Manuela Schmidt

Hind limb proportions and kinematics: are small primates different from other small mammals?

SUMMARY The crouched limb posture of small mammals enables them to react to unexpected irregularities in the support. Small arboreal primates would benefit from these kinematics in their arboreal habitat but it has been demonstrated that primates display certain differences in forelimb kinematics to other mammals. The objective of this paper is to find out whether these changes in forelimb kinematics are related to changes in body size and limb proportions. As primates descended from small ancestors, a comparison between living small primates and other small mammals makes it possible to determine the polarity of character transformations for kinematic and morphometric features proposed to be unique to primates. Walking kinematics of mouse lemurs, brown lemurs, cotton-top tamarins and squirrel monkeys was investigated using cineradiography. Morphometry was conducted on a sample of 110 mammals comprising of primates, marsupials, rodents and carnivores. It has been shown that forelimb kinematics change with increasing body size in such a way that limb protraction increases but retraction decreases. Total forelimb excursion, therefore, is almost independent of body size. Kinematic changes are linked to changes in forelimb proportions towards greater asymmetry between scapula and radius. Due to the spatial restriction inherent in the diagonal footfall sequence of primates, forelimb excursion is influenced by the excursion of the elongated hind limb. Hindlimb geometry, however, is highly conserved, as has been previously shown. The initial changes in forelimb kinematics might, therefore, be explained as solutions to a constraint rather than as adaptations to the particular demands of arboreal locomotion.

Morphological Integration in Mammalian Limb Proportions: Dissociation between Function and Development

During mammalian evolution, fore- and hindlimbs underwent a fundamental reorganization in the transformation from the sprawled to the parasagittal condition. This caused a dissociation between serial and functional homologues. The mobilized scapula functions as the new proximal forelimb element and is functionally analogous to the femur of the hindlimb. Tarsus and metatarsus built a new functional hindlimb element that is functionally analogous to the forearm of the forelimb. Morphological covariation between serially homologous fore- and hindlimb elements can conflict with biomechanical demands when certain intralimb proportions are required for the postural stability of motion. The limb proportions of 189 mammalian species were examined to test whether intralimb proportions are governed by a general principle that corresponds to biomechanical predictions. Morphological covariation between functionally analogous and serially homologous fore- and hindlimb elements was tested by a correlation analysis. A clear relationship exists between the proportions of the first and the third elements of each limb, while the middle element is less involved in alterations of intralimb proportions. Hindlimb proportions are largely uniform across mammals and correspond to biomechanical predictions regarding postural stability. The greater variability in forelimb proportion is likely be the expression of various adaptations but might results also from constraints due to the shared developmental programs with the hindlimb.

Cineradiographic study of forelimb movements during quadrupedal walking in the brown lemur (Eulemur fulvus, primates: Lemuridae)

Movements of forelimb joints and segments during walking in the brown lemur (Eulemur fulvus) were analyzed using cineradiography (150 frames/sec). Metric gait parameters, forelimb kinematics, and intralimb coordination are described. Calculation of contribution of segment displacements to stance propulsion shows that scapular retroversion in a fulcrum near the vertebral border causes more than 60% of propulsion. The contribution by the shoulder joint is 30%, elbow joint 5%, and wrist joint 1%. Correlation analysis was applied to reveal the interdependency between metric and kinematic parameters. Only the effective angular movement of the elbow joint during stance is speed-dependent. Movements of all other forelimb joints and segments are independent of speed and influence, mainly, linear gait parameters (stride length, stance length). Perhaps the most important result is the hitherto unknown and unexpected degree of scapular mobility. Scapular movements consist of ante-/retroversion, adduction/abduction, and scapular rotation about the longitudinal axis. Inside rotation of the scapula (60 degrees -70 degrees ), together with flexion in the shoulder joint, mediates abduction of the humerus, which is not achieved in the shoulder joint, and is therefore strikingly different from humeral abduction in man. Movements of the shoulder joint are restricted to flexion and extension. At touch down, the shoulder joint of the brown lemur is more extended compared to that of other small mammals. The relatively long humerus and forearm, characteristic for primates, are thus effectively converted into stride length. Observed asymmetries in metric and kinematic behavior of the left and right forelimb are caused by an unequal lateral bending of the spinal column.

Gait abnormalities differentially indicate pain or structural joint damage in monoarticular antigen-induced arthritis

ABSTRACT Gait abnormalities have been suggested to provide an objective measure for joint pain in animal models. Here, we aimed to assess whether parameters of gait analysis correlate with measures of pain‐related behavior in experimental monoarthritis. For this purpose, antigen‐induced arthritis was induced in the left knee joints of 68 female Lewis rats, of which 30 were treated with tumor necrosis factor‐alpha(TNF)‐neutralizing compounds. During the course of arthritis, paw print analysis parameters and measures for mechanical and thermal hyperalgesia were obtained. Knee joints harvested on either day 3 or day 21 were scored histologically for signs of inflammation and cartilage and bone destructions. Data were compared to those obtained from 33 immunized control rats and correlated for days 3 and 21. Arthritic rats showed distinct asymmetric gait abnormalities. In the acute stage of antigen‐induced arthritis, but not in the chronic phase, there was a significant correlation between the gait parameter ‘left–right distance’ and measures of primary and secondary hyperalgesia. Both in the acute and chronic phases, however, the gait parameter ‘angle between paws’ indicating outward rotation of paws mainly correlated with joint destruction as assessed using histology. Etanercept treatment exhibited pronounced anti‐nociceptive and pro‐locomotional effects, but the described correlations remained. In conclusion, some parameters of gait analysis may represent a good measure for arthritis pain, mainly in acute inflammation, while others are increasingly influenced by mechanical joint deformation as indicated by cartilage and bone destructions. Thus, gait abnormalities may not unequivocally be suitable for objective pain assessment in all stages of experimental arthritis.

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.

Scapula Movements and Their Contribution to Three-Dimensional Forelimb Excursions in Quadrupedal Primates

Primates are endowed with a great repertoire of locomotor and nonlocomotor abilities, for which they rely on their powerful prehensile hind limbs and their skilled and mobile forelimbs. The overall mobility of the forelimb depends to a considerable degree on structure and function of the shoulder region but only scant information about the detailed motion of the primate shoulder is available so far. Therefore, we investigated shoulder movements during locomotion in four arboreal quadruped primates using high-speed cineradiography. Together with previous radiographic studies, four different patterns of combined scapular and humeral excursions can be identified that differ in the degree of dorsolateral scapular motion and mediolateral glenohumeral mobility. It becomes obvious that the overall shoulder mobility in primates is affected by scapular mobility on one hand and glenohumeral mobility on the other hand, but the two components of shoulder mobility likely evolved, to some extent, independently. Finding morphological correlates to the observed motion patterns, however, is difficult because morphometric features likely determine the maximum range of shoulder motion, which is not necessarily the motion range that occurs during locomotor activities of the forelimb. For a better understanding of the great variability in shoulder morphology, future studies both in the field and the laboratory should focus on the overall repertoire of shoulder function in primates. Only the combined effort of both research strategies will enhance our understanding of the evolution of this morphofunctional complex in primates.

Videoradiographic analysis of the range of motion in unilateral experimental knee joint arthritis in rats

IntroductionThe translational and predictive value of animal models highly depends on the validity of respective readout parameters. In arthritis research, there has been a shift from sole threshold testing for pain-related behavior, as well as from swelling and histology assessment for inflammation, toward an analysis of joint function as indicated, for instance, by an increasing number of studies on gait abnormalities. Clinically, the range of motion (ROM) of the affected joint plays a major role in diagnosis and the assessment of treatment benefits. This parameter, however, is only insufficiently detected by currently used analytic systems in animals.MethodsHere we used high-resolution videoradiographic analysis to assess ROM in experimental knee joint arthritis in rats. This parameter is described during the 21-day course of antigen-induced arthritis in rats. Furthermore, the therapeutic effects of antinociceptive (morphine) and anti-inflammatory (dexamethasone) treatment on ROM are documented. To obtain additional information on the implications of ROM in animal models, correlations were performed to measure pain-related behavior and inflammation.ResultsThe study animals showed a significant reduction in ROM of the inflamed knee joint in the acute phase of arthritis. This was accompanied by an increase in knee joint movement on the contralateral side, indicating a compensational mechanism. Both morphine and dexamethasone treatment increased and thus normalized ROM. Changes in ROM were further stage-dependently correlated with weight bearing and joint swelling, that is, with both pain-related behavior and signs of inflammation.ConclusionsThe dynamic ROM observed in freely moving rats in our model of knee joint arthritis might serve as a parameter for global disease activity and might thus represent a promising readout parameter for preclinical assessment regarding the overall efficacy not only of antiarthritic but also of antinociceptive compounds.

The role of vibrissal sensing in forelimb position control during travelling locomotion in the rat (Rattus norvegicus, Rodentia).

In the stem lineage of therians, a comprehensive reorganization of limb and body mechanics took place to provide dynamic stability for rapid locomotion in a highly structured environment. At what was probably the same time, mammals developed an active sense of touch in the form of movable mystacial vibrissae. The rhythmic movements of the limbs and vibrissae are controlled by central pattern-generating networks which might interact with each other in sensorimotor control. To test this possible interaction, we studied covariation between the two by investigating speed-dependent adjustments in temporal and spatial parameters of forelimb and vibrissal kinematics in the rat. Furthermore, the possible role of carpal vibrissae in connecting the two oscillating systems was explored. We compared locomotion on continuous and discontinuous substrates in the presence and absence of the mystacial or/and carpal vibrissae across a speed range of 0.2-0.5m/s and found that a close coupling of the kinematics of the two oscillating systems appears to be precluded by their differential dependence on the animals speed. Speed-related changes in forelimb kinematics mainly occur in temporal parameters, whereas vibrissae change their spatial excursion. However, whisking frequency is always high enough that at least one whisk cycle falls into the swing phase of the limb, which is the maximum critical period for sensing the substrate on which the forepaw will be placed. The influence of tactile cues on forelimb positional control is more subtle than expected. Tactile cues appear to affect the degree of parameter variation but not average parameters or the failure rate of limbs during walking on a perforated treadmill. The carpal vibrissae appear to play a role in sensing the animals speed by measuring the duration of the stance phase. The absence of this cue significantly reduces speed-related variation in stride frequency and vibrissal protraction.

Adjustments of Limb Mechanics in Cotton-top Tamarins to Moderate and Steep Support Orientations: Significance for the Understanding of Early Primate Evolution

Early primate evolution is connected to the efficient exploitation of the terminal branch habitat. Mammals that forage in this habitat constantly encounter flexible thin branches that bend under the weight of the animals and thus form steeply inclined and declined supports. This study was aimed to gain insight into how cotton-top tamarins – a previously proposed modern analogue for a hypothetical stage in early primate evolution with prehensile autopodia – meet the specific functional demands when navigating thin, branch-like supports of different orientation. X-ray motion analysis was combined with synchronous single limb substrate reaction force measurements to discern limb mechanical adjustments. Previously reported gait parameter adjustments were confirmed for moderate support orientations, but on the steepest inclines and declines kinematic discontinuities were observed. These are interpreted to emphasize the functional roles of the forelimbs (net-braking role) and hind limbs (net-propulsive role) already established for level and moderately inclined supports. Tensile forces were exerted by the forelimbs on the steepest inclines and by the hind limbs on the steepest declines (head-first descents). Even though non-specialized small mammals have also been shown to successfully negotiate similar supports, prehensility offers advantages for foraging on thin, steeply inclined and declined terminal branches. Thus, the evolution of prehensile autopodia in small early primates likely has enhanced the exploitation of the terminal branch habitat.

A biologically based neural system coordinates the joints and legs of a tetrapod.

A biologically inspired neural control system has been developed that coordinates a tetrapod trotting gait in the sagittal plane. The developed neuromechanical system is used to explore properties of connections in inter-leg and intra-leg coordination. The neural controller is built with biologically based neurons and synapses, and connections are based on data from literature where available. It is applied to a planar biomechanical model of a rat with 14 joints, each actuated by a pair of antagonistic Hill muscle models. The controller generates tension in the muscles through activation of simulated motoneurons. The hind leg and inter-leg control networks are based on pathways discovered in cat research tuned to the kinematic motions of a rat. The foreleg network was developed by extrapolating analogous pathways from the hind legs. The formulated intra-leg and inter-leg networks properly coordinate the joints and produce motions similar to those of a walking rat. Changing the strength of a single inter-leg connection is sufficient to account for differences in phase timing in different trotting rats.