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.

Variation of thoracolumbar vertebral morphology in anthropoid primates.

OBJECTIVES: Morphological variation among extant primates in the lumbar vertebral column is well studied. However, knowledge concerning the thoracic spine, an important region responsible for supporting and facilitating movement in the upper trunk, remains relatively scarce. Consequently, our comprehension of the functional differentiation exhibited throughout the thoracolumbar vertebral column among various primate species remains constrained. In this study, we examined patterns of morphological variation in the thoracolumbar vertebral column of extant hominoids, cercopithecoids, and Ateles. MATERIALS AND METHODS: We collected external shape data on 606 thoracic and lumbar vertebrae from Homo sapiens, Pan troglodytes, Hylobates lar, Macaca fuscata, Chlorocebus aethiops, Colobus guereza, Ateles geoffroyi, and A. belzebuth. Forty-four landmarks were obtained on the three-dimensional surface. Geometric morphometrics was used to quantify the centroid size and variation of the shapes of thoracic and lumbar vertebrae. RESULTS: Cercopithecoids exhibited greater variation in the size and shape of their thoracic and lumbar vertebrae compared to hominoids and Ateles. Although many vertebral features contributed to the observed variation throughout the thoracolumbar vertebral column within the taxon, the transverse and spinous processes exhibited relatively major contributions. DISCUSSION: Our results suggest that quadrupedal locomotion requires the functional differentiation between thoracic and lumbar vertebrae, and for hominoids, functional adaptation to orthograde posture necessitates a relatively more uniform shape of thoracic and lumbar vertebrae.

Range of rotation of thoracolumbar vertebrae in Japanese macaques.

In humans, the range of thoracic vertebral rotation is known to be greater than that of the lumbar vertebrae due to their zygapophyseal orientation and soft tissue structure. However, little is known regarding vertebral movements in non-human primate species, which are primarily quadrupedal walkers. To understand the evolutionary background of human vertebral movements, this study estimated the range of axial rotation of the thoracolumbar spine in macaque monkeys. First, computed tomography (CT) was performed while passively rotating the trunk of whole-body cadavers of Japanese macaques, after which the motion of each thoracolumbar vertebra was estimated. Second, to evaluate the influence of the shoulder girdle and surrounding soft tissues, specimens with only bones and ligaments were prepared, after which the rotation of each vertebra was estimated using an optical motion tracking system. In both conditions, the three-dimensional coordinates of each vertebra were digitized, and the axial rotational angles between adjacent vertebrae were calculated. In the whole-body condition, the lower thoracic vertebrae had a greater range of rotation than did the other regions, similar to that observed in humans. In addition, absolute values for the range of rotation were similar between humans and macaques. However, in the bone-ligament preparation condition, the upper thoracic vertebrae had a range of rotation similar to that of the lower thoracic vertebrae. Contrary to previous speculations, our results showed that the mechanical restrictions by the ribs were not as significant; rather, the shoulder girdle largely restricted the rotation of the upper thoracic vertebrae, at least, in macaques.

Testing the reliability of the rearticulation of osteological primate pelves in comparative morphological studies.

The evolution of human pelvic form is primarily studied using disarticulated osteological material of living and fossil primates that need rearticulation to approximate anatomical position. To test whether this technique introduces errors that impact biological signals, virtual rearticulations of the pelvis in anatomical position from computed tomography scans were compared with rearticulated models from the same individuals for one female and one male of Homo sapiens, Pan troglodytes, Macaca mulatta, Lepilemur mustelinus, Galago senegalensis, and Nycticebus pygmaeus. "Cadaveric" pelvic bones were first analyzed in anatomical position, then the three bones were segmented individually, intentionally scattered, and "rearticulated" to test for rearticulation error. Three-dimensional landmarks and linear measurements were used to characterize the overall pelvis shape. Cadaveric and rearticulated pelves were not identical, but inter-specific and intra-specific shape differences were higher than the landmarking error in the cadaveric individuals and the landmarking/rearticulation error in the rearticulated pelves, demonstrating that the biological signal is stronger than the noise introduced by landmarking and rearticulation. The rearticulation process, however, underestimates the medio-lateral pelvic measurements in species with a substantial pubic gap (e.g., G. senegalensis, N. pygmaeus) possibly because the greater contribution of soft tissue to the pelvic girdle introduces higher uncertainty during rearticulation. Nevertheless, this discrepancy affects only the caudal-most part of the pelvis. This study demonstrates that the rearticulation of pelvic bones does not substantially affect the biological signal in comparative 3D morphological studies but suggests that anatomically connected pelves of species with wide pubic gaps should be preferentially included in these studies.

Diagonal-couplet gaits on discontinuous supports in Japanese macaques and implications for the adaptive significance of the diagonal-sequence, diagonal-couplet gait of primates.

OBJECTIVES: Diagonal-sequence, diagonal-couplet (DSDC) gaits have been proposed as an adaptation to travel on discontinuously arranged arboreal branches. Only a few studies have examined primate gait adjustment to support discontinuity. We analyzed the gaits of Japanese macaques walking on the "ground" and two discontinuous conditions, "circle" and "point," to better understand the advantages of DSDC gaits on discontinuous supports. MATERIALS AND METHODS: Seventy-eight vertical posts, each with a circular upper surface, were arranged in four rows at a spacing of 200 mm. The diameter of the circular upper surface was 150 mm ("circle condition") or 50 mm ("point condition"). We calculated the limb phase, duty factor, and time interval from hindlimb touchdown to ipsilateral forelimb liftoff. The supports the fore- and hindlimbs landed on during walking were identified in the circle and point condition. RESULTS: The macaques predominantly used DSDC gaits in the ground and circle conditions and lateral-sequence, diagonal-couplet (LSDC) gaits in the point condition. The macaques usually placed their hindlimbs on the same supports as their ipsilateral forelimbs during the gait cycle. DISCUSSION: Japanese macaques overlapped the ipsilateral fore- and hindlimb stance phase in all DSDC and some LSDC gaits to proximate the ipsilateral limbs on the discontinuous support, allowing the forelimb to guide the hindlimb placement to the support. The overlap duration of the ipsilateral limb stance phases may be extended by DSDC gaits longer than by LSDC gaits, allowing for a direct pass of the support being held by the prehensile hand to the prehensile foot.

Muscle-tendon arrangement and intramuscular nerve distribution of flexor digitorum superficialis in the siamang (Symphalangus syndactylus), western lowland gorilla (Gorilla gorilla gorilla), western chimpanzee (Pan troglodytes verus), and Japanese macaque (Macaca fuscata).

Flexor digitorum superficialis (FDS) shows diverse muscle-tendon arrangements among primates. The intramuscular nerve distribution pattern is a criterion for discussing the homology of FDS. In this study, the muscle-tendon arrangement and intramuscular nerve distribution of FDS were examined in the siamang, western lowland gorilla, western chimpanzee, and Japanese macaques. The FDS had muscle bellies to digits II-V. FDS had proximal belly and intermediate tendon except for siamang. Distal belly to digit II (in the western lowland gorilla and western chimpanzees) or distal bellies to digits II and V (in Japanese macaque) originated from the intermediate tendon. In all specimens, nerve branches within digit III belly extended into digit IV belly, and nerve branch(es) within digit IV belly extended into digit V belly. This consistent pattern suggested that each muscle belly to digits III-V is interspecifically homologous. The digit II belly in the siamang and the distal belly to digit II in the western lowland gorilla, western chimpanzees, and Japanese macaques could be homologous based on their similar innervating patterns. The proximal belly was innervated by branches from the communicating nerve between median and ulnar nerves in the western lowland gorilla or branches from median and ulnar nerves in western chimpanzees. In the siamang and Japanese macaque, the whole FDS was innervated by median nerve. The proximal belly in the western lowland gorilla, western chimpanzees, and Japanese macaques could be classified into different groups from the other part of the FDS.

Morphological significance of the medial brachial cutaneous nerve: An anatomical study of the brachial plexus in primates.

The medial brachial cutaneous nerve (MBC) originates from the medial cord of the brachial plexus and innervates the skin sensory in the medial posterior surface of the upper arm. Considering previous reports of the primate brachial plexus, the MBC appeared to be the sole branch in the brachial plexus that only some primates possess. However, the detailed descriptions and records regarding the morphology of the MBC and related nerves, their origins and distributions (dermatomes) in particular, were frequently lacked in the previous reports, and it remains unclear why the difference in the MBC appearance exists among primates. In this study, the brachial plexus and its branches were first re-evaluated and certainly identified in several primates, humans, chimpanzee, macaque monkey, lutung, tamarin, squirrel monkey, and spider monkey. The MBC was identified in humans, chimpanzee, spider monkey, and squirrel monkey. In the other species, the intercostobrachial nerve (ICB) originating from some of 1st to 3rd intercostal nerves developed and distributed instead of the MBC. According to the kinesiological and behavioral studies, the former species possessing MBC show high shoulder joint mobility associated with their locomotive patterns. We speculate that the MBC corresponds to transformed ICB; specifically, where it originates presumably transfers from the 1st and/or 2nd intercostal nerves to the brachial plexus, which allows it to reach the upper arm by coursing the shortest distance even if the forelimb is raised high. Therefore, MBC may embody phylogenetic morphogenesis of the nerve associated with the locomotive evolution and adaptation in primate forelimb.

Comparison of the soleus and plantaris muscles in humans and other primates: Macroscopic neuromuscular anatomy and evolutionary significance.

In humans, the soleus is more developed compared to other primates and has a unique architecture composed of anterior bipennate and posterior unipennate parts, which are innervated by different nerve branches. The anterior part of the human soleus was proposed to be important for bipedalism, however, the phylogenetic process resulting in its acquisition remains unclear. Providing insights into this process, the anterior part of the soleus was suggested to be closely related to the plantaris based on the branching pattern of their nerve fascicles. To reveal the phylogeny of the soleus and plantaris in primates, the innervation patterns of the posterior crural muscles were compared among a wide range of species. From their branching pattern, posterior crural muscles could be classified into superficial and deep muscle groups. The anterior part of the soleus and plantaris both belonged to the deep muscle group. In all the examined specimens of ring-tailed lemurs and chimpanzees, as well as in one out of two specimens of siamang, the nerve branches corresponding to those innervating the anterior part of the human soleus were found. The muscular branches innervating the anterior part of the soleus and plantaris formed a common trunk or were connected in all the specimens. These results indicate that the anterior part of the soleus is closely related to the plantaris across different species of primates. In turn, this suggests that the anterior part of the soleus is maintained among primates, and especially in humans, where it develops as the characteristic bipennate structure.

Relationship between the lumbosacral plexus deviation and 12th rib length in Japanese macaques (Macaca fuscata).

The relationship between the lumbosacral plexus (LSP) origin and the 12th rib length was recently determined in humans; cranial and caudal deviations of the plexus origin are related to shortening and elongation of the 12th rib, respectively. However, it remains unclear whether such anatomical correlations are also observed in non-human mammals. To address this issue, in the present study, we evaluated the LSP origin and the 12th rib length in Japanese macaques (Macaca fuscata). In typical cases, the femoral and obturator nerves were derived from both the 4th and 5th lumbar nerves, and the lumbosacral trunk was from the 5th to 7th lumbar nerves. Some of the LSPs exhibited a caudal deviation of their origins; the femoral and obturator nerves were also derived from the 6th lumbar nerve, in addition to the 4th and 5th lumbar nerves; the lumbosacral trunk lost the 5th lumbar nerve origin and arose from the 6th and 7th lumbar nerves. Individuals with the caudal deviation of LSP origin exhibited significant elongation of the 12th ribs, in comparison with individuals with the typical plexus. The present findings indicate that the caudal deviation of LSP origin was correlated to the 12th rib elongation in Japanese macaques, similar to humans. As a future studies, we need to clarify which mammalian groups exhibit such correlation between the deviation of the LSP origin and the lowest rib length, and further to provide evolutionary implications of this correlation.

Hip medial rotator action of gluteus medius in Japanese macaque (Macaca fuscata) and implications to adaptive significance for quadrupedal walking in primates.

The gluteus medius (GM) muscle in quadrupedal primates has long been thought to mainly act as a hip extensor. However, previous reports argue that it may be a prime hip medial rotator and functions to rotate the pelvis in the horizontal plane, suggesting the functional differentiation between the GM and other hip extensors as hamstrings. In this study, we aim to quantify the muscle actions of the GM and hamstrings using muscle moment arm lengths and discuss the functional differentiation among hip extensors. Muscle attachment sites of eight specimens of Japanese macaque (Macaca fuscata) were digitized, and musculoskeletal models were constructed. Flexor-extensor, abductor-adductor, and medial-lateral rotator moment arms were calculated as the models were moved following the experimentally acquired kinematic data during walking on a pole substrate. Using electromyography, we also recorded the pattern of muscle activation. The GM showed a larger medial rotator moment arm length than the extensor moment arm length when it was activated, suggesting this muscle acts mainly as a hip medial rotator rather than as a hip extensor. The medial rotator action of the GM in the early support phase may rotate the pelvis in the horizontal plane and function to help contralateral forelimb reaching as a previous study suggested and facilitate contralateral hindlimb swinging to place the foot near the ipsilateral forelimb's hand.

Anatomical study of the incisivus labii superioris and inferioris muscles in non-human primates.

The facial muscles have significant roles for vocalization, feeding, and facial expression in both human and non-human primates. Of these, the anatomy of the incisivus labii superioris (ILS) and incisivus labii inferioris (ILI), which are considered as the accessory bundle of the orbicularis oris (OO) in humans, has rarely been documented in the literature. Our current understanding of the function of the ILS and ILI is that they probably retract the upper and lower lips. Also, there is no account of these muscles in non-human primates in the current literature. The aim of this study was to reveal the ILS and ILI in non-human primates. Five Macaca fascicularis, one Macaca fuscata, one Macaca fuscata yakui, and one Pan troglodytes were dissected. Seven formalin-fixed cadavers and one fresh cadaver were included. Both the ILS and ILI were observed in all specimens. The ILS originated from the incisive fossa of the maxilla and inserted into the OO. The mentalis (MT) and ILI arose from the incisive fossa of the mandible and inserted into the OO and the skin of the chin area. The MT and ILI in the P. troglodytes examined were thicker than in the other three non-human species, and the ILS and ILI in the three macaques were similar in shape to those of humans. The difference of these muscles may result in different functions of the lip such as during vocalization, feeding, and facial expression.

A comparison of axial trunk rotation during bipedal walking between humans and Japanese macaques.

OBJECTIVES: Human walking involves out-of-phase axial rotations of the thorax and pelvis. It has long been believed that this rotational capability is a distinctive feature of the genus Homo. However, Thompson et al. (2015) showed that chimpanzees also counter-rotate their thorax relative to the pelvis during bipedal walking, which raised questions regarding the origins and development of this characteristic. In this study, we measured the axial rotation of the trunk during bipedal walking in humans and macaques to investigate if intra-trunk axial rotations are observed in non-hominoid primate species. MATERIALS AND METHODS: We collected three-dimensional trunk kinematic data during bipedal walking in six humans and five Japanese macaques. The human subjects walked on a treadmill, and the animal subjects walked on a 5-m runway. During walking, the positions of cluster markers, which defined trunk segments, were recorded by multiple video cameras. Segmental xyz coordinates were digitized, and transverse rotations were calculated using motion analysis software. RESULTS: Although trunk rotations in the global coordinate system were greater in macaques than in humans, the intra-trunk rotation and range of motion showed a similar pattern in the two species. CONCLUSIONS: Thoracic rotation relative to the pelvis during bipedal walking is not unique to the hominid lineage but rather a characteristic generated by the mechanical requirements of bipedal walking. The fact that the range of motion of counter rotation is similar in these species infers that an optimal range of rotation exists for bipedal walking.

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.

Muscle-tendon arrangement and innervation pattern of the m. flexor digitorum superficialis in the common marmoset (Callithrix jacchus), squirrel monkey (Saimiri sciureus) and spider monkey (Ateles sp.).

The muscle-tendon arrangement of the m. flexor digitorum superficialis (FDS) varies among different primate groups. Recent developmental investigations revealed that the primordium of FDS emerges in the hand region first and relocates to the forearm later. The relationship between the diverse muscle-tendon arrangement and the characteristic developmental process of FDS is important for understanding the evolutionary changes of the FDS. Moreover, the innervation pattern cannot go unremarked when discussing the muscle homology and evolution. We examined the muscle-tendon arrangement and intramuscular nerve distribution of the FDS in three genera of Platyrrhini: three common marmosets (Callithrix jacchus), two squirrel monkeys (Saimiri sciureus) and two spider monkeys (Ateles sp.). We observed that the FDS consisted of multiple muscle bellies. The origin of the muscle bellies to digits II and V varied, whereas muscle bellies to digits III and IV consistently originated from the medial epicondyle. The muscle-tendon arrangement of the FDS differed among the three genera owing to the different origins of muscle bellies to digits II and V. In all the examined specimens, the muscle bellies to digits II and/or III were innervated by the direct nerve branches from the median nerve. However, the muscle bellies to digits IV and V never received direct nerve branches from the median nerve. Nerve branches within the belly to digit III extended into the belly to digit IV, and one nerve branch within the belly to digit IV extended into the belly to digit V. These consistent nerve distribution patterns suggest that different patterns of FDS muscle-tendon arrangement have changed from that of a common ancestral condition. It is plausible that the diverse origins of muscle bellies in the FDS are attributable to the difference in the destination for the relocation of the muscle bellies during developmental processes.

Age-related changes in the cranial thickness of Japanese macaques ( Macaca fuscata ) / Cambios relacionados con la edad en el grosor craneal de los macacos japoneses ( Macaca fuscata )

Craniometry has revealed that continuous skull expansion occurs after dental maturity in macaques and other nonhuman primates. Endocranial volume has been shown to increase with age from mid-adulthood to older age in macaques. Thus, neurocranial thickness may decrease with age, especially from mid-adulthood to older age. Here, we investigated age-related changes in the cranial thickness of Japanese macaques (Macaca fuscata). Ten cranial thickness measurements (ten neurocranial landmarks) were made using computed tomographic scans of 140 crania from adult macaques (67 males and 73 females). The cranial thickness at many sites was shown to increase in the neurocranium from young adulthood (7-9 years) to early-mid adulthood (14-19 years) in males and latemid adulthood (19-24 years) in females, while it was decreased in the oldest age group (>24 years). The cranial thickness at various sites showed a significant decrease from mid-adulthood to very old age in both sexes, although females had more sites with decreasing thickness than did males. The difference between sexes in terms of age-related changes in cranial thickness at sites on the mid-sagittal plane may be associated with the differences in the size of the projecting face and canines between males and females. The greater number of sites with decreasing thickness in females than in males may be associated with postmenopausal estrogen depletion in female macaques.

La craneometría ha revelado que la expansión continua del cráneo se produce después de la madurez dental en macacos y otros primates no humanos. Se ha demostrado que el volumen endocraneal aumenta con la edad desde mediados de la edad adulta hasta la edad más avanzada en macacos. Por lo tanto, el grosor neurocraneal puede disminuir con la edad, especialmente desde la edad adulta media hasta la edad avanzada. Aquí, investigamos los cambios relacionados con la edad en el grosor craneal de los macacos Japoneses (Macaca fuscata). Se realizaron diez mediciones del grosor craneal (considerando diez puntos de referencia neurocraneales) mediante tomografías computarizadas de 140 cráneos de macacos adultos (67 machos y 73 hembras). Se observó que el grosor craneal en muchos sitios aumentó en el neurocráneo desde la edad adulta joven (7-9 años) hasta la edad adulta media (14-19 años) en los hombres y en la edad adulta media tardía (19-24 años) en las mujeres, mientras que se redujo en el grupo de mayor edad (> 24 años). El grosor craneal en varios sitios mostró una disminución significativa desde la edad adulta media hasta la edad muy avanzada en ambos sexos, aunque las hembras tenían más sitios con grosor decreciente. La diferencia entre sexos, en términos de cambios relacionados con la edad, en el grosor craneal en los sitios en el plano mediano puede asociarse con las diferencias en el tamaño de la cara y en los caninos entre machos y hembras. El mayor número de sitios con grosor decreciente en las hembras respecto a los machos puede estar asociado con el agotamiento de los estrógenos posmenopáusicos en los macacos hembras.

Locomotor Kinematics of Two Semi-Wild Macaque Species (Macaca assamensis and Macaca arctoides) in Thailand.

This project aimed to investigate primate locomotor kinematics noninvasively in the wild. Semi-wild Assamese and stump-tailed macaques were selected for the study, which was performed in Thailand. We investigated their locomotor kinematics and its relationship to habitat use. The macaques' positional behavior was recorded with two video cameras, and kinematic parameters were estimated during terrestrial quadrupedal locomotion, using the markerless method. The data analyzed so far revealed that stump-tailed macaques walk with longer, less frequent strides than Assamese macaques. Although stump-tailed macaques present a smaller angular excursion of the shoulder joint than Assamese macaques, they exhibited a relatively large shoulder girdle motion and anteroposterior translation of the shoulder, which increased their stride length. Additionally, stump-tailed macaques exhibited a digitigrade gait and elbow extension, suggesting a good adaptation to terrestrial locomotion. Assamese macaques, on the other hand, exhibited a gait that did not seem optimized for terrestrial locomotion, using the hands in a palmigrade posture and frequently flexing the fingers at varying degrees. The kinematic characteristics of the two species studied is consistent with previous field observations reporting that Assamese macaques are highly arboreal, whereas stump-tailed macaques are more terrestrial.

Muscle Spindle Density of Lateral Rotators of the Thigh in Japanese Macaques and a Gibbon.

We examined the six small lateral rotators of the hip joint, which is one of the most flexible joints and allows kinematically complex motions of the hindlimb, to elucidate the functional differentiation among these muscles and to test the hypothesis that species-specific characteristics in hindlimb use during locomotion are reflected in the muscle spindle density and in other parameters of the deep small hip joint rotators. For these purposes, we estimated the number of muscle spindles of the superior gemellus muscle (SG), inferior gemellus muscle, quadratus femoris muscle, obturator internus muscle (OI), obturator externus muscle, and piriformis muscle in three Japanese macaques and a gibbon, using 30-µm-thick serial sections throughout each muscle length after azan staining. The numbers of muscle spindles per 10,000 muscle fibers were determined to compare inter-muscle variation. The spindle density was highest in the SG and lowest in the OI in the Japanese macaques, suggesting that the SG, which is attached to the tendon of the OI, functions as a kinesiological monitor of the OI. On the other hand, SG the was missing in the gibbon, and the OI in the gibbon contained more spindles than that in the Japanese macaques. This suggests that the SG and the OI fused into one muscle in the gibbon. We postulate that the relative importance of the deep small hip rotator muscles differs between the Japanese macaques and gibbon and that the gibbon's muscles are less differentiated in terms of the spindle density, probably because this brachiating species uses its hindlimbs less frequently.

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.