Inter-joint coupling effects on muscle contributions to endpoint force and acceleration in a musculoskeletal model of the cat hindlimb

The biomechanical principles underlying the organization of muscle activation patterns during standing balance are poorly understood. The goal of this study was to understand the influence of biomechanical inter-joint coupling on endpoint forces and accelerations induced by the activation of individual muscles during postural tasks. We calculated induced endpoint forces and accelerations of 31 muscles in a 7 degree-of-freedom, three-dimensional model of the cat hindlimb. To test the effects of inter-joint coupling, we systematically immobilized the joints (excluded kinematic degrees of freedom) and evaluated how the endpoint force and acceleration directions changed for each muscle in 7 different conditions. We hypothesized that altered inter-joint coupling due to joint immobilization of remote joints would substantially change the induced directions of endpoint force and acceleration of individual muscles. Our results show that for most muscles crossing the knee or the hip, joint immobilization altered the endpoint force or acceleration direction by more than 90° in the dorsal and sagittal planes. Induced endpoint forces were typically consistent with behaviorally observed forces only when the ankle was immobilized. We then activated a proximal muscle simultaneous with an ankle torque of varying magnitude, which demonstrated that the resulting endpoint force or acceleration direction is modulated by the magnitude of the ankle torque. We argue that this simple manipulation can lend insight into the functional effects of co-activating muscles. We conclude that inter-joint coupling may be an essential biomechanical principle underlying the coordination of proximal and distal muscles to produce functional endpoint actions during motor tasks.     

Barrels XII - Proceedings

Spinalized frogs were microstimulated in the intermediate grey layers of the lumbar spinal cord; the forces evoked in the hindlimb were measured at several limb positions. The data were expressed as force fields. After the collection of many force fields, the dorsal roots were cut with the stimulating electrode in place, and the position-dependent stimulation-evoked forces were again measured repeatedly. We found that the position-dependent pattern of evoked forces—the force fields—did not change after the dorsal roots were cut. In other words, the postcut evoked forces pointed in the same direction as the precut evoked forces. This result was predicted and confirmed by the muscle activations (EMGs): Before and after the dorsal roots were cut, the same muscles were activated in the same proportions. In all limb positions, the rank ordering of the muscle activations remained fixed. The stimulation needed to evoke forces was increased by deafferentation, and there were subtle changes in the force magnitudes that were consistent with a linearization of the muscle stiffness by the afferents. We conclude that the microstimulation activated specific muscle synergies that resulted in limb forces pointing toward a particular posture. The patterns of evoked forces were predominantly attributable to feedforward activation of these muscle synergies.     

Functional muscle synergies constrain force production during postural tasks

We recently demonstrated that a set of five functional muscle synergies were sufficient to characterize both hindlimb muscle activity and active forces during automatic postural responses in cats standing at multiple postural configurations. This characterization depended critically upon the assumption that the endpoint force vector (synergy force vector) produced by the activation of each muscle synergy rotated with the limb axis as the hindlimb posture varied in the sagittal plane. Here, we used a detailed, 3D static model of the hindlimb to confirm that this assumption is biomechanically plausible: as we varied the model posture, simulated synergy force vectors rotated monotonically with the limb axis in the parasagittal plane (r2=0.94+/-0.08). We then tested whether a neural strategy of using these five functional muscle synergies provides the same force-generating capability as controlling each of the 31 muscles individually. We compared feasible force sets (FFSs) from the model with and without a muscle synergy organization. FFS volumes were significantly reduced with the muscle synergy organization (F=1556.01, p<0.01), and as posture varied, the synergy-limited FFSs changed in shape, consistent with changes in experimentally measured active forces. In contrast, nominal FFS shapes were invariant with posture, reinforcing prior findings that postural forces cannot be predicted by hindlimb biomechanics alone. We propose that an internal model for postural force generation may coordinate functional muscle synergies that are invariant in intrinsic limb coordinates, and this reduced-dimension control scheme reduces the set of forces available for postural control.     

Effects of sustained stimulation on the excitability of motoneurons innervating paralyzed and control muscles.

The excitability of thenar motoneurons (reflected by F-wave persistence and amplitude) and thenar muscle force were measured during a stimulation protocol (90 s of 18-Hz supramaximal electrical stimulation of the median nerve) designed to induce muscle fatigue (force decline). Data from muscles (n = 15) paralyzed by chronic cervical spinal cord injury were compared with those obtained from control muscles (n = 6). The persistence of F waves in both paralyzed and control muscles increased from approximately 60 to approximately 76% during the first 10 s of the fatigue protocol. Persistence then declined progressively to approximately 33% at 90 s. These changes in F-wave persistence suggest that similar reductions occur in the excitability of the motoneurons to paralyzed and control motor units after sustained antidromic activation. Despite this, significantly larger force declines occurred in the paralyzed muscles of spinal cord-injured subjects (approximately 60%) than in the muscles of control subjects (approximately 15%). These data suggest that the decreases in motoneuron excitability for both the spinal cord-injured and control subjects are a result of activity-dependent changes in motoneuron properties that are independent of fatigue-related processes in the muscles.     

Reduction of neuromuscular redundancy for postural force generation using an intrinsic stability criterion

Postural control requires the coordination of multiple muscles to achieve both endpoint force production and postural stability. Multiple muscle activation patterns can produce the required force for standing, but the mechanical stability associated with any given pattern may vary, and has implications for the degree of delayed neural feedback necessary for postural stability. We hypothesized that muscular redundancy is reduced when muscle activation patterns are chosen with respect to intrinsic musculoskeletal stability as well as endpoint force production. We used a three-dimensional musculoskeletal model of the cat hindlimb with 31 muscles to determine the possible contributions of intrinsic muscle properties to limb stability during isometric force generation. Using dynamic stability analysis we demonstrate that within the large set of activation patterns that satisfy the force requirement for posture, only a reduced subset produce a mechanically stable limb configuration. Greater stability in the frontal-plane suggests that neural control mechanisms are more highly active for sagittal-plane and for ankle joint control. Even when the limb was unstable, the time-constants of instability were sufficiently great to allow long-latency neural feedback mechanisms to intervene, which may be preferential for movements requiring maneuverability versus stability. Local joint stiffness of muscles was determined by the stabilizing or destabilizing effects of moment-arm versus joint angle relationships. By preferentially activating muscles with high local stiffness, muscle activation patterns with feedforward stabilizing properties could be selected. Such a strategy may increase intrinsic postural stability without co-contraction, and may be useful criteria in the force-sharing problem.     

A Proprioception Based Regulation Model to Estimate the Trunk Muscle Forces

Evaluation of loads acting on the spine requires the knowledge of the muscular forces acting on it, but muscles redundancy necessitates developing a muscle forces attribution strategy. Optimisation, EMG, or hybrid models allow evaluating muscle force patterns, yielding a unique muscular arrangement or/and requiring EMG data collection. This paper presents a regulation model of the trunk muscles based on a proprioception hypothesis, which searches to avoid the spinal joint overloading. The model is also compared to other existing models for evaluation. Compared to an optimisation model, the proposed alternative muscle pattern yielded a significant spine postero-anterior shear decrease. Compared to a model based on combination of optimisation criteria, present model better fits muscle activation observed using EMG (38% improvement). Such results suggest that the proposed model, based on regulation of all spinal components, may be more relevant from a physiologic point of view.     

A proprioception based regulation model to estimate the trunk muscle forces

Evaluation of loads acting on the spine requires the knowledge of the muscular forces acting on it, but muscles redundancy necessitates developing a muscle forces attribution strategy. Optimisation, EMG, or hybrid models allow evaluating muscle force patterns, yielding a unique muscular arrangement or/and requiring EMG data collection. This paper presents a regulation model of the trunk muscles based on a proprioception hypothesis, which searches to avoid the spinal joint overloading. The model is also compared to other existing models for evaluation. Compared to an optimisation model, the proposed alternative muscle pattern yielded a significant spine postero-anterior shear decrease. Compared to a model based on combination of optimisation criteria, present model better fits muscle activation observed using EMG (38% improvement). Such results suggest that the proposed model, based on regulation of all spinal components, may be more relevant from a physiologic point of view.     

Maximum isometric arm forces in the horizontal plane

In this paper, we measured the maximum isometric force at the hand in eight directions in the horizontal plane and at five positions in the workplace. These endpoint forces were the result of shoulder horizontal adduction/abduction and elbow flexion/extension torques. We found that the normalized maximum forces of all the six subjects deviated less than 15%, despite intra-subject differences in muscle strength of more than a factor of two. The maximum forces were found to systematically depend on the force direction and on the hand position in the workspace. The largest forces were found in a direction approximately along the line connecting shoulder joint and hand, and the smallest forces perpendicular to that line, thereby forming an elliptically shaped pattern. The elongation of the pattern was the largest for those hand positions having the more extended elbow joint. By using a lumped six-muscle model, with two mono-articular muscle pairs and one bi-articular pair, we were able to predict the observed force patterns. Here, we assumed that one of the muscles generates its maximum force and the others adjust their output to point the endpoint force in the required direction. We used a principal component analysis of the surface EMGs of simultaneously measured representatives of four of the six muscles. With the same model, we were then able to determine the principal directions of all the six muscle groups.     

Three-dimensional model of the feline hindlimb

This article describes a three-dimensional musculoskeletal model of the feline hindlimb based on digitized musculoskeletal anatomy. The model consists of seven degrees of freedom: three at the hip and two each at the knee and ankle. Lines of action and via points for 32 major muscles of the limb are described. Interspecimen variability of muscle paths was surprisingly low; most via points displayed a scatter of only a few millimeters. Joint axes identified by mechanical techniques as noncoincident and nonorthogonal were further honed to yield moment arms consistent with previous reports. Interspecimen variability in joint axes was greater than that of muscle paths and highlights the importance of joint axes in kinematic models. The contribution of specific muscles to the direction of endpoint force generation is discussed.     

Modifications of motoneuron development following transplantation of thoracic spinal cord to the lumbar region in the chick embryo: Evidence for target-derived signals that regulate differentiation

In order to examine the role of target cells in the development of spinal motoneurons, the neural tube from thoracic segments was transplanted to the lumbar region on embryonic day (E) 2, and allowed to innervate hindlimb muscles in the chick embryo. When examined at later stages of development, the proportion of white and gray matter in the thoracic transplant was altered to resemble normal lumbar cord. Many thoracic motoneurons were able to survive up to posthatching stages following transplantation. The branching and arborization of dendrites of thoracic motoneurons innervating hindlimb muscles, as well as motoneuron (soma) size, were also increased to an extent approximating that seen in normal lumbar motoneurons. In support of previous studies using a similar transplant model, we have also found that the peripheral (intramuscular) branching pattern of thoracic motoneuron axons innervating hindlimb muscles was similar to that of normal lumbar motoneurons. Axon size and the degree of myelination of transplanted thoracic motoneuron axons were also increased so that these parameters more closely resembled axons of normal lumbar than normal thoracic spinal motoneurons. Virtually all of the changes in motoneuron properties noted above were observed irrespective of whether or not the transplanted spinal cord had developed in anatomical continuity with the host rostral cord. Accordingly, it is unlikely that the changes in the development of transplanted thoracic motoneurons reported here are induced either entirely, or in part, by signals derived from the host central nervous system. Rather, these changes appear to be mediated by interactions between the transplanted motoneurons and the hindlimb. We favor the notion that retrograde trophic signals derived from the hindlimb act to modulate the development of innervating motoneurons. Whether this signal involves a diffusible trophic agent released from target cells, or acts by some other mechanism is presently unknown. © 1992 John Wiley & Sons, Inc.     

Brachially innervated ectopic hindlimbs in the chick embryo. I. Limb motility and motor system anatomy during the development of embryonic behavior

The functional status of brachially innervated hindlimbs, produced by transplanting hindlimb buds of chick embryos in place of forelimb buds, was quantified by analyzing the number and temporal distribution of spontaneous limb movements. Brachially innervated hindlimbs exhibited normal motility until E10 but thereafter became significantly less active than normal limbs and the limb movements were more randomly distributed. Contrary to the findings with axolotls and frogs, functional interaction between brachial motoneurons and hindlimb muscles cannot be sustained in the chick embryo. Dysfunction is first detectable at E10 and progresses to near total immobility by E20 and is associated with joint ankylosis and muscular atrophy. Although brachially innervated hindlimbs were virtually immobile by the time of hatching (E21), they produced strong movements in response to electrical stimulation of their spinal nerves, suggesting a central rather than peripheral defect in the motor system. The extent of motoneuron death in the brachial spinal cord was not significantly altered by the substitution of the forelimb bud with the hindlimb bud, but the timing of motoneuron loss was appropriate for the lumbar rather than brachial spinal cord, indicating that the rate of motoneuron death was dictated by the limb. Measurements of nuclear area indicated that motoneuron size was normal during the motoneuron death period (E6-E10) but the nuclei of motoneurons innervating grafted hindlimbs subsequently became significantly larger than those of normal brachial motoneurons. Although the muscle mass of the grafted hindlimb at E18 was significantly less than that of the normal hindlimb (and similar to that of a normal forelimb), electronmicroscopic examination of the grafted hindlimbs and brachial spinal cords of E20 embryos revealed normal myofiber and neuromuscular junction ultrastructure and a small increase in the number of axosomatic synapses on cross-sections of motoneurons innervating grafted hindlimbs compared to motoneurons innervating normal forelimbs. The anatomical data indicate that, rather than being associated with degenerative changes, the motor system of the brachial hindlimb of late-stage embryos is intact, but inactive. © 1993 John Wiley & Sons, Inc.     

Modifications of motoneuron development following transplantation of thoracic spinal cord to the lumbar region in the chick embryo: evidence for target-derived signals that regulate differentiation.

In order to examine the role of target cells in the development of spinal motoneurons, the neural tube from thoracic segments was transplanted to the lumbar region on embryonic day (E) 2, and allowed to innervate hindlimb muscles in the chick embryo. When examined at later stages of development, the proportion of white and gray matter in the thoracic transplant was altered to resemble normal lumbar cord. Many thoracic motoneurons were able to survive up to posthatching stages following transplantation. The branching and arborization of dendrites of thoracic motoneurons innervating hindlimb muscles, as well as motoneuron (soma) size, were also increased to an extent approximating that seen in normal lumbar motoneurons. In support of previous studies using a similar transplant model, we have also found that the peripheral (intramuscular) branching pattern of thoracic motoneuron axons innervating hindlimb muscles was similar to that of normal lumbar motoneurons. Axon size and the degree of myelination of transplanted thoracic motoneuron axons were also increased so that these parameters more closely resembled axons of normal lumbar than normal thoracic spinal motoneurons. Virtually all of the changes in motoneuron properties noted above were observed irrespective of whether or not the transplanted spinal cord had developed in anatomical continuity with the host rostral cord. Accordingly, it is unlikely that the changes in the development of transplanted thoracic motoneurons reported here are induced either entirely, or in part, by signals derived from the host central nervous system. Rather, these changes appear to be mediated by interactions between the transplanted motoneurons and the hindlimb. We favor the notion that retrograde trophic signals derived from the hindlimb act to modulate the development of innervating motoneurons. Whether this signal involves a diffusible trophic agent released from target cells, or acts by some other mechanism is presently unknown.     

Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: anatomical aspects

Thoracic spinal cord transplanted to the lumbar region at the time of neural tube closure in the chick embryo survives and initially differentiates normally similar to in situ thoracic cord. Normal numbers of motoneurons are produced that innervate the host hindlimb musculature. In control thoracic cord approximately 70% of the motoneurons are lost by normal cell death between embryonic day (E) 6 and E11-E12. By contrast, the transplanted thoracic cord loses only about 30% of the motoneurons during this period. Transplantation of one hindlimb to the thoracic region also reduces the normal loss of in situ thoracic motoneurons. We conclude that some factor(s) associated with the increased target size provided by the hindlimbs promotes the survival of thoracic motoneurons. In contrast, by E16-E18 motoneuron numbers in the thoracic transplants decrease to below control levels. Dorsal root ganglion cells in the transplant were also initially increased (on E8) but later decreased to below control values. Hindlimb muscles innervated by thoracic motoneurons in the transplant also differentiated normally up to E10 to E12. Myotube size and numbers, muscle size and myotube types (fast versus slow) all developed normally in several thoracically-innervated hindlimb muscles. However, beginning on E14 myotube numbers and muscle size were markedly decreased resulting in muscle atrophy. Injections of horseradish peroxidase (HRP) into the thoracic transplants labelled neurons in the host spinal cord and brainstem rostral to the transplant thereby indicating an anatomical continuity between host and transplant neural tube. Injections of HRP into specific thoracically innervated hindlimb muscles on E8 labelled distinct pools of motoneurons in the transplants.(ABSTRACT TRUNCATED AT 250 WORDS)     

Size of motoneuron pool may be related to number of myotubes in developing muscle

The number of myotube clusters in various chicken hindlimb muscles has been counted at the time of motoneuron cell death and found to be quantitatively similar to the number of neurons which innervate these muscles in the adult. It is proposed that the capacity of a muscle to support motoneurons is related to the number of “myotube clusters” in that muscle at the time of motoneuron cell death.     

Biomechanics of the rabbit knee and ankle: muscle, ligament, and joint contact force predictions

Mathematical models of small animals that predict in vivo forces acting on the lower extremities are critical for studies of musculoskeletal biomechanics and diseases. Rabbits are advantageous in this regard because they remodel their cortical bone similar to humans. Here, we enhance a recent mathematical model of the rabbit knee joint to include the loading behavior of individual muscles, ligaments, and joint contact at the knee and ankle during the stance phase of hopping. Geometric data from the hindlimbs of three adult New Zealand white rabbits, combined with previously reported intersegmental forces and moments, were used as inputs to the model. Muscle, ligament, and joint contact forces were computed using optimization techniques assuming that muscle endurance is maximized and ligament strain energy resists tibial shear force along an inclined plateau. Peak forces developed by the quadriceps and gastrocnemius muscle groups and by compressive knee contact were within the range of theoretical and in vivo predictions. Although a minimal force was carried by the anterior cruciate and medial collateral ligaments, force patterns in the posterior cruciate ligament were consistent with in vivo tibial displacement patterns during hopping in rabbits. Overall, our predictions compare favorably with theoretical estimates and in vivo measurements in rabbits, and enhance previous models by providing individual muscle, ligament, and joint contact information to predict in vivo forces acting on the lower extremities in rabbits.     

Effects of hindlimb suspension on soleus muscle fibers and their spinal motoneurons in Wistar Hannover rats

Cross-sectional areas and succinate dehydrogenase (SDH) activities of soleus muscle fibers and their spinal motoneurons in male Wistar Hannover rats were determined after 16 days of hindlimb suspension. A decreased percentage of type I fibers and an increased percentage of type I+II fibers were observed after hindlimb suspension. Cross-sectional areas of all types of fibers were smaller in the hindlimb suspended than control rats. SDH activities of all types of fibers did not change after hindlimb suspension. Numbers, cross-sectional areas, or SDH activities of spinal motoneurons did not change after hindlimb suspension. It is suggested that spinal motoneurons innervating the rat soleus muscle are not affected by decreased neuromuscular activity on Earth and that gravity itself is important for maintaining of spinal motoneuron metabolic properties.     

Control of ground reaction forces by hindlimb muscles during cat locomotion

It has been proposed that biarticular muscles are primarily responsible for the control of the direction of external forces, as their activation is closely related and highly sensitive to the direction of external forces. This functional role for biarticular muscles has been supported qualitatively by experimental evidence, but has never been tested quantitatively for lack of a mathematical/mechanical formulation of this theory and the difficulty of measuring individual muscle forces during voluntary movements. The purposes of this study were: (1) to define rules for muscular coordination based on the control of external forces; (2) to develop a model of the cat hindlimb that allows for the calculation of the magnitude and direction of the ground reaction forces (GRFs) produced by individual hindlimb muscles; and (3) to test if the coordination of mono- and biarticular cat hindlimb muscles is related to the control of the resultant GRF. We measured the GRF, hindlimb kinematics, selected muscle forces and activations during cat locomotion. Then, the measured muscle forces were used as input to the hindlimb model to compute the muscle-induced GRF. We assume that if activation (and possibly force) increased as the muscle-induced component of GRF approximated the resultant GRF, then that muscle was used by the central nervous system (CNS) to help control the direction of the external GRF. During cat walking, medial gastrocnemius (MG) and plantaris (PL) forces increased with increasing proximity to the GRF, while soleus (SOL) forces and vastus lateralis (VL) activations did not. SOL and VL activation were most strongly related to the vertical and parallel (braking/accelerating) component of the GRF, respectively. We concluded from these results that MG and PL are primarily responsible for the control of the direction of the GRF, while SOL primarily functions as an anti-gravity muscle, and VL as an acceleration/deceleration muscle.     

Differentiation of fiber types in aneural musculature of the prenatal rat hindlimb

The presynaptic neurotoxin, beta-bungarotoxin, was injected into rat fetuses in utero to destroy the innervation of their hindlimb muscles. These injections were made prior to the invasion of motor axons into the muscles and, in some cases, prior to the cleavage of individual muscles. Examination of the lateral motor column of the spinal cord showed a dramatic reduction (greater than 95%) in the number of motoneuron cell bodies. Staining of sections of the hindlimb with silver and with antibodies to neurofilament proteins and to a synaptic vesicle protein indicated that the muscles were aneural. Anti-myosin antibodies applied to sections of the hindlimb revealed that these aneural muscles by the 20th day of gestation had the same types of fibers as were present in normal muscles of the same age. Moreover, fiber types in most muscles showed their characteristic intramuscular distributions. These findings suggest that fiber types can differentiate in the absence of the nervous system. However, some fibers achieved their ultimate fiber type fate without passing through the normal sequence of myosin expressions. Moreover, some slow fibers lost their slow expression, suggesting that the maintenance of the slow differentiation may require innervation. Muscle growth was dramatically affected by the absence of motoneurons; some muscles were decreased in size and others disappeared completely. In muscles which had not degenerated by the time secondary myogenesis normally begins, secondary muscle fibers were generated indicating that the genesis of these fibers is not strictly nerve dependent. Because fiber types differentiate independently of the nervous system, this study suggests that motoneurons selectively innervate fiber types during normal development.     

Stimulation of calcineurin Aalpha activity attenuates muscle pathophysiology in mdx dystrophic mice

Calcineurin activation ameliorates the dystrophic pathology of hindlimb muscles in mdx mice and decreases their susceptibility to contraction damage. In mdx mice, the diaphragm is more severely affected than hindlimb muscles and more representative of Duchenne muscular dystrophy. The constitutively active calcineurin Aalpha transgene (CnAalpha) was overexpressed in skeletal muscles of mdx (mdx CnAalpha*) mice to test whether muscle morphology and function would be improved. Contractile function of diaphragm strips and extensor digitorum longus and soleus muscles from adult mdx CnAalpha* and mdx mice was examined in vitro. Hindlimb muscles from mdx CnAalpha* mice had a prolonged twitch time course and were more resistant to fatigue. Because of a slower phenotype and a decrease in fiber cross-sectional area, normalized force was lower in fast- and slow-twitch muscles of mdx CnAalpha* than mdx mice. In the diaphragm, despite a slower phenotype and a approximately 35% reduction in fiber size, normalized force was preserved. This was likely mediated by the reduction in the area of the diaphragm undergoing degeneration (i.e., mononuclear cell and connective and adipose tissue infiltration). The proportion of centrally nucleated fibers was reduced in mdx CnAalpha* compared with mdx mice, indicative of improved myofiber viability. In hindlimb muscles of mdx mice, calcineurin activation increased expression of markers of regeneration, particularly developmental myosin heavy chain isoform and myocyte enhancer factor 2A. Thus activation of the calcineurin signal transduction pathway has potential to ameliorate the mdx pathophysiology, especially in the diaphragm, through its effects on muscle degeneration and regeneration and endurance capacity.     

Correlation of muscle function and bone strain in the hindlimb of the river cooter turtle (Pseudemys concinna)

During terrestrial locomotion, limb muscles must generate mechanical work and stabilize joints against the ground reaction force. These demands can require high force production that imposes substantial loads on limb bones. To better understand how muscle contractile function influences patterns of bone loading in terrestrial locomotion, and refine force platform equilibrium models used to estimate limb bone safety factors, we correlated in vivo recordings of femoral strain with muscle activation and strain in a major propulsive hindlimb muscle, flexor tibialis internus (FTI), of a species with a published model of hindlimb force production (river cooter turtles, Pseudemys concinna). Electromyography (EMG) recordings indicate FTI activity prior to footfall that continues through approximately 50% of the stance phase. Large EMG bursts occur just after footfall when the muscle has reached its maximum length and is beginning to actively shorten, concurrent with increasing compressive strain on the anterior femur. The FTI muscle shortens through 35% of stance, with mean fascicle shortening strains reaching 14.0 ± 5.4% resting length (L₀). At the time of peak compressive strains on the femur, the muscle fascicles remain active, but fascicles typically lengthen until mid‐stance as the knee extends. Influenced by the activity of the dorsal knee extensor femorotibialis, the FTI muscle continues to passively lengthen simultaneously with knee extension and a shift to tensile axial strain on the anterior femur at approximately 40% of stance. The near coincidence in timing of peak compressive bone strain and peak muscle shortening (5.4 ± 4.1% stance) indicates a close correlation between the action of the hip extensor/knee flexor, FTI, and femoral loading in the cooter hindlimb. In the context of equilibrium models of limb bone loading, these results may help explain differences in safety factor estimates observed between previous force platform and in vivo strain analyses in cooters. J. Morphol. 274:1060–1069, 2013. © 2013 Wiley Periodicals, Inc.