Functional Analysis of the Primate Shoulder

Studies of the shoulder girdle are in most cases restricted to morphological comparisons and rarely aim at elucidating function in a strictly biomechanical sense. To fill this gap, we investigated the basic functional conditions that occur in the shoulder joint and shoulder girdle of primates by means of mechanics. Because most of nonhuman primate locomotion is essentially quadrupedal walking—although on very variable substrates—our analysis started with quadrupedal postures. We identified the mechanical situation at the beginning, middle, and end of the load-bearing stance phase by constructing force parallelograms in the shoulder joint and the scapulo-thoracal connection. The resulting postulates concerning muscle activities are in agreement with electromyographical data in the literature. We determined the magnitude and directions of the internal forces and explored mechanically optimal shapes of proximal humerus, scapula, and clavicula using the Finite Element Method. Next we considered mechanical functions other than quadrupedal walking, such as suspension and brachiation. Quadrupedal walking entails muscle activities and joint forces that require a long scapula, the cranial margin of which has about the same length as the axillary margin. Loading of the hand in positions above the head and suspensory behaviors lead to force flows along the axillary margin and so necessitate a scapula with an extended axillary and a shorter cranial margin. In all cases, the facies glenoidalis is nearly normal to the calculated joint forces. In anterior view, terrestrial monkeys chose a direction of the ground reaction force requiring (moderate) activity of the abductors of the shoulder joint, whereas more arboreal monkeys prefer postures that necessitate activity of the adductors of the forelimb even when walking along branches. The same adducting and retracting muscles are recruited in various forms of suspension. As a mechanical consequence, the scapula is in a more frontal, rather than parasagittal, position on the thorax. In both forms of locomotion—quadrupedal walking and suspension—the compression-resistant clavicula contributes to keeping the shoulder complex distant from the rib cage. Future studies should consider the consequences for thorax shape. The morphological specializations of all Hominoidea match the functional requirements of suspensory behavior. The knowledge of mechanical functions allows an improved interpretation of fossils beyond morphological similarity.     

Functional analysis of the shoulder girdle of cats during locomotion

The movements of the shoulder girdle of eight adult cats during overground stepping were studied, using standard slow motion cinematographic techniques. The patterns of activity of shoulder muscles were examined, using simultaneous intramuscular electromyography. Walking, trotting and galloping steps were analyzed from digitized single motion picture frame images. Angular movements of the shoulder girdle consist of biphasic flexion and extension of the shoulder joint and a monophasic flexion-extension alternation of the scapula on the thorax during each step cycle. In addition, the center of the scapula moves craniad during the swing phase and caudad during the stance phase with respect to a fixed reference point on the animal. Similar vertical movements of the center of the scapula also occur in each step cycle. Results of EMG studies of the 17 muscles capable of acting on the shoulder girdle indicate that three overall patterns of activity are found: (1) a pattern typical of extensor muscles, active during all the extension epochs; (2) a pattern typical of flexor muscles, active during the flexion epoch; and (3) a biphasic pattern of activity, active twice in each step. There data are used, along with a re-examination of previous models of the mechanics of the shoulder girdle of carnivores to examine the function and mechanics of shoulder motion. It is concluded that the rotary and translatory movements of the shoulder girdle during stepping combine to enhance step length.     

Morphometric affinities of the human shoulder

To analyze differences between apes and monkeys and the affinities of man, we have studied the shoulder girdle of 327 specimens of anthropoid primates. The scapula, clavicle and humerus are viewed as an integrated functional complex on the basis of 18 measurements. Several varieties of multivariate analysis show that man is clearly closer to other hominoids than to the included monkey taxa (whether terrestrial or arboreal, Old World or New World). The marked shoulder differences between apes and monkeys and similarities between apes and man correlate with the muscular anatomy, which in hominoids allows the motions involved in their locomotion and feeding behavior. As the hominid-pongid correspondence in shoulder morphology is especially detailed regarding the functionally important joint surfaces, it is consistent with a fairly recent period of common ancestry and behavior. No hypothetical evolutionary pathway or ancestral form of the human shoulder need look far beyond the model afforded by extant pongids. In contrast with previous studies on the primate shoulder, these results agree with information accumulating from other systems—comparative anatomy, primate behavior, and molecular biology — in suggesting very close relationship between man and extant African pongids.     

Evaluation of regression-based 3-D shoulder rhythms

The movements of the humerus, the clavicle, and the scapula are not completely independent. The coupled pattern of movement of these bones is called the shoulder rhythm. To date, multiple studies have focused on providing regression-based 3-D shoulder rhythms, in which the orientations of the clavicle and the scapula are estimated by the orientation of the humerus. In this study, six existing regression-based shoulder rhythms were evaluated by an independent dataset in terms of their predictability. The datasets include the measured orientations of the humerus, the clavicle, and the scapula of 14 participants over 118 different upper arm postures. The predicted orientations of the clavicle and the scapula were derived from applying those regression-based shoulder rhythms to the humerus orientation. The results indicated that none of those regression-based shoulder rhythms provides consistently more accurate results than the others. For all the joint angles and all the shoulder rhythms, the RMSE are all greater than 5°. Among those shoulder rhythms, the scapula lateral/medial rotation has the strongest correlation between the predicted and the measured angles, while the other thoracoclavicular and thoracoscapular bone orientation angles only showed a weak to moderate correlation. Since the regression-based shoulder rhythm has been adopted for shoulder biomechanical models to estimate shoulder muscle activities and structure loads, there needs to be further investigation on how the predicted error from the shoulder rhythm affects the output of the biomechanical model.     

Three-dimensional kinematic analysis of the pectoral girdle during upside-down locomotion of two-toed sloths (Choloepus didactylus, Linné 1758)

Background

Theria (marsupials and placental mammals) are characterized by a highly mobile pectoral girdle in which the scapula has been shown to be an important propulsive element during locomotion. Shoulder function and kinematics are highly conservative during locomotion within quadrupedal therian mammals. In order to gain insight into the functional morphology and evolution of the pectoral girdle of the two-toed sloth we here analyze the anatomy and the three-dimensional (3D) pattern of shoulder kinematics during quadrupedal suspensory ('upside-down') locomotion.

Methods

We use scientific rotoscoping, a new, non-invasive, markerless approach for x-ray reconstruction of moving morphology (XROMM), to quantify in vivo the 3D movements of all constituent skeletal elements of the shoulder girdle. Additionally we use histologic staining to analyze the configuration of the sterno-clavicular articulation (SCA).

Results

Despite the inverse orientation of the body towards gravity, sloths display a 3D kinematic pattern and an orientation of the scapula relative to the thorax similar to pronograde claviculate mammalian species that differs from that of aclaviculate as well as brachiating mammals. Reduction of the relative length of the scapula alters its displacing effect on limb excursions. The configuration of the SCA maximizes mobility at this joint and demonstrates a tensile loading regime between thorax and limbs.

Conclusions

The morphological characteristics of the scapula and the SCA allow maximal mobility of the forelimb to facilitate effective locomotion within a discontinuous habitat. These evolutionary changes associated with the adoption of the suspensory posture emphasized humeral influence on forelimb motion, but allowed the retention of the plesiomorphic 3D kinematic pattern.     

Effect of axis alignment on in vivo shoulder kinematics

Background. To describe 3D shoulder joint movements, the International Society of Biomechanics (ISB) recommends using segment coordinate systems (SCSs) on the humerus, scapula and thorax, and joint coordinate systems (JCSs) on the shoulder. However, one of the remaining problems is how to define the zero angles when the arm is in an initial reference position. The aim of this paper is to compare various methods of determining the JCSs of the shoulder that make it possible to define the zero angles of the arm in the resting position.

Methods. Able-bodied subjects performed elevation movements in the scapular plane, specifically neutral, internal and external rotations of the humerus. The initial humerus position (at the beginning of the arm movement) and range of motion were analysed for the purpose of clinical interpretation of arm attitude and movement. The following four different JCSs were explored: (1) the standard JCS, defined as recommended by the ISB, (2) a first aligned JCS, where the humerus SCS is initially aligned with the scapula SCS, (3) a second aligned JCS, where the opposite operation is performed and 4) a third aligned JCS, where both the humerus and the scapular SCS are initially aligned with the thorax SCS.

Findings. The second aligned JCS was the only method that did not produce any exaggerated range of movement in either anatomical plane.

Interpretation. Mathematical JCS alignment allows clearer clinical interpretation of arm attitude and movement.     

Scapular position in primates

Scapular position affects shoulder mobility, which plays an important role in the upper limb adaptations in primates. However, currently available data on scapular position are unsatisfactory because of the failure to simultaneously consider the relative dimensions of all the three skeletal elements of the shoulder girdle, i.e. the clavicle, the scapula and the thorax. In the present study, the clavicular length and the scapular spine length were measured on preserved cadavers, and the dorsoventral thoracic diameter was measured on scaled radiographs of a wide range of primates, permitting a quantitative comparison of scapular position among primates. It was found that arboreal monkeys have a more dorsally situated scapula than terrestrial ones, but the same difference was not found between terrestrial and arboreal prosimians. Hominoids were found to have the most dorsally situated scapula. Contrary to the slow climbing theory of hominoid evolution, which tries to explain most postcranial specializations of hominoids as adaptations for slow climbing, the scapulae of slow-climbing lorines and Alouatta are much less dorsal than those of the hominoids.     

Shoulder joint kinematics during elevation measured by ultrasound-based measuring system.

In order to analyze shoulder joint movements, the authors use a ZEBRIS CMS-HS ultrasound-based movement analysis system. In essence, the measurement involves the determination of the spatial position of the 16 anatomical points, which are specified on the basis of the coordinates of ultrasound-based triplets positioned on the upper limb, the scapula, and the thorax; their spatial position is measured in the course of motion. Kinematic characteristics of 74 shoulder joints of 50 healthy persons were identified during elevation in the plane of the scapula. Kinematic characteristics of motion were identified by scapulothoracic, glenohumeral, and humeral elevation angles; range of angles; scapulothoracis and glenohumeral rhythm; scapulothoracic, glenohumeral, and scapuloglenoid ratios; and the relative displacement between the rotation centers of the humerus and the scapula. Motion of the humerus and the scapula relative to each other was characterized by their rotation as well as the relative displacement between the rotation centers of scapula and humerus. The biomechanical model of the shoulder joint during elevation can be described by analyzing the results of the measurements performed.     

Postural differences in shoulder dynamics during pushing and pulling

Assessments of shoulder dynamics (e.g. the inertial, viscous, and stiffness properties of the joint) can provide important insights into the stability of the joint at rest and during volitional contraction. The purpose of this study was to investigate how arm posture influences shoulder dynamics while generating pushing or pulling torques in the horizontal plane. Sixteen healthy participants were examined in seven postures encompassing a large workspace of the shoulder. At each posture, the participant’s shoulder was rapidly perturbed while measuring the resultant change in shoulder torque about the glenohumeral axis. Participants were examined both at rest and while producing horizontal flexion and extension torques scaled to 15% of a maximum voluntary contraction. Shoulder stiffness, viscosity, and damping ratio were estimated using impedance-based matching, and changes in these outcome measures with torque level, elevation angle, and plane of elevation angle were explored with a linear mixed effects model. Shoulder stiffness was found to decrease with increasing elevation angles (p < 0.001) without subsequent changes in viscosity, leading to a greater damping ratios at higher elevation angles (p < 0.001). Shoulder stiffness, viscosity, and damping ratio (all p < 0.05) were all found to significantly increase as the plane of elevation of the arm was increased. The relationship between the viscosity, stiffness and the damping ratio of the shoulder is one that the central nervous system must regulate in order to maintain stability, protect against injury, and control the shoulder joint as the inertial and muscle contributions change across different arm postures.     

MSCT-3D技术在动物与人骨骼形态比较研究中的应用

目的应用MSCT-3D显示技术比较正常贵州香猪、Marshall比格犬、恒河猴与人上肢带骨及躯干骨的形态学差异。方法采用MSCT分别对贵州香猪、比格犬和恒河猴进行CT全身扫描并进行图像重建,观察其上肢带骨、躯干骨形态结构与人的异同。结果比格犬、恒河猴、贵州香猪脊椎骨和肋的基本组成与人相同,脊椎骨由椎体和附件组成,肋骨包括真肋、假肋和浮肋。而脊柱曲度、各段椎骨数目、胸骨结构、肋的数目、胸肋连接、上肢带骨的组成与人不同,恒河猴的脊柱曲度和上肢带骨连接与人相同,有颈、胸、腰、骶四个生理性弯曲并由锁骨和肩胛骨共同连接自由上肢骨,比格犬和贵州香猪只有颈、胸腰、骶三个生理性弯曲,仅由肩胛骨连接自由上肢骨。结论恒河猴躯干骨和上肢带骨与人有良好的相似性,而比格犬和贵州香猪与人差别较大。MSCT-3D技术为实验动物形态学比较研究提供了一种相对无创、快速、可以在体研究并动态连续观察的科学有效方法。     

Locomotion and feeding postures of spider and howling monkeys: field study and evolutionary interpretation

Field observations demonstrate clear differences in locomotion and feeding postures between spider monkeys (Ateles) and howling monkeys (Alouatta). When feeding, Ateles employs sitting postures approximately half the time, and a variety of suspensory postures using the tail the other half. Ateles moves quadrupedally during 52% of locomotion, by tail-arm suspension 25%, and various mixed support-suspensory modes the remainder. Tail-arm suspension is practiced more rapidly on thinner supports, and on more negatively inclined supports than is quadrupedal movement. Howlers do not locomote by tail-arm suspension: movement is almost entirely quadrupedal and is slower than that of spider monkeys. The positional behavior of spider monkeys fits closely recent views of major adaptive changes in hominoid evolution emphasizing brachiation and speed during travel. Howler locomotion and also tissue composition appear related to diet and digestive mechanisms.     

A regression-based 3-D shoulder rhythm

In biomechanical modeling of the shoulder, it is important to know the orientation of each bone in the shoulder girdle when estimating the loads on each musculoskeletal element. However, because of the soft tissue overlying the bones, it is difficult to accurately derive the orientation of the clavicle and scapula using surface markers during dynamic movement. The purpose of this study is to develop two regression models which predict the orientation of the clavicle and the scapula. The first regression model uses humerus orientation and individual factors such as age, gender, and anthropometry data as the predictors. The second regression model includes only the humerus orientation as the predictor. Thirty-eight participants performed 118 static postures covering the volume of the right hand reach. The orientation of the thorax, clavicle, scapula and humerus were measured with a motion tracking system. Regression analysis was performed on the Euler angles decomposed from the orientation of each bone from 26 randomly selected participants. The regression models were then validated with the remaining 12 participants. The results indicate that for the first model, the r² of the predicted orientation of the clavicle and the scapula ranged between 0.31 and 0.65, and the RMSE obtained from the validation dataset ranged from 6.92° to 10.39°. For the second model, the r² ranged between 0.19 and 0.57, and the RMSE obtained from the validation dataset ranged from 6.62° and 11.13°. The derived regression-based shoulder rhythm could be useful in future biomechanical modeling of the shoulder.     

Homo floresiensis and the evolution of the hominin shoulder

The holotype of Homo floresiensis, diminutive hominins with tiny brains living until 12,000 years ago on the island of Flores, is a partial skeleton (LB1) that includes a partial clavicle (LB1/5) and a nearly complete right humerus (LB1/50). Although the humerus appears fairly modern in most regards, it is remarkable in displaying only 110 degrees of humeral torsion, well below modern human average values. Assuming a modern human shoulder configuration, such a low degree of humeral torsion would result in a lateral set to the elbow. Such an elbow joint would function more nearly in a frontal than in a sagittal plane, and this is certainly not what anyone would have predicted for a tool-making Pleistocene hominin. We argue that Homo floresiensis probably did not have a modern human shoulder configuration: the clavicle was relatively short, and we suggest that the scapula was more protracted, resulting in a glenoid fossa that faced anteriorly rather than laterally. A posteriorly directed humeral head was therefore appropriate for maintaining a normally functioning elbow joint. Similar morphology in the Homo erectus Nariokotome boy (KNM-WT 15000) suggests that this shoulder configuration may represent a transitional stage in pectoral girdle evolution in the human lineage.     

Subscapularis function in gibbons and chimpanzees: Implications for interpretation of humeral head torsion in hominoids

Chimpanzees and gibbons, along with other hominoids, share a number of features in the morphology of their shoulders that have generally been associated with use of the upper limb in overhead postural and locomotor activities. These include the position and shape of the scapula, as well as the morphology of the proximal end of the humerus. Results of an electromyographic (EMG) analysis of shoulder muscle activity patterns indicate that these two species of hominoids also share broad similarities in shoulder muscle function during locomotion and voluntary movements. Differences do exist, however, in the activity patterns of subscapularis, a medial rotator of the arm. These differences mainly involve a greater participation by the gibbon subscapularis in free arm movements. This greater participation is characterized by earlier onset of muscle activity, higher amplitude of recruitment, and involvement of more of the total mass of the muscle. These differences in muscle recruitment suggest that the shoulder of gibbons differs from that of chimpanzees in some manner that necessitates the greater contribution of a medial rotator to the production of motion in the upper limb. I suggest that the low degree of humeral head torsion in gibbons, compared to that of other hominoids, gives their elbow a “lateral set” that must be overcome by the action of subscapularis during free arm movements. I propose that this modest degree of humeral head torsion in gibbons reflects a compromise between necessary changes caused by the repositioning of the scapula onto the dorsum of the thorax and the demands for extreme positioning of the elbow during brachiation. In addition, I suggest that the greater amount of torsion in the chimpanzee humerus is an accommodation to quadrupedal habits, and finally, that the high degree of torsion in human humeri is an independently acquired trait related to use of the upper limb as a manipulatory organ.     

Effect of axis alignment on in vivo shoulder kinematics

BACKGROUND. To describe 3D shoulder joint movements, the International Society of Biomechanics (ISB) recommends using segment coordinate systems (SCSs) on the humerus, scapula and thorax, and joint coordinate systems (JCSs) on the shoulder. However, one of the remaining problems is how to define the zero angles when the arm is in an initial reference position. The aim of this paper is to compare various methods of determining the JCSs of the shoulder that make it possible to define the zero angles of the arm in the resting position. METHODS. Able-bodied subjects performed elevation movements in the scapular plane, specifically neutral, internal and external rotations of the humerus. The initial humerus position (at the beginning of the arm movement) and range of motion were analysed for the purpose of clinical interpretation of arm attitude and movement. The following four different JCSs were explored: (1) the standard JCS, defined as recommended by the ISB, (2) a first aligned JCS, where the humerus SCS is initially aligned with the scapula SCS, (3) a second aligned JCS, where the opposite operation is performed and 4) a third aligned JCS, where both the humerus and the scapular SCS are initially aligned with the thorax SCS. FINDINGS. The second aligned JCS was the only method that did not produce any exaggerated range of movement in either anatomical plane. INTERPRETATION. Mathematical JCS alignment allows clearer clinical interpretation of arm attitude and movement.     

Cellular and molecular investigations into the development of the pectoral girdle

The forelimbs of higher vertebrates are composed of two portions: the appendicular region (stylopod, zeugopod and autopod) and the less prominent proximal girdle elements (scapula and clavicle) that brace the limb to the main trunk axis.We show that the formation of the muscles of the proximal limb occurs through two distinct mechanisms. The more superficial girdle muscles (pectoral and latissimus dorsi) develop by the “In–Out” mechanism whereby migration of myogenic cells from the somites into the limb bud is followed by their extension from the proximal limb bud out onto the thorax. In contrast, the deeper girdle muscles (e.g. rhomboideus profundus and serratus anterior) are induced by the forelimb field which promotes myotomal extension directly from the somites. Tbx5 inactivation demonstrated its requirement for the development of all forelimb elements which include the skeletal elements, proximal and distal muscles as well as the sternum in mammals and the cleithrum of fish. Intriguingly, the formation of the diaphragm musculature is also dependent on the Tbx5 programme. These observations challenge our classical views of the boundary between limb and trunk tissues. We suggest that significant structures located in the body should be considered as components of the forelimb.     

Contributions of the individual muscles of the shoulder to glenohumeral joint stability during abduction

The aim of this study was to determine the relative contributions of the deltoid and rotator cuff muscles to glenohumeral joint stability during arm abduction. A three-dimensional model of the upper limb was used to calculate the muscle and joint-contact forces at the shoulder for abduction in the scapular plane. The joints of the shoulder girdle-sternoclavicular joint, acromioclavicular joint, and glenohumeral joint-were each represented as an ideal three degree-of-freedom ball-and-socket joint. The articulation between the scapula and thorax was modeled using two kinematic constraints. Eighteen muscle bundles were used to represent the lines of action of 11 muscle groups spanning the glenohumeral joint. The three-dimensional positions of the clavicle, scapula, and humerus during abduction were measured using intracortical bone pins implanted into one subject. The measured bone positions were inputted into the model, and an optimization problem was solved to calculate the forces developed by the shoulder muscles for abduction in the scapular plane. The model calculations showed that the rotator cuff muscles (specifically, supraspinatus, subscapularis, and infraspinatus) by virtue of their lines of action are perfectly positioned to apply compressive load across the glenohumeral joint, and that these muscles contribute most significantly to shoulder joint stability during abduction. The middle deltoid provides most of the compressive force acting between the humeral head and the glenoid, but this muscle also creates most of the shear, and so its contribution to joint stability is less than that of any of the rotator cuff muscles.     

The range of passive arm circumduction in primates: Do hominoids really have more mobile shoulders?

Hominoids and lorines are assumed to possess greater shoulder mobility than other primates. This assumption is based on morphological characteristics of the shoulder, rather than on empirical data. However, recent studies have shown that the glenohumeral joint of hominoids is not more mobile than that of other primates (Chan LK. 2007. Glenohumeral mobility in primates. Folia Primatol (Basel) 78(1):1–18), and the thoracic shape of hominoids does not necessarily promote shoulder mobility (Chan LK. 2007. Scapular position in primates. Folia Primatol (Basel) 78(1):19–35). Moreover, lorines differ significantly from hominoids in both these features, thus challenging the assumption that both hominoids and lorines have greater shoulder mobility. The present study aims to test this assumption by collecting empirical data on shoulder mobility in 17 primate species. Passive arm circumduction (a combination of glenohumeral and pectoral girdle movement) was performed on sedated subjects (except humans), and the range measured on the video images of the circumduction. The motion differed among primate species mostly in the craniodorsal directions, the directions most relevant to the animal's ability to brachiate and slow climb. Hylobatids possessed the highest craniodorsal mobility among all primate species studied. However, nonhylobatid hominoids did not have greater craniodorsal mobility than arboreal quadrupedal monkeys, and lorines did not have greater craniodorsal mobility than arboreal quadrupedal prosimians. Nonhylobatid hominoids and lorines had similar craniodorsal mobility, but this was due to a longer clavicle, more dorsal scapula, and lower glenohumeral mobility in the former, and a shorter clavicle, less dorsal scapula, and greater glenohumeral mobility in the latter. This study provides evidence for the reexamination of the brachiation, slow climbing, and vertical climbing hypotheses. Am J Phys Anthropol, 2008. © 2008 Wiley‐Liss, Inc.     

A Biomechanical Model of the Scapulothoracic Joint to Accurately Capture Scapular Kinematics during Shoulder Movements

The complexity of shoulder mechanics combined with the movement of skin relative to the scapula makes it difficult to measure shoulder kinematics with sufficient accuracy to distinguish between symptomatic and asymptomatic individuals. Multibody skeletal models can improve motion capture accuracy by reducing the space of possible joint movements, and models are used widely to improve measurement of lower limb kinematics. In this study, we developed a rigid-body model of a scapulothoracic joint to describe the kinematics of the scapula relative to the thorax. This model describes scapular kinematics with four degrees of freedom: 1) elevation and 2) abduction of the scapula on an ellipsoidal thoracic surface, 3) upward rotation of the scapula normal to the thoracic surface, and 4) internal rotation of the scapula to lift the medial border of the scapula off the surface of the thorax. The surface dimensions and joint axes can be customized to match an individual’s anthropometry. We compared the model to “gold standard” bone-pin kinematics collected during three shoulder tasks and found modeled scapular kinematics to be accurate to within 2mm root-mean-squared error for individual bone-pin markers across all markers and movement tasks. As an additional test, we added random and systematic noise to the bone-pin marker data and found that the model reduced kinematic variability due to noise by 65% compared to Euler angles computed without the model. Our scapulothoracic joint model can be used for inverse and forward dynamics analyses and to compute joint reaction loads. The computational performance of the scapulothoracic joint model is well suited for real-time applications; it is freely available for use with OpenSim 3.2, and is customizable and usable with other OpenSim models.