Gaits of Japanese macaques (Macaca fuscata) on a horizontal ladder and arboreal stability

Most primates use diagonal sequence (DS), diagonal couplets (DC) gaits when they walk or run quadrupedally, and it has been suggested that DSDC gaits contribute to stability in their natural arboreal habitats compared to other symmetrical gaits. However, this postulate is based solely on studies of primate gaits using continuous terrestrial and arboreal substrates. A particular species may select suitable gaits according to the substrate properties. Here, we analyzed the gaits of Japanese macaques moving on a horizontal ladder with rung intervals ranging from 0.40 to 0.80 m to elucidate the relative advantages of each observed form of gait. The rung arrangement forced our macaques to choose either diagonal coupling or DS gaits. One macaque consistently used diagonal coupling (i.e., DSDC and LSDC gaits) across narrow and intermediate rung intervals, whereas the other macaque used DS gaits (i.e., DSDC and DSLC gaits). At wider rung intervals, both macaques shifted to a two‐one sequence (TOS), which is characterized by two nearly simultaneous touchdowns of both forelimbs and one touchdown of each hind limb in a stride. The transition to the TOS sequence increased the duration of support on multiple limbs, but always included periods of a whole‐body aerial phase. These results suggest that Japanese macaques prefer DSDC gaits, because the diagonal coupling and DS contribute separately to stability on complex supports compared to the lateral coupling and lateral sequence. We also postulate that stability triggers the transition from symmetrical gaits to the TOS sequence. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Symmetrical gaits of Cebus apella: implications for the functional significance of diagonal sequence gait in primates

Quadrupedal locomotion of primates is distinguished from the quadrupedalism of many other mammals by several features, including a diagonal sequence (DS) footfall used in symmetrical gaits. This presumably unique feature of primate locomotion has been attributed to an ancestral adaptation for cautious arboreal quadrupedalism on thin, flexible branches. However, the functional significance of DS gait remains largely hypothetical. The study presented here tests hypotheses about the functional significance of DS gait by analyzing the gait mechanics of a primate that alternates between DS and lateral sequence (LS) gaits, Cebus apella. Kinematic and kinetic data were gathered from two subjects as they moved across both terrestrial and simulated arboreal substrates. These data were used to test four hypotheses: (1) locomotion on arboreal supports is associated with increased use of DS gait, (2) DS gait is associated with lower peak vertical substrate reaction forces than LS gait, (3) DS gait is associated with greater forelimb/hind limb differentiation in force magnitudes, and (4) DS gait offers increased stability. Our results indicate that animals preferred DS gait on the arboreal substrate, and LS gait while on the ground. Peak vertical substrate reaction forces showed a tendency to be lower in DS gait, but not consistently so. Pole ("arboreal") forces were lower than ground forces in DS gait, but not in LS gait. The preferred symmetrical gait on both substrates was a grounded run or amble, with the body supported by only one limb throughout most of the stride. During periods of bilateral support, the DS gait had predominantly diagonal support couplets. This benefit for stability on an arboreal substrate is potentially outweighed by overstriding, its associated ipsilateral limb interference in DS gait and hind foot positioning in front of the hand on untested territory. DS gait also did not result in an optimal anchoring position of the hind foot under the center of mass of the body at forelimb touchdown. In sum, the results are mixed regarding the superiority of DS gait in an arboreal setting. Consequently, the notion that DS gait is an ancestral adaptation of primates, conditioned by the selection demands of an arboreal environment, remains largely hypothetical.     

Gait selection and the ontogeny of quadrupedal walking in squirrel monkeys (Saimiri boliviensis)

Locomotor researchers have long known that adult primates employ a unique footfall sequence during walking. Most mammals use lateral sequence (LS) gaits, in which hind foot touchdowns are followed by ipsilateral forefoot touchdowns. In contrast, most quadrupedal primates use diagonal sequence (DS) gaits, in which hind foot touchdowns are followed by contralateral forefoot touchdowns. However, gait selection in immature primates is more variable, with infants and juveniles frequently using LS gaits either exclusively or in addition to DS gaits. I explored the developmental bases for this phenomenon by examining the ontogeny of gait selection in juvenile squirrel monkeys walking on flat and simulated arboreal substrates (i.e., a raised pole). Although DS gaits predominated throughout development, the juvenile squirrel monkeys nonetheless utilized LS gaits in one-third of the ground strides and in one-sixth of pole strides. Multiple logistic regression analyses showed that gait selection within the juvenile squirrel monkey sample was not significantly associated with either age or body mass per se, arguing against the oft-cited argument that general neuromuscular maturation is responsible for ontogenetic changes in preferred footfall sequence. Rather, lower level biomechanical variables, specifically the position of the whole-body center of mass and the potential for interference between ipsilateral fore and hindlimbs, best explained variation in footfall patterns. Overall, results demonstrate the promise of developmental studies of growth and locomotor development to serve as "natural laboratories" in which to explore how variability in morphology is, or is not, associated with variability in locomotor behavior.     

Origins of primate locomotion: gait mechanics of the woolly opossum

The locomotion of primates differs from that of other mammals in three fundamental ways. During quadrupedal walking, primates use diagonal sequence gaits, protract their arms more at forelimb touchdown, and experience lower vertical substrate reaction forces on their forelimbs relative to their hindlimbs. It is widely held that the unusual walking gaits of primates represent a basal adaptation for movement on thin, flexible branches and reflect a major change in the functional role of the forelimb. However, little data on nonprimate arboreal mammals exist to test this notion. To that end, we examined the gait mechanics of the woolly opossum (Caluromys philander), a marsupial convergent with small-bodied prosimians in ecology, behavior, and morphology. Data on the footfall sequence, relative arm protraction, and peak vertical substrate reaction forces were obtained from videotapes and force records for three adult woolly opossums walking quadrupedally on a wooden runway and a thin pole. For all steps recorded on both substrates, woolly opossums always used diagonal sequence walking gaits, protracted their arms beyond 90 degrees relative to horizontal body axis, and experienced peak vertical substrate reaction forces on forelimbs that were significantly lower than on hindlimbs. The woolly opossum is the first nonprimate mammal to show locomotor mechanics that are identical to those of primates. This case of convergence between primates and a committed fine-branch, arboreal marsupial strongly implies that the earliest primates evolved gait specializations for fine-branch locomotion, which reflect important changes in forelimb function.     

Substrate determines asymmetrical gait dynamics in marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri boliviensis)

Studies of skeletal pathology indicate that injury from falling accounts for most long bone trauma in free‐ranging primates, suggesting that primates should be under strong selection to manifest morphological and behavioral mechanisms that increase stability on arboreal substrates. Although previous studies have identified several kinematic and kinetic features of primate symmetrical gaits that serve to increase arboreal stability, very little work has focused on the dynamics of primate asymmetrical gaits. Nevertheless, asymmetrical gaits typify the rapid locomotion of most primates, particularly in smaller bodied taxa. This study investigated asymmetrical gait dynamics in growing marmosets and squirrel monkeys moving on terrestrial and simulated arboreal supports (i.e., an elevated pole). Results showed that monkeys used several kinematic and kinetic adjustments to increase stability on the pole, including reducing peak vertical forces, limiting center of mass movements, increasing substrate contact durations, and using shorter and more frequent strides (thus limiting disruptive whole‐body aerial phases). Marmosets generally showed greater adjustment to pole locomotion than did squirrel monkeys, perhaps as a result of their reduced grasping abilities and retreat from the fine‐branch niche. Ontogenetic increases in body size had relatively little independent influence on asymmetrical gait dynamics during pole locomotion, despite biomechanical theory suggesting that arboreal instability is exacerbated as body size increases relative to substrate diameter. Overall, this study shows that 1) symmetrical gaits are not the only stable way to travel arboreally and 2) small‐bodied primates utilize specific kinematic and kinetic adjustments to increase stability when using asymmetrical gaits on arboreal substrates. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque

Climbing is one of the most important components of primate locomotor modes. We previously reported that the kinesiological characteristics of vertical climbing by the spider monkey and Japanese macaque are clearly different, based on their kinetics and kinematics. In this study, a more detailed analysis using inverse dynamics was conducted to estimate the biomechanical characteristics of vertical climbing in the spider monkey and Japanese macaque. One of the main findings was the difference in forelimb use by the two species. The results of a joint moment analysis and estimates of muscular force indicate that the spider monkey uses its forelimbs to keep the body close to the substrate, rather than to generate propulsion. The forelimb of the Japanese macaque, on the other hand, likely contributes more to propulsion. This supports the idea that "forelimb-hindlimb differentiation" is promoted in the spider monkey. The estimated muscular force also suggests that the spider monkey type of climbing could develop the hindlimb extensor muscles, which are important in bipedal posture and walking. As a result, we conclude that the spider monkey type of climbing could be functionally preadaptive for human bipedalism. This type of climbing would develop the hip and knee extensor muscles, and result in more extended lower limb joints, a more erect trunk posture, and more functionally differentiated fore- and hindlimbs, all of which are important characteristics of human bipedalism.     

Manual digital pressures during knuckle‐walking in chimpanzees (Pan troglodytes)

Considerable attention has been given to hand morphology and function associated with knuckle‐walking in the African apes because of the implications they have for the evolution of bipedalism in early hominins. Knuckle‐walking is associated with a unique suite of musculoskeletal features of the wrist and hand, and numerous studies have hypothesized that these anatomical features are associated with the dynamics of load distribution across the digits during knuckle‐walking. We collected dynamic digital pressures on two chimpanzees during terrestrial and simulated arboreal locomotion. Comparisons were made across substrates, limb positions, hand positions, and age categories. Peak digital pressures were similar on the pole and on the ground but were distributed differently across the digits on each substrate. In young animals, pressure was equally high on digits 2–4 on the ground but higher on digits 3 and 4 on the pole. Older animals experience higher pressures on digits 2 and 3 on the ground. Hand posture (palm‐in vs. palm‐back) influenced the distribution and timing of peak pressures. Age‐related increases in body mass also result in higher overall pressures and increased variation across the digital row. In chimpanzees, digit 5 typically bears relatively little load regardless of hand position or substrate. These are the first quantitative data on digital pressures during knuckle‐walking in hominoids, and they afford the opportunity to develop hypotheses about variation among hominoids and biomechanical models of wrist and forearm loading. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Development of an anatomically based whole‐body musculoskeletal model of the Japanese macaque (Macaca fuscata)

We constructed a three‐dimensional whole‐body musculoskeletal model of the Japanese macaque (Macaca fuscata) based on computed tomography and dissection of a cadaver. The skeleton was modeled as a chain of 20 bone segments connected by joints. Joint centers and rotational axes were estimated by joint morphology based on joint surface approximation using a quadric function. The path of each muscle was defined by a line segment connecting origin to insertion through an intermediary point if necessary. Mass and fascicle length of each were systematically recorded to calculate physiological cross‐sectional area to estimate the capacity of each muscle to generate force. Using this anatomically accurate model, muscle moment arms and force vectors generated by individual limb muscles at the foot and hand were calculated to computationally predict muscle functions. Furthermore, three‐dimensional whole‐body musculoskeletal kinematics of the Japanese macaque was reconstructed from ordinary video sequences based on this model and a model‐based matching technique. The results showed that the proposed model can successfully reconstruct and visualize anatomically reasonable, natural musculoskeletal motion of the Japanese macaque during quadrupedal/bipedal locomotion, demonstrating the validity and efficacy of the constructed musculoskeletal model. The present biologically relevant model may serve as a useful tool for comprehensive understanding of the design principles of the musculoskeletal system and the control mechanisms for locomotion in the Japanese macaque and other primates. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Differences in terrestrial velocity in Macaca and Presbytis

Over 150 sequences of terrestrial movement were timed and measured in the toque macaque, the gray langur, and the purple-faced langur to determine the relation between velocity, gait, and psychosocial context. Species differences were found in mean velocity, “favored” gait, and surface preference. All three species used the walk and the gallop at the slowest and fastest speeds respectively. The macaques and gray langurs walked frequently, but the purple-faced langurs were never seen to do so. At intermediate speeds, the macaques used either the “fast” walk or the “slow” gallop, whereas the gray langurs used irregular patterns of walk-gallop-walk-gallop. The purple-faced langurs were faster (about 20 fps) and less variable than the other species, regardless of distance. These data suggest that motor expression varies among the Cercopithecoid monkeys: the correlation between locomotion and anatomy is not as close as it is among wholly terrestrial or arboreal forms; slowness in the macaque is an expression of social confidence, not of biomechanical inability; high speed in the purple-faced langur is due to psychosocial factors rather than to “terrestrial” adaptability.     

Experimentally generated footprints in sand: Analysis and consequences for the interpretation of fossil and forensic footprints

Fossilized footprints contain information about the dynamics of gait, but their interpretation is difficult, as they are the combined result of foot anatomy, gait dynamics, and substrate properties. We explore how footprints are generated in modern humans. Sixteen healthy subjects walked on a solid surface and in a layer of fine‐grained sand. In each condition, 3D kinematics of the leg and foot were analyzed for three trials at preferred speed, using an infrared camera system. Additionally, calibrated plantar pressures were recorded. After each trial in sand, the depth of the imprint was measured under specific sites. When walking in sand, subjects showed greater toe clearance during swing and a 7° higher knee yield during stance. Maximal pressure was the most influential factor for footprint depth under the heel. For other foot zones, a combination of factors correlates with imprint depth, with pressure impulse (the pressure‐time integral) gaining importance distally, at the metatarsal heads and the hallux. We conclude that footprint topology cannot be related to a single variable, but that different zones of the footprint reflect different aspects of the kinesiology of walking. Therefore, an integrated approach, combining anatomical, kinesiological, and substrate‐mechanical insights, is necessary for a correct interpretation. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Dynamic balance in persons with multiple sclerosis who have a falls history is altered compared to non-fallers and to healthy controls

Around 60% of persons with multiple sclerosis (MS) experience falls, however the dynamic balance differences between those who fall and those who don’t are not well understood. The purpose of this study is to identify distinct biomechanical features of dynamic balance during gait that are different between fallers with MS, non-fallers with MS, and healthy controls. 27 recurrent fallers with MS, 28 persons with MS with no falls history, and 27 healthy controls walked on a treadmill at their preferred speed for 3 min. The variability of trunk accelerations and the average and variability of minimum toe clearance, spatiotemporal parameters, and margin of stability were compared between groups. Fallers with MS exhibited a slower cautious gait compared to non-fallers and healthy controls, but had decreased anterior-posterior margin of stability and minimum toe clearance. Fallers walked with less locally stable and predictable trunk accelerations, and increased variability of step length, stride time, and both anterior-posterior and mediolateral margin of stability compared to non-fallers and healthy controls. The present work provides evidence that within a group of persons with MS, there are gait differences that are influenced by falls history. These differences indicate that in persons with MS who fall, the center of mass is poorly controlled through base of support placement and the foot is closer to the ground during swing phase relative to the non-fallers. These identified biomechanical differences could be used to evaluate dynamic balance in persons with MS and to help improve fall prevention strategies.     

Estimating the Functional Axis of the Primate Foot Using the Distribution of Plantar Muscles

Morton (American Journal of Physical Anthropology 5, 305–336, 1922) used the longest metatarsal, which he assumed functions as a lever during locomotion, to define the functional axis of the primate foot. In humans and apes, the functional foot axis lies on the second digit, whereas that of nonhominoid anthropoids is mostly on the third digit, suggesting that a medial shift of the functional axis occurred during primate foot evolution. Myological observations support this idea; the dorsal interossei of the human foot are arranged around the second digit, whereas those of nonhominoid anthropoids are around the third digit. However, it is still unclear when, why, and how such a change in foot musculature occurred. In addition, there is inconsistency among the limited number of studies that have examined foot musculature in apes. We examined modifications in the interosseous muscles of the chimpanzee, gibbon, spider monkey, and Japanese macaque in terms of the shift in the functional foot axis. We found that the dorsal interossei are arranged around the third digit; this is true even in the chimpanzee, whose functional axis based on metatarsal length lies on the second digit. This suggests that the change in the arrangement of the interosseous muscles phylogenetically lagged behind the shift of the osteological axis. Our results also indicate that the dorsal interossei are composite muscles consisting of the deep short flexors and the intermetatarsal abductors. We postulate that changes in the contributions of these 2 components to the formation of dorsal interossei likely occurred in the hominin lineage, resulting in the medial shift of the myological axis. The medial shift of the functional foot axis may have started with the elongation of the second metatarsal in the hominoid ancestors’ lineage, and was completed on the rearrangement of the interosseous muscles.     

Temporal characteristics of plantar shear distribution: relevance to diabetic patients

Diabetic foot ulcers are known to have a biomechanical etiology. Among the mechanical factors that cause foot lesions, shear stresses have been either neglected or underestimated. The purpose of this study was to determine various plantar pressure and shear variables in the diabetic and control groups and compare them. Fifteen diabetic patients with neuropathy and 20 non-diabetic subjects without foot symptoms were recruited. Subjects walked on a custom-built platform capable of measuring local normal and tangential forces simultaneously. Pressure-time integral quantities were increased by 54% (p=0.013) in the diabetic group. Peak AP and resultant shear magnitudes were found to be about 32% larger (p<0.05), even though diabetic subjects walked at a slower velocity. Lower AP and ML stress range (peak-to-peak) values were observed in the control subjects (p<0.05). Shear-time integral values were increased in the diabetic group by 61% and 132% for AP and resultant shear cases, respectively (p<0.05). Plantar shear is known to be a factor in callus formation and has previously been associated with higher ulcer incidence. During gait, shear stresses are induced with twice the frequency of pressure characteristically. Therefore, plantar shear should be investigated further from a broader perspective including the temporal specifications and fatigue failure characteristics of the affected plantar tissue.     

Neuromuscular response of hip-spanning and low back muscles to medio-lateral foot center of pressure manipulation during gait

Background: Footwear-generated medio-lateral foot center of pressure manipulation has been shown to have potential positive effects on gait parameters of hip osteoarthritis patients, ultimately reducing maximum joint reaction forces. The objective of this study was to investigate effects of medio-lateral foot center of pressure manipulation on muscle activity of hip-spanning and back muscles during gait in bilateral hip osteoarthritis patients. Methods: Foot center of pressure was shifted along the medio-lateral foot axis using a foot-worn biomechanical device allowing controlled center of pressure manipulation. Sixteen female bilateral hip osteoarthritis patients underwent electromyography analysis while walking in the device set to three parasagittal configurations: neutral (control), medial, and lateral. Seven hip-spanning muscles (Gluteus Medius, Gluteus Maximus, Tensor Fascia Latae, Rectus Femoris, Semitendinosis, Biceps Femoris, Adductor Magnus) and one back muscle (Erector Spinae) were analyzed. Magnitude and temporal parameters were calculated. Results: The amplitude and temporal parameter varied significantly between foot center of pressure positions for 5 out of 8 muscles each for either the more or less symptomatic leg in at least one subphase of the gait cycle. Conclusion: Medio-lateral foot center of pressure manipulation significantly affects neuromuscular pattern of hip and back musculature during gait in female hip bilateral osteoarthritis patients.     

Foot structure and knee joint kinetics during walking with and without wedged footwear insoles

The relationship between static foot structure characteristics and knee joint biomechanics during walking, or the biomechanical response to wedged insoles are currently unknown. In this study, 3D foot scanning, dual X-ray absorptiometry and gait analysis methods were used to determine structural parameters of the foot and assess their relation to knee joint loading and biomechanical response to wedged insoles in 30 patients with knee osteoarthritis. In multiple linear regression models, foot fat content, height of the medial longitudinal arch and static hind foot angle were not associated with the magnitude of the knee adduction moment (R² = 0.24, p = 0.060), knee adduction angular impulse (R² = 0.21, p = 0.099) or 3D resultant knee moment (R² = 0.23, p = 0.073) during gait. Furthermore, these foot structure parameters were not associated with the patients’ biomechanical response to medial or lateral wedge footwear insoles (all p < 0.01). These findings suggest that static foot structure is not associated with gait mechanics at the knee, and that static foot structure alone cannot be utilized to predict an individual’s biomechanical response to wedged footwear insoles in patients with knee osteoarthritis.     

手足温针灸联合步行阶梯训练对老年糖尿病周围神经病变患者步态异常、血流动力学和感觉及运动神经传导的影响

摘要 目的：观察手足温针灸联合步行阶梯训练对老年糖尿病周围神经病变（DPN）患者步态异常、血流动力学和感觉及运动神经传导的影响。方法：按照随机数字表法将上海市第六人民医院2020年3月~2022年1月期间收治的119例老年DPN患者分为对照组（n=59,步行阶梯训练）和研究组（n=60,手足温针灸联合步行阶梯训练）。对比两组疗效、步态异常、血流动力学、临床症状改善情况和感觉及运动神经传导变化情况。结果：研究组91.67%的临床总有效率高于对照组72.88%（P<0.05）。研究组干预后的密歇根糖尿病神经病变评分（MDNS）和多伦多临床评分系统（TCSS）评分低于对照组（P<0.05）。研究组干预后的腓总神经及胫神经的感觉神经传导速度（SNCV）、运动神经传导速度（MNCV）高于对照组（P<0.05）。研究组干预后的全血黏度、血浆比黏度、纤维蛋白原低于对照组（P<0.05）。研究组足底压力中心轨迹（COP）曲线异常、全足平衡性曲线异常、全足压力变化曲线异常例数少于对照组（P<0.05）。结论：手足温针灸联合步行阶梯训练可促进老年DPN患者步态异常、血流动力学和感觉及运动神经传导恢复,疗效较好。     

Forward dynamic simulation of bipedal walking in the Japanese macaque: investigation of causal relationships among limb kinematics, speed, and energetics of bipedal locomotion in a nonhuman primate

Japanese macaques that have been trained for monkey performances exhibit a remarkable ability to walk bipedally. In this study, we dynamically reconstructed bipedal walking of the Japanese macaque to investigate causal relationships among limb kinematics, speed, and energetics, with a view to understanding the mechanisms underlying the evolution of human bipedalism. We constructed a two-dimensional macaque musculoskeletal model consisting of nine rigid links and eight principal muscles. To generate locomotion, we used a trajectory-tracking control law, the reference trajectories of which were obtained experimentally. Using this framework, we evaluated the effects of changes in cycle duration and gait kinematics on locomotor efficiency. The energetic cost of locomotion was estimated based on the calculation of mechanical energy generated by muscles. Our results demonstrated that the mass-specific metabolic cost of transport decreased as speed increased in bipedal walking of the Japanese macaque. Furthermore, the cost of transport in bipedal walking was reduced when vertical displacement of the hip joint was virtually modified in the simulation to be more humanlike. Human vertical fluctuations in the body's center of mass actually contributed to energy savings via an inverted pendulum mechanism.     

Ankle and foot power in gait analysis: Implications for science,technology and clinical assessment

In human gait analysis studies, the entire foot is typically modeled as a single rigid-body segment; however, this neglects power generated/absorbed within the foot. Here we show how treating the entire foot as a rigid body can lead to misunderstandings related to (biological and prosthetic) foot function, and distort our understanding of ankle and muscle-tendon dynamics. We overview various (unconventional) inverse dynamics methods for estimating foot power, partitioning ankle vs. foot contributions, and computing combined anklefoot power. We present two case study examples. The first exemplifies how modeling the foot as a single rigid-body segment causes us to overestimate (and overvalue) muscle-tendon power generated about the biological ankle (in this study by up to 77%), and to misestimate (and misinform on) foot contributions; corroborating findings from previous multi-segment foot modeling studies. The second case study involved an individual with transtibial amputation walking on 8 different prosthetic feet. The results exemplify how assuming a rigid foot can skew comparisons between biological and prosthetic limbs, and lead to incorrect conclusions when comparing different prostheses/interventions. Based on analytical derivations, empirical findings and prior literature we recommend against computing conventional ankle power (between shank-foot). Instead, we recommend using an alternative estimate of power generated about the ankle joint complex (between shank-calcaneus) in conjunction with an estimate of foot power (between calcaneus-ground); or using a combined anklefoot power calculation. We conclude that treating the entire foot as a rigid-body segment is often inappropriate and ill-advised. Including foot power in biomechanical gait analysis is necessary to enhance scientific conclusions, clinical evaluations and technology development.