailed muscle–tendon architecture. We provide quantitative anatomical data on the muscle–tendon architecture (muscle mass, physiological cross-sectional area, fascicle length and tendon length) of the forelimb of four gibbon species, collected by detailed dissections of unfixed cadavers. Data are compared between different gibbon species and with similar published data of non-brachiating primates such as macaques, chimpanzees and humans. No quantitative differences are found between the studied gibbon species. Both their forelimb anatomy and muscle dimensions are comparable when normalized to the same body mass. Gibbons have shoulder flexors, extensors, rotator muscles and elbow flexors with a high power or work-generating capacity and their wrist flexors have a high force-generating capacity. Compared with other primates, the elbow flexors of gibbons are particularly powerful, suggesting that these muscles are particularly important for a brachiating lifestyle. Based on this anatomical study, the shoulder flexors, extensors, rotator muscles, elbow flexors and wrist flexors are expected to contribute the most to brachiation.     

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.     

Muscle moment arms of the gibbon hind limb: implications for hylobatid locomotion

Muscles facilitate skeletal movement via the production of a torque or moment about a joint. The magnitude of the moment produced depends on both the force of muscular contraction and the size of the moment arm used to rotate the joint. Hence, larger muscle moment arms generate larger joint torques and forces at the point of application. The moment arms of a number of gibbon hind limb muscles were measured on four cadaveric specimens (one Hylobates lar, one H. moloch and two H. syndactylus). The tendon travel technique was used, utilizing an electro‐goniometer and a linear voltage displacement transducer. The data were analysed using a technique based on a differentiated cubic spline and normalized to remove the effect of body size. The data demonstrated a functional differentiation between voluminous muscles with short fascicles having small muscle moment arms and muscles with longer fascicles and comparatively smaller physiological cross‐sectional area having longer muscle moment arms. The functional implications of these particular configurations were simulated using a simple geometric fascicle strain model that predicts that the rectus femoris and gastrocnemius muscles are more likely to act primarily at their distal joints (knee and ankle, respectively) because they have short fascicles. The data also show that the main hip and knee extensors maintain a very small moment arm throughout the range of joint angles seen in the locomotion of gibbons, which (coupled to voluminous, short‐fascicled muscles) might help facilitate rapid joint rotation during powerful movements.     

Functional specialisation of the pelvic limb of the hare (Lepus europeus)

We provide quantitative anatomical data on the muscle-tendon architecture of the hare pelvic limb (specifically muscle mass, fascicle length, pennation angle, tendon mass and length). In addition, moment arms of major pelvic limb muscles were measured. Maximum isometric force and power of muscles, the moment of force about a joint, and tendon stress and strain were estimated. Data are compared with published data for other cursorial mammals such as the horse and dog, and a non-specialised Lagamorph, the rabbit. The pelvic limb of the hare was found to contain substantial amounts of hip extensor and adductor/abductor muscle volume, which is likely to be required for power production and stability during rapid turning. A proximal to distal reduction in muscle volume and fascicle length was also observed, as is the case in other cursorial quadrupeds, along with a reduction in distal limb mass via the replacement of muscle volume by long distal limb tendons, capable of storing large amounts of elastic energy. The majority of hare pelvic limb muscle moment arms varied with joint position, giving the hare the capacity to vary muscle function with limb posture and presumably different locomotor activities.     

Muscle architecture of biceps brachii, triceps brachii and supraspinatus in the horse

Three muscles from the proximal equine forelimb were dissected in order to investigate their potential to contribute to proximal limb mechanics. Muscle mass, fibre length, tendon mass and tendon length were measured from biceps brachii, triceps brachii, supraspinatus and lacertus fibrosus (biceps lateral head mass 171-343.4 g and fibre length 0.5-0.8 cm; biceps medial head mass 283-500 g and fibre length 2.2-4 cm; biceps tendon mass 121.8-260 g and tendon length 35-44 cm; triceps long head mass 3200-6663 g and fibre length 19-26.3 cm; triceps lateral head mass 513.8-1240 g and fibre length 17.5-24 cm; triceps medial head mass 85.2-270.6 g and fibre length 9-16.8 cm; supraspinatus mass 793-1546 g and fibre length 4.7-12.4 cm; lacertus fibrosus mass 4.6-12.4 g and length 10-16 cm). Physiological cross-sectional area (PCSA) and maximum isometric force were estimated for each muscle, and moment arm measurements were taken at the shoulder and elbow joints. Biceps has a greater isometric force-generating capacity than supraspinatus. It also appears to have a larger shoulder moment arm, so could therefore have the potential to make a greater contribution to the shoulder moment than supraspinatus. Supraspinatus is likely to function primarily as a shoulder stabilizer rather than a shoulder extensor. Biceps also functions as an elbow flexor and data here indicate that it has a greater PCSA and isometric force-generating capacity than its antagonist triceps brachii. Calculation of tendon forces showed that the biceps tendon can withstand much greater forces than lacertus fibrosus. This study will enable further investigation into the interaction between energy recycling in elastic tissues and the generation and absorption of mechanical work by adjacent muscle groups in the equine forelimb.     

The scaling of postcranial muscles in cats (Felidae) I: forelimb,cervical, and thoracic muscles

The body masses of cats (Mammalia, Carnivora, Felidae) span a ~300‐fold range from the smallest to largest species. Despite this range, felid musculoskeletal anatomy remains remarkably conservative, including the maintenance of a crouched limb posture at unusually large sizes. The forelimbs in felids are important for body support and other aspects of locomotion, as well as climbing and prey capture, with the assistance of the vertebral (and hindlimb) muscles. Here, we examine the scaling of the anterior postcranial musculature across felids to assess scaling patterns between different species spanning the range of felid body sizes. The muscle architecture (lengths and masses of the muscle‐tendon unit components) for the forelimb, cervical and thoracic muscles was quantified to analyse how the muscles scale with body mass. Our results demonstrate that physiological cross‐sectional areas of the forelimb muscles scale positively with increasing body mass (i.e. becoming relatively larger). Many significantly allometric variables pertain to shoulder support, whereas the rest of the limb muscles become relatively weaker in larger felid species. However, when phylogenetic relationships were corrected for, most of these significant relationships disappeared, leaving no significantly allometric muscle metrics. The majority of cervical and thoracic muscle metrics are not significantly allometric, despite there being many allometric skeletal elements in these regions. When forelimb muscle data were considered in isolation or in combination with those of the vertebral muscles in principal components analyses and MANOVAs, there was no significant discrimination among species by either size or locomotory mode. Our results support the inference that larger felid species have relatively weaker anterior postcranial musculature compared with smaller species, due to an absence of significant positive allometry of forelimb or vertebral muscle architecture. This difference in strength is consistent with behavioural changes in larger felids, such as a reduction of maximal speed and other aspects of locomotor abilities.     

Structural and functional anatomy of the neck musculature of the dog (Canis familiaris)

The morphometric properties and the anatomical relationships of the entire musculature of the canine cervical spine are reported herein. These data were obtained from the dissection of cadavers of six dogs. Total muscle length, muscle weight, fascicle length and angles of pennation were recorded for each muscle comprising the canine cervical spine. Based upon these properties, physiological cross-section area (PCSA) and architectural index were estimated. When scaled by whole body mass, the values of each of these parameters were found to be similar between all dogs. Muscles that course from the cranial neck to the shoulder girdle or the rib cage (e.g. brachiocephalicus and rhomboideus capitis) were found to have relatively long fascicles and low PCSA values and thus appear to be designed for rapid excursions. By contrast, muscles that primarily support the neck and shoulder against gravitational forces (e.g. serratus ventralis and trapezius) were found to have relatively high PCSA values and short fascicle lengths, and thus have the capacity to generate large forces. Differences of morphometry as well as nomenclature were found between the canine and human neck musculature. Nevertheless, many similarities exist; in particular, both species have similar muscles adapted to force generation or large excursions. We thus conclude that the canine neck may be used as a modelling tool for biomechanical investigations of the human cervical region as long as the differences listed are borne in mind.     

Comparative anatomy and muscle architecture of selected hind limb muscles in the Quarter Horse and Arab

The Quarter Horse (bred for acceleration) and the Arab (bred for endurance) are situated at either end of the equine athletic spectrum. Studies into the form and function of the leg muscles in human sprint and endurance runners have demonstrated that differences exist in their muscle architecture. It is not known whether similar differences exist in the horse. Six Quarter Horse and six Arab fresh hind limb cadavers were dissected to gain information on the muscle mass and architecture of the following muscles: gluteus medius; biceps femoris; semitendinosus; vastus lateralis; gastrocnemius; tibialis cranialis and extensor digitorum longus. Specifically, muscle mass, fascicle length and pennation angle were quantified and physiological cross-sectional area (PCSA) and maximum isometric force were estimated. The hind limb muscles of the Quarter Horse were of a significantly greater mass, but had similar fascicle lengths and pennation angles when compared with those of the Arab; this resulted in the Quarter Horse hind limb muscles having greater PCSAs and hence greater isometric force potential. This study suggests that Quarter Horses as a breed inherently possess large strong hind limb muscles, with the potential to accelerate their body mass more rapidly than those of the Arab.     

Dimensions of forelimb muscles in orangutans and chimpanzees

Eight forelimbs of three orangutans and four chimpanzees were dissected and the muscle mass, fascicle length and physiological cross-sectional area (PCSA) of all forelimb muscles were systematically recorded to explore possible interspecies variation in muscle dimensions. Muscle mass and PCSA were divided by the total mass and total PCSA of the entire forelimb muscles for normalization. The results indicate that the mass and PCSA ratios of the monoarticular elbow flexors ( M. brachialis and M. brachioradialis ) are significantly larger in orangutans. In contrast, the mass ratios of the biarticular muscles in the upper arm (the short head of M. biceps brachii and the long head of M. triceps brachii ) are significantly larger in chimpanzees. For the rotator cuff muscles, the force-generating capacity of M. subscapularis is significantly larger in orangutans, whereas the opposite rotator cuff muscle, M. infraspinatus , is larger in chimpanzees. These differences in forelimb muscle dimensions of the two species may reflect functional specialization for their different positional and locomotor behaviors.     

Muscle length affects the architecture and pattern of innervation differently in leg muscles of mouse, guinea pig, and rabbit compared to those of human and monkey muscles

The innervation pattern and fascicular anatomy of muscles of different lengths in mouse, guinea pig, rabbit, macaque monkey and human legs were analyzed. Neuromuscular junctions, muscle tendon junctions and ends of intrafascicularly terminating fibers were stained for acetylcholinesterase, and fascicle lengths measured. A high correlation between increasing fascicle length and increasing number of neuromuscular junctions was found, with non-primate (mouse, guinea pig, rabbit) and primate (macaque monkey, human) muscles forming two discrete groups. In non-primates, muscles with a single endplate band, fascicles were always shorter than 35 mm, fixing the limit of fiber length served by one neuromuscular junction. Muscles with fascicles longer than this had multiple discrete bands of motor endplates crossing their width at regular intervals. An increase in muscle length across or within species corresponded to an equivalent, standard increase of 10-12 mm fascicle length per motor endplate band. All human and monkey leg muscles, with the exception of gracilis and sartorius, were singly innervated and all muscle fibers ran the full distance from tendon to tendon. Singly innervated primate muscle fibers were up to 140 mm long whereas the mean distance between endplate bands in the two multiply innervated muscles was also considerably greater than in non-primates. These data indicate that allometric effects of increasing fascicle length, are distinct in common laboratory animals and two primates, when architecture and pattern of innervation are compared.     

Muscle moment arms and function of the siamang forelimb during brachiation

Moment arms have an important modulating impact on muscle function, as they represent the capacity of the muscle to convert muscle action into limb movements. In the current paper, we provide muscle moment arm data of the forelimb of four siamangs, collected by detailed dissections on unfixed cadavers. The aim of this study is to assess the role of different forelimb muscles during brachiation. Moment arm data are compared with similar published data of non‐brachiating primates such as macaques, chimpanzees and humans. Our data show that shoulder adductors and endorotators and the elbow flexors are built for force generation, whereas the shoulder abductors, flexors and exorotators are best suited to gain speed and to change direction. Compared to non‐brachiating species, both elbow and wrist flexors are particularly noticeable in terms of moment of force‐generating capacity. However, the moment of force‐generating capacity of the elbow extensor is not negligible, which indicates that the triceps also plays an active role, especially at the end of the support phase. Except for the elbow flexors, all muscles reach their maximum moment of force‐generating capacity during the support phase of brachiation. When brachiating on a more complex setup, the siamang will flex the elbows to angles that induce maximum moment arms as well.     

Relationship between myoelectric and mechanical manifestations of fatigue in the quadriceps femoris muscle group

Fatigue is commonly defined as “the failure to maintain the required force”. As such, it may be argued that the use of electromyographic (EMG) power spectral statistics to monitor muscle fatigue is inappropriate, because, during the maintenance of a submaximal force of contraction, EMG changes are readily observable in the absence of any decline in the muscle's mechanical output. However, it is possible that the EMG changes reflect the changing metabolic status of the muscle and hence its inability to generate its normal maximal force. The present study sought to examine whether the decline in EMG median frequency, which occurs during the maintenance of a submaximal force, is correlated with a reduction in the muscle's maximum force-generating capacity. The maximum voluntary contraction (MVC) of the knee extensors in ten young, healthy subjects was determined. On five separate occasions, randomly assigned forces of 20, 30, 40, 50 and 60% MVC were held to the limit of endurance. At intervals throughout the sustained contractions, subjects were required to rapidly generate an MVC for 1–2 s, then return to the fixed submaxial target force. Surface EMG signals were recorded throughout the contractions from the rectus lemons and vastus lateralis muscles, from which the power spectrum median frequency was calculated. Regression analysis revealed highly significant relationships between the rate of decline in MF and the rate of decline in MVC, and between each of these parameters and endurance time to fatigue (P = 0.0001, in each case). It is concluded that the decline in MF can be used to monitor fatigue, where fatigue is defined as the inability to generate the maximum force that can be produced by the muscle in its fresh state.     

A comparison of the moment arms of pelvic limb muscles in horses bred for acceleration (Quarter Horse) and endurance (Arab)

Selective breeding for performance has resulted in distinct breeds of horse, such as the Quarter Horse (bred for acceleration) and the Arab (bred for endurance). Rapid acceleration, seen during Quarter Horse racing, requires fast powerful muscular contraction and the generation of large joint torques, particularly by the hind limb muscles. This study compared hind limb moment arm lengths in the Quarter Horse and Arab. We hypothesized that Quarter Horse hind limb extensor muscles would have longer moment arms when compared to the Arab, conferring a greater potential for torque generation at the hip, stifle and tarsus during limb extension. Six Quarter Horse and six Arab hind limbs were dissected to determine muscle moment arm lengths for the following muscles: gluteus medius, biceps femoris, semitendinosus, vastus lateralis, gastrocnemius (medialis and lateralis) and tibialis cranialis. The moment arms of biceps femoris (acting at the hip) and gastrocnemius lateralis (acting at the stifle) were significantly longer in the Quarter Horse, although the length of the remaining muscle moment arms were similar in both breeds of horse. All the Quarter Horse muscles were capable of generating greater muscle moments owing to their greater physiological cross-sectional area (PCSA) and therefore greater isometric force potential, which suggests that PCSA is a better determinant of muscle torque than moment arm length in these two breeds of horse. With the exception of gastrocnemius and tibialis cranialis, the observed muscle fascicle length to moment arm ratio (MFL : MA ratio) was greater for the Arab horse muscles. It appears that the Arab muscles have the potential to operate at slower velocities of contraction and hence generate greater force outputs when compared to the Quarter Horse muscles working over a similar range of joint motion; this would indicate that Arab hind limb muscles are optimized to function at maximum economy rather than maximum power output.