Differential leg and trunk operation during skipping without and with hurdles in bipedal Japanese macaque.

When locomoting bipedally at higher speeds, macaques preferred unilateral skipping (galloping). The same skipping pattern was maintained while hurdling across two low obstacles at the distance of a stride within our experimental track. The present study investigated leg and trunk joint rotations and leg joint moments, with the aim of clarifying the differential leg and trunk operation during skipping in bipedal macaques. Especially at the hip, the range of joint rotation and extension at lift off was larger in the leading than in the trailing leg. The flexing knee absorbed energy and the extending ankle generated work during each step. The trunk showed only minor deviations from symmetry. Hurdling amplified the differences and notably resulted in a quasi-elastic use of the leading knee and in an asymmetric operation of the trunk.

Skipping without and with hurdles in bipedal macaque: global mechanics.

Macaques trained to perform bipedally used running gaits across a wide range of speeds. At higher speeds they preferred unilateral skipping (galloping). The same asymmetric stepping pattern was used while hurdling across two low obstacles placed at the distance of a stride within our experimental track. In bipedal macaques during skipping, we expected a differential use of the trailing and leading legs. The present study investigated global properties of the effective and virtual leg, the location of the virtual pivot point (VPP), and the energetics of the center of mass (CoM), with the aim of clarifying the differential leg operation during skipping in bipedal macaques. When skipping, macaques displayed minor double support and aerial phases during one stride. Asymmetric leg use was indicated by differences in leg kinematics. Axial damping and tangential leg work did not influence the indifferent peak ground reaction forces and impulses, but resulted in a lift of the CoM during contact of the leading leg. The aerial phase was largely due to the use of the double support. Hurdling amplified the differential leg operation. Here, higher ground reaction forces combined with increased double support provided the vertical impulse to overcome the hurdles. Following CoM dynamics during a stride, skipping and hurdling represented bouncing gaits. The elevation of the VPP of bipedal macaques resembled that of human walking and running in the trailing and leading phases, respectively. Because of anatomical restrictions, macaque unilateral skipping differs from that of humans, and may represent an intermediate gait between grounded and aerial running.

Limb, joint and pelvic kinematic control in the quail coping with steps upwards and downwards.

Small cursorial birds display remarkable walking skills and can negotiate complex and unstructured terrains with ease. The neuromechanical control strategies necessary to adapt to these challenging terrains are still not well understood. Here, we analyzed the 2D- and 3D pelvic and leg kinematic strategies employed by the common quail to negotiate visible steps (upwards and downwards) of about 10%, and 50% of their leg length. We used biplanar fluoroscopy to accurately describe joint positions in three dimensions and performed semi-automatic landmark localization using deep learning. Quails negotiated the vertical obstacles without major problems and rapidly regained steady-state locomotion. When coping with step upwards, the quail mostly adapted the trailing limb to permit the leading leg to step on the elevated substrate similarly as it did during level locomotion. When negotiated steps downwards, both legs showed significant adaptations. For those small and moderate step heights that did not induce aerial running, the quail kept the kinematic pattern of the distal joints largely unchanged during uneven locomotion, and most changes occurred in proximal joints. The hip regulated leg length, while the distal joints maintained the spring-damped limb patterns. However, to negotiate the largest visible steps, more dramatic kinematic alterations were observed. There all joints contributed to leg lengthening/shortening in the trailing leg, and both the trailing and leading legs stepped more vertically and less abducted. In addition, locomotion speed was decreased. We hypothesize a shift from a dynamic walking program to more goal-directed motions that might be focused on maximizing safety.

Comparative analysis of a geometric and an adhesive righting strategy against toppling in inclined hexapedal locomotion.

Animals are known to exhibit different walking behaviors in hilly habitats. For instance, cats, rats, squirrels, tree frogs, desert iguana, stick insects and desert ants were observed to lower their body height when traversing slopes, whereas mound-dwelling iguanas and wood ants tend to maintain constant walking kinematics regardless of the slope. This paper aims to understand and classify these distinct behaviors into two different strategies against toppling for climbing animals by looking into two factors: (i) the torque of the center of gravity (CoG) with respect to the critical tipping axis, and (ii) the torque of the legs, which has the potential to counterbalance the CoG torque. Our comparative locomotion analysis on level locomotion and inclined locomotion exhibited that primarily only one of the proposed two strategies was chosen for each of our sample species, despite the fact that a combined strategy could have reduced the animal's risk of toppling over even more. We found that Cataglyphis desert ants (species Cataglyphis fortis) maintained their upright posture primarily through the adjustment of their CoG torque (geometric strategy), and Formica wood ants (species Formica rufa), controlled their posture primarily by exerting leg torques (adhesive strategy). We further provide hints that the geometric strategy employed by Cataglyphis could increase the risk of slipping on slopes as the leg-impulse substrate angle of Cataglyphis hindlegs was lower than that of Formica hindlegs. In contrast, the adhesion strategy employed by Formica front legs not only decreased the risk of toppling but also explained the steeper leg-impulse substrate angle of Formica hindlegs which should relate to more bending of the tarsal structures and therefore to more microscopic contact points, potentially reducing the risk of hindleg slipping.

Measuring strain in the exoskeleton of spiders-virtues and caveats.

The measurement of cuticular strain during locomotion using foil strain gauges provides information both on the loads of the exoskeleton bears and the adaptive value of the specific location of natural strain detectors (slit sense organs). Here, we critically review available literature. In tethered animals, by applying loads to the metatarsus tip, strain and mechanical sensitivity (S = strain/load) induced at various sites in the tibia were determined. The loci of the lyriform organs close to the tibia-metatarsus joint did not stand out by high strain. The strains induced at various sites during free locomotion can be interpreted based on S and, beyond the joint region, on beam theory. Spiders avoided laterad loading of the tibia-metatarsus joint during slow locomotion. Balancing body weight, joint flexors caused compressive strain at the posterior and dorsal tibia. While climbing upside down strain measurements indicate strong flexor activity. In future studies, a precise calculation and quantitative determination of strain at the sites of the lyriform organs will profit from more detailed data on the overall strain distribution, morphology, and material properties. The values and caveats of the strain gauge technology, the only one applicable to freely moving spiders, are discussed.

The influence of sagittal trunk lean on uneven running mechanics.

The role of trunk orientation during uneven running is not well understood. This study compared the running mechanics during the approach step to and the step down for a 10 cm expected drop, positioned halfway through a 15 m runway, with that of the level step in 12 participants at a speed of 3.5 m s-1 while maintaining self-selected (17.7±4.2 deg; mean±s.d.), posterior (1.8±7.4 deg) and anterior (26.6±5.6 deg) trunk leans from the vertical. Our findings reveal that the global (i.e. the spring-mass model dynamics and centre-of-mass height) and local (i.e. knee and ankle kinematics and kinetics) biomechanical adjustments during uneven running are specific to the step nature and trunk posture. Unlike the anterior-leaning posture, running with a posterior trunk lean is characterized by increases in leg angle, leg compression, knee flexion angle and moment, resulting in a stiffer knee and a more compliant spring-leg compared with the self-selected condition. In the approach step versus the level step, reductions in leg length and stiffness through the ankle stiffness yield lower leg force and centre-of-mass position. Contrariwise, significant increases in leg length, angle and force, and ankle moment, reflect in a higher centre-of-mass position during the step down. Plus, ankle stiffness significantly decreases, owing to a substantially increased leg compression. Overall, the step down appears to be dominated by centre-of-mass height changes, regardless of having a trunk lean. Observed adjustments during uneven running can be attributed to anticipation of changes to running posture and height. These findings highlight the role of trunk posture in human perturbed locomotion relevant for the design and development of exoskeleton or humanoid bipedal robots.

Trunk and leg kinematics of grounded and aerial running in bipedal macaques.

Across a wide range of Froude speeds, non-human primates such as macaques prefer to use grounded and aerial running when locomoting bipedally. Both gaits are characterized by bouncing kinetics of the center of mass. In contrast, a discontinuous change from pendular to bouncing kinetics occurs in human locomotion. To clarify the mechanism underlying these differences in bipedal gait mechanics between humans and non-human primates, we investigated the influence of gait on joint kinematics in the legs and trunk of three macaques crossing an experimental track. The coordination of movement was compared with observations available for primates. Compared with human running, macaque leg retraction cannot merely be produced by hip extension, but needs to be supported by substantial knee flexion. As a result, despite quasi-elastic whole-leg operation, the macaque's knee showed only minor rebound behavior. Ankle extension resembled that observed during human running. Unlike human running and independent of gait, torsion of the trunk represents a rather conservative feature in primates, and pelvic axial rotation added to step length. Pelvic lateral lean during grounded running by macaques (compliant leg) and human walking (stiff leg) depends on gait dynamics at the same Froude speed. The different coordination between the thorax and pelvis in the sagittal plane as compared with human runners indicates different bending modes of the spine. Morphological adaptations in non-human primates to quadrupedal locomotion may prevent human-like operation of the leg and limit exploitation of quasi-elastic leg operation despite running dynamics.

Low leg compliance permits grounded running at speeds where the inverted pendulum model gets airborne.

Animals typically switch from grounded (no flight phases) to aerial running at dimensionless speeds u^ < 1. But some birds use grounded running far above u^ = 1, which puzzles biologists because the inverted pendulum becomes airborne at this speed. Here, we combine computer experiments using the spring-mass model with locomotion data from small birds, macaques and humans to understand the relationship between leg function (stiffness, angle of attack), locomotion speed and gait. With our model, we found three-humped ground reaction force profiles for slow grounded running speeds. The minimal single-humped grounded running speed is u^ = 0.4. This speed value roughly coincides with the transition speed from vaulting to bouncing mechanics in bipeds. Maximal grounded running speed in the model is not limited. In experiments, animals changed from grounded to aerial running at dimensionless contact time around 1. Considering these real-world contact times reduces the solution space drastically, but experimental data fit well. The model still predicts maximal grounded running speed  u^ > 1 for low stiffness values used by birds but decreases below u^ = 1 for increasing stiffness. For stiffer legs used in human walking and running, periodic grounded running vanishes. At speeds at which birds and macaques change to aerial running, we found periodic aerial running to intersect grounded running. This could explain why animals can alternate between grounded and aerial running at the same speed and identical leg parameters. Compliant legs enable different gaits and speeds with similar leg parameters, stiff legs require parameter adaptations.

Humans adjust the height of their center of mass within one step when running across camouflaged changes in ground level.

In running, humans use different control strategies that are most likely influenced by environmental conditions. For example, when human runners face a change in ground level, they adapt the height of their center of mass (CoM) in preparation. In a situation in which a drop might occur but without visual cues regarding its actual height, such a preparation is not possible. We here used camouflaged drops (which occurred by chance) as mechanical disturbances and analyzed the adaptations in the vertical oscillation of the runners CoM. We found that humans lowered their CoM by about 25% of the possible drop height in preparation for the camouflaged contact, regardless of whether a drop occurred or not. In flight phase following the disturbance, the CoM was lowered by about 90% of the drop height in the case of the camouflaged drop and remained almost unaffected (+5%) in the case of level ground. Thus, runners resort to a CoM-control strategy with a fixed desired trajectory height in the flight phase following the camouflaged ground contact. In contrast to previously reported results which show that visible ground level changes were compensated within several steps, this strategy compensates ground level disturbances instantly within a single step.

Global dynamics of bipedal macaques during grounded and aerial running.

Macaques trained to perform bipedally use grounded running, skipping and aerial running, but avoid walking. The preference for grounded running across a wide range of speeds is substantially different from the locomotion habits observed in humans, which may be the result of differences in leg compliance. In the present study, based on kinematic and dynamic observations of three individuals crossing an experimental track, we investigated global leg properties such as leg stiffness and viscous damping during grounded and aerial running. We found that, in macaques, similar to human and bird bipedal locomotion, the vector of the ground reaction force is directed from the center of pressure (COP) to a virtual pivot point above the center of mass (COM). The visco-elastic leg properties differ for the virtual leg (COM-COP) and the effective leg (hip-COP) because of the position of the anatomical hip with respect to the COM. The effective leg shows damping in the axial direction and positive work in the tangential component. Damping does not prevent the exploration of oscillatory modes. Grounded running is preferred to walking because of leg compliance. The transition from grounded to aerial running is not accompanied by a discontinuous change. With respect to dynamic properties, macaques seem to be well placed between bipedal specialists (humans and birds). We speculate that the losses induced in the effective leg by hip placement and slightly pronograde posture may not pay off by facilitating stabilization, making bipedal locomotion expensive and insecure for macaques.

Bipedal gait versatility in the Japanese macaque (Macaca fuscata).

It was previously believed that, among primates, only humans run bipedally. However, there is now growing evidence that at least some non-human primates can not only run bipedally but can also generate a running gait with an aerial phase. Japanese macaques trained for bipedal performances have been known to exhibit remarkable bipedal locomotion capabilities, but no aerial-phase running has previously been reported. In the present study, we investigated whether Japanese macaques could run with an aerial phase by collecting bipedal gait sequences from three macaques on a level surface at self-selected speeds (n = 188). During our experiments, body kinematics and ground reaction forces were recorded by a motion-capture system and two force plates installed within a wooden walkway. Our results demonstrated that macaques were able to utilize a variety of bipedal gaits including grounded running, skipping, and even running with an aerial phase. The self-selected bipedal locomotion speed of the macaques was fast, with Froude speed ranging from 0.4 to 1.3. However, based on congruity, no single trial that could be categorized as a pendulum-like walking gait was observed. The parameters describing the temporal, kinematic, and dynamic characteristics of macaque bipedal running gaits follow the patterns previously documented for other non-human primates and terrestrial birds that use running gaits, but are different from those of humans and from birds' walking gaits. The present study confirmed that when a Japanese macaque engages in bipedal locomotion, even without an aerial phase, it generally utilizes a spring-like running mechanism because the animals have a limited ability to stiffen their legs. That limitation is due to anatomical restrictions determined by the morphology and structure of the macaque musculoskeletal system. The general adoption of grounded running in macaques and other non-human primates, along with its absence in human bipedal locomotion, suggests that abandonment of compliant gait was a critical transition in the evolution of human obligatory bipedalism.

Locomotor stability in able-bodied trunk-flexed gait across uneven ground.

This study aimed to explore the control of dynamic stability of the imposed trunk-flexed gaits across uneven ground. For ten young healthy participants, we compared the anteroposterior margin of stability (MoS) and lower limb joint kinematics at foot-contact during accommodating a consecutive stepdown and step-up (10-cm visible drop) to that of level steps while maintaining four postures: regular erect, ∼30°, ∼50° and maximal trunk flexion from the vertical. Two-way repeated measures ANOVAs revealed no significant step × posture interactions for the MoS (p = .187) and for the parameters that contributed to the MoS calculation (p > .05), whereas significant interactions were found for the hip flexion, hip position (relative to the posterior boundary of the base of support) and the knee flexion. The main effect of step (p = .0001), but not posture (p = .061), on the MoS was significant. Post hoc tests, compared with the level step, showed that the decreased magnitude of the MoS during stepping down (p = .011)-mainly due to a further forward displacement of the center of mass position (p = .006)-significantly increased in the immediate following step-up (p = .002) as a consequence of a substantial increase in the base of support (p = .003). In the stepdown versus level step, the hip and knee flexions as well as the hip position did not significantly change in the trunk-flexed gaits (p > .05). In the step-up, the knee flexion increased (except for the gaits with the maximum trunk flexion), whereas other kinematic variables remained unchanged. Quantifying the step-to-step control of dynamic stability in a perturbed walking reflected continuous control adaptations through the interaction between gait and posture. In fact, the able-bodied participants were able to safely control the motion of the body's CoM with the combination of compensatory kinematic adjustments in lower-limb and adaptations in stepping pattern.

Packing of muscles in the rabbit shank influences three-dimensional architecture of M. soleus.

Isolated and packed muscles (e.g. in the calf) exhibit different three-dimensional muscle shapes. In packed muscles, cross-sections are more angular compared to the more elliptical ones in isolated muscles. As far as we know, it has not been examined yet, whether the shape of the muscle in its packed condition influences its internal arrangement of muscle fascicles and accordingly the contraction behavior in comparison to the isolated condition. To evaluate the impact of muscle packing, we examined the three-dimensional muscle architecture of isolated and packed rabbit M. soleus for different ankle angles (65°, 75°, 85°, 90°, and 95°) using manual digitization (MicroScribe® MLX). In general, significantly increased values of pennation angle and fascicle curvature were found in packed compared to isolated M. soleus (except for fascicle curvature at 90° ankle angle). On average, fascicle length of isolated muscles exceeded fascicle lengths of packed muscles by 2.6%. Reduction of pennation angle in the packed condition had only marginal influence on force generation (about 1% of maximum isometric force) in longitudinal direction (along the line of action) although an increase of transversal force component (perpendicular to the line of action) of about 26% is expected. Results of this study provide initial evidence that muscle packing limits maximum muscle performance observed in isolated M. soleus. Besides an enhanced understanding of the impact of muscle packing on architectural parameters, the outcomes of this study are essential for realistic three-dimensional muscle modeling and model validation.

The effects of an expected twofold perturbation on able-bodied gait: Trunk flexion and uneven ground surface.

BACKGROUND: Although alteration in trunk orientation and ground level potentially affects gait pattern individually, it is plausible to examine the interaction effects of such factors. OBJECTIVE: The interaction effects between trunk-flexed gait and uneven ground on able-bodied gait pattern. METHODS: For twelve able-bodied participants, we compared the adaptive mechanisms in kinematics, kinetics and spatial-temporal parameters of gait (STPG) with bent postures (30° and 50° of sagittal trunk flexion) across uneven surface (10-cm visible drop at the sight of the second ground contact) with that of upright posture on even ground surface. RESULTS: Significant between-posture changes on the uneven surface included a decreased peak ankle dorsiflexion angle and vertical ground reaction force (GRF) 2nd peak as trunk flexion increased. Moreover, significant between-ground surface changes for each individual gait posture were a decreased peak ankle dorsiflexion angle and ankle range of motion irrespective of trunk posture and a reduced trailing step duration and vertical GRF 2nd peak in upright walking. The spatial parameters of gait remained unchanged across uneven surface, but at the expense of pronounced adjustments in temporal parameters, i.e., a more conservative gait strategy, indicating a distinct contribution from spatial and temporal strategies in trunk-flexed gaits. This was associated with greater peak flexion angles across lower limb joints regardless of trunk posture, alongside with an exertion of greater forces at faster rates earlier in stance and attenuated forces at lower rates at the end of the stance (i.e., early-skewed vertical GRF). When considering the main effect of posture, a more crouched gait was executed with reduced temporal parameters (except for cadence) and an early-skewed vertical GRF patterns with increasing trunk flexion. SIGNIFICANCE: These results may have implications for understanding the nature of compensatory mechanisms in gait pattern of older adults and/or patients with altered trunk orientations while accommodating uneven ground.

Posture alteration as a measure to accommodate uneven ground in able-bodied gait.

Though the effects of imposed trunk posture on human walking have been studied, less is known about such locomotion while accommodating changes in ground level. For twelve able participants, we analyzed kinematic parameters mainly at touchdown and toe-off in walking across a 10-cm visible drop in ground level (level step, pre-perturbation step, step-down, step-up) with three postures (regular erect, ~30° and ~50° of trunk flexion from the vertical). Two-way repeated measures ANOVAs revealed step-specific effects of posture on the kinematic behavior of gait mostly at toe-off of the pre-perturbation step and the step-down as well as at touchdown of the step-up. In preparation to step-down, with increasing trunk flexion the discrepancy in hip-center of pressure distance, i.e. effective leg length, (shorter at toe-off versus touchdown), compared with level steps increased largely due to a greater knee flexion at toe-off. Participants rotated their trunk backwards during step-down (2- to 3-fold backwards rotation compared with level steps regardless of trunk posture) likely to control the angular momentum of their whole body. The more pronounced trunk backwards rotation in trunk-flexed walking contributed to the observed elevated center of mass (CoM) trajectories during the step-down which may have facilitated drop negotiation. Able-bodied individuals were found to recover almost all assessed kinematic parameters comprising the vertical position of the CoM, effective leg length and angle as well as hip, knee and ankle joint angles at the end of the step-up, suggesting an adaptive capacity and hence a robustness of human walking with respect to imposed trunk orientations. Our findings may provide clinicians with insight into a kinematic interaction between posture and locomotion in uneven ground. Moreover, a backward rotation of the trunk for negotiating step-down may be incorporated into exercise-based interventions to enhance gait stability in individuals who exhibit trunk-flexed postures during walking.

Force direction patterns promote whole body stability even in hip-flexed walking, but not upper body stability in human upright walking.

Directing the ground reaction forces to a focal point above the centre of mass of the whole body promotes whole body stability in human and animal gaits similar to a physical pendulum. Here we show that this is the case in human hip-flexed walking as well. For all upper body orientations (upright, 25°, 50°, maximum), the focal point was well above the centre of mass of the whole body, suggesting its general relevance for walking. Deviations of the forces' lines of action from the focal point increased with upper body inclination from 25 to 43 mm root mean square deviation (RMSD). With respect to the upper body in upright gait, the resulting force also passed near a focal point (17 mm RMSD between the net forces' lines of action and focal point), but this point was 18 cm below its centre of mass. While this behaviour mimics an unstable inverted pendulum, it leads to resulting torques of alternating sign in accordance with periodic upper body motion and probably provides for low metabolic cost of upright gait by keeping hip torques small. Stabilization of the upper body is a consequence of other mechanisms, e.g. hip reflexes or muscle preflexes.

Propulsion in hexapod locomotion: how do desert ants traverse slopes?

The employment of an alternating tripod gait to traverse uneven terrains is a common characteristic shared among many Hexapoda. Because this could be one specific cause for their ecological success, we examined the alternating tripod gait of the desert ant Cataglyphis fortis together with their ground reaction forces and weight-specific leg impulses for level locomotion and on moderate (±30 deg) and steep (±60 deg) slopes in order to understand mechanical functions of individual legs during inclined locomotion. There were three main findings from the experimental data. (1) The hind legs acted as the main brake (negative weight-specific impulse in the direction of progression) on both the moderate and steep downslopes while the front legs became the main motor (positive weight-specific impulse in the direction of progression) on the steep upslope. In both cases, the primary motor or brake was found to be above the centre of mass. (2) Normalised double support durations were prolonged on steep slopes, which could enhance the effect of lateral shear loading between left and right legs with the presence of direction-dependent attachment structures. (3) The notable directional change in the lateral ground reaction forces between the moderate and steep slopes implied the utilisation of different coordination programs in the extensor-flexor system.

Increasing trunk flexion transforms human leg function into that of birds despite different leg morphology.

Pronograde trunk orientation in small birds causes prominent intra-limb asymmetries in the leg function. As yet, it is not clear whether these asymmetries induced by the trunk reflect general constraints on the leg function regardless of the specific leg architecture or size of the species. To address this, we instructed 12 human volunteers to walk at a self-selected velocity with four postures: regular erect, or with 30 deg, 50 deg and maximal trunk flexion. In addition, we simulated the axial leg force (along the line connecting hip and centre of pressure) using two simple models: spring and damper in series, and parallel spring and damper. As trunk flexion increases, lower limb joints become more flexed during stance. Similar to birds, the associated posterior shift of the hip relative to the centre of mass leads to a shorter leg at toe-off than at touchdown, and to a flatter angle of attack and a steeper leg angle at toe-off. Furthermore, walking with maximal trunk flexion induces right-skewed vertical and horizontal ground reaction force profiles comparable to those in birds. Interestingly, the spring and damper in series model provides a superior prediction of the axial leg force across trunk-flexed gaits compared with the parallel spring and damper model; in regular erect gait, the damper does not substantially improve the reproduction of the human axial leg force. In conclusion, mimicking the pronograde locomotion of birds by bending the trunk forward in humans causes a leg function similar to that of birds despite the different morphology of the segmented legs.

Stability in skipping gaits.

As an alternative to walking and running, humans are able to skip. However, adult humans avoid it. This fact seems to be related to the higher energetic costs associated with skipping. Still, children, some birds, lemurs and lizards use skipping gaits during daily locomotion. We combined experimental data on humans with numerical simulations to test whether stability and robustness motivate this choice. Parameters for modelling were obtained from 10 male subjects. They locomoted using unilateral skipping along a 12 m runway. We used a bipedal spring loaded inverted pendulum to model and to describe the dynamics of skipping. The subjects displayed higher peak ground reaction forces and leg stiffness in the first landing leg (trailing leg) compared to the second landing leg (leading leg). In numerical simulations, we found that skipping is stable across an amazing speed range from skipping on the spot to fast running speeds. Higher leg stiffness in the trailing leg permits longer strides at same system energy. However, this strategy is at the same time less robust to sudden drop perturbations than skipping with a stiffer leading leg. A slightly higher stiffness in the leading leg is most robust, but might be costlier.