Back muscle function during bipedal walking in chimpanzee and gibbon: implications for the evolution of human locomotion

The evolution of erect posture and locomotion continues to be a major focus of interest among paleoanthropologists and functional morphologists. To date, virtually all of our knowledge about the functional role of the back muscles in the evolution of bipedalism is based on human experimental data. In order to broaden our evolutionary perspective on the vertebral region, we have undertaken an electromyographic (EMG) analysis of three deep back muscles (multifidus, longissimus thoracis, iliocostalis lumborum) in the chimpanzee (Pan troglodytes) and gibbon (Hylobates lar) during bipedal walking. The recruitment patterns of these three muscles seen in the chimpanzee closely parallel those observed in the gibbon. The activity patterns of multifidus and longissimus are more similar to each other than either is to iliocostalis. Iliocostalis recruitment is clearly related to contact by the contralateral limb during bipedal walking in both species. It is suggested that in both the chimpanzee and gibbon, multifidus controls trunk movement primarily in the sagittal plane, iliocostalis responds to and adjusts movement in the frontal plane, while longissimus contributes to both of these functions. In many respects, the activity patterns shared by the chimpanzee and gibbon are quite consistent with recent human experimental data. This suggests a basic similarity in the mechanical constraints placed on the back during bipedalism among these three hominoids. Thus, the acquisition of habitual bipedalism in humans probably involved not so much a major change in back muscle action or function, but rather an improvement in the mechanical advantages and architecture of these muscles.     

Stresses on the limbs of quadrupedal primates

Data is presented from eight primates on the ground reaction forces on the limbs during locomotion. These subjects supported from 30 to 45% of their body weight on their forelimbs. Other quadrupedal mammals support 55-60% of their body weight on their forelimbs. The increase of peak vertical force with speed varies greatly between the subjects. The variation in weight supported by the forelimbs and the peak forces on the forelimbs is proposed to correlate with variation in locomotor adaptations. It is suggested that the occurrence of bipedalism in primates represents the extreme expression of the tendency in primates to reduce the compressive forces on their forelimbs.     

Neural control of quadrupedal and bipedal stance: implications for the evolution of erect posture

The transition among hominids from quadrupedalism to bipedalism resulted in modifications in their musculoskeletal morphology. It is unclear, however, whether changes in the circuitry of the CNS were also necessary in order to accommodate the unique balance requirements of two-limb support. This study addresses the issue of modifications in control strategies by investigating the rapid, automatic postural responses of feline and human subjects to sudden disturbances of balance in the anteroposterior (AP) direction while they stand quadrupedally and bipedally on movable platforms. Postural responses are characterized in terms of segmental adjustments, generated AP shear forces, and electromyographic activity. Feline and human subjects correct posture similarly when standing quadrupedally. Furthermore, both species correct stance primarily with their hindlimbs and use their forelimbs as supportive struts. In contrast, both species use completely different correctional strategies when standing bipedally. Morphological restrictions, however, prevent cats from adopting the pillar-like plantigrade posture of human beings. Thus, the correctional strategies of bipedal cats are distinct from those of bipedal human subjects. It is concluded that 1) automatic postural response patterns of quadrupedal Felis and bipedal Homo reflect the different biomechanical characteristics of the initial postures rather than species differences in CNS circuitry controlling stance; 2) hindlimb-dominated posture control is probably a common and relatively ancient pattern; and 3) reorganization of hominid CNS circuitry was probably unnecessary because hindlimb control was already a feature of the system.     

Mechanics of increased support of weight by the hindlimbs in primates

Quadrupedal primates support most of their weight on their hindlimbs during locomotion. Neither the position of their center of gravity nor the average position of their foot contacts is substantially different from that of other quadrupeds supporting most of their weight on their forelimbs. Arguments are presented to support the theory that high levels of hindlimb retractor activity will produce this shift of support to the hindlimbs. If this muscular activity is appropriately timed, it will generate only low horizontal accelerations, which can be offset by small changes in the average position of the limbs. Estimates of muscular force are derived from force plate and kinematic data, which indicate that primates in fact do exhibit the postulated pattern of muscular activity. It is suggested that this shift occurs to reduce the compressive forces on the forelimbs.     

Further evidence for the role of supraspinatus in quadrupedal monkeys.

Differences in the degree of projection of the greater tubercle above the level of the humeral head in primate proximal humeri have been associated with differing leverage requirements for supraspinatus during arboreal vs. terrestrial quadrupedal locomotion. Since most workers have assumed that supraspinatus acts as a humeral protractor, interpretations of the variation in greater tubercle height have focused on the need for powerful vs. rapid humeral protraction during the swing phase of quadrupedal locomotion. However, in an EMG study on the activity patterns of supraspinatus in the vervet monkey, Larson and Stern (Am. J. Phys. Anthropol. 79:369-377, 1989) reported that although supraspinatus is active during arm elevations against gravity, it is silent during the swing phase of quadrupedal locomotion, and instead acts as a joint stabilizer during support phase. They suggested that the pattern of activity for supraspinatus observed in the vervet was common for all quadrupedal primates, and that differences in greater tubercle projection could be related to the degree of mobility of the shoulder. In the current study, we present additional EMG data on a baboon and three macaques supporting the suggestions offered by Larson and Stern (1989).     

Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates

The forelimb joints of terrestrial primate quadrupeds appear better able to resist mediolateral (ML) shear forces than those of arboreal quadrupedal monkeys. These differences in forelimb morphology have been used extensively to infer locomotor behavior in extinct primate quadrupeds. However, the nature of ML substrate reaction forces (SRF) during arboreal and terrestrial quadrupedalism in primates is not known. This study documents ML-SRF magnitude and orientation and forelimb joint angles in six quadrupedal anthropoid species walking across a force platform attached to terrestrial (wooden runway) and arboreal supports (raised horizontal poles). On the ground all subjects applied a lateral force in more than 50% of the steps collected. On horizontal poles, in contrast, all subjects applied a medially directed force to the substrate in more than 75% of the steps collected. In addition, all subjects on arboreal supports combined a lower magnitude peak ML-SRF with a change in the timing of the ML-SRF peak force. As a result, during quadrupedalism on the poles the overall SRF resultant was relatively lower than it was on the runway. Most subjects in this study adduct their humerus while on the poles. The kinetic and kinematic variables combine to minimize the tendency to collapse or translate forelimbs joints in an ML plane in primarily arboreal quadrupedal primates compared to primarily terrestrial quadrupedal ones. These data allow for a more complete understanding of the anatomy of the forelimb in terrestrial vs. arboreal quadrupedal primates. A better understanding of the mechanical basis of morphological differences allows greater confidence in inferences concerning the locomotion of extinct primate quadrupeds.     

The relationship between flexibility and EMG activity pattern of the erector spinae muscles during trunk flexion–extension

BackgroundMovements in the lumbar spine, including flexion and extension are governed by a complex neuromuscular system involving both active and passive units. Several biomechanical and clinical studies have shown the myoelectric activity reduction of the lumbar extensor muscles (flexion–relaxation phenomenon) during lumbar flexion from the upright standing posture. The relationship between flexibility and EMG activity pattern of the erector spinae during dynamic trunk flexion–extension task has not yet been completely discovered.ObjectiveThe purpose of this study was to investigate the relationship between general and lumbar spine flexibility and EMG activity pattern of the erector spinae during the trunk flexion–extension task.MethodsThirty healthy female college students were recruited in this study. General and lumbar spine flexibilities were measured by toe-touch and modified schober tests, respectively. During trunk flexion–extension, the surface electromyography (EMG) from the lumbar erector spinae muscles as well as flexion angles of the trunk, hip, lumbar spine and lumbar curvature were simultaneously recorded using a digital camera. The angle at which muscle activity diminished during flexion and initiated during extension was determined and subjected to linear regression analysis to detect the relationship between flexibility and EMG activity pattern of the erector spinae during trunk flexion–extension.ResultsDuring flexion, the erector spinae muscles in individuals with higher toe-touch scores were relaxed in larger trunk and hip angles and reactivated earlier during extension according to these angles (P < 0.001) while in individuals with higher modified schober scores this muscle group was relaxed later and reactivated sooner in accordance with lumbar angle and curvature (P < 0.05). Toe-touch test were significantly correlated with trunk and hip angles while modified schober test showed a significant correlation with lumbar angle and curvature variables.ConclusionThe findings of this study indicate that flexibility plays an important role in trunk muscular recruitment pattern and the strategy of the CNS to provide stability. The results reinforce the possible role of flexibility alterations as a contributing factor to the motor control impairments. This study also shows that flexibility changes behavior is not unique among different regions of the body.     

Ground-reaction-force profiles of bipedal walking in bipedally trained Japanese monkeys

Ground-reaction-force (GRF) profiles of bipedal locomotion in bipedally trained Japanese macaques (performing monkeys) were analyzed in order to clarify the dynamic characteristics of their locomotion. Five trained and two ordinary monkeys participated in the experiment. They walked on a wooden walkway at a self-selected speed, and three components of the GRF vector were measured using a force platform. Our measurements reveal that trained monkeys exhibited vertical-GRF profiles that were single-peaked, similar to those of ordinary monkeys; they did not generate the double-peaked force curve that is seen in humans, despite their extensive training. However, in the trained monkeys, the peak appeared relatively earlier in the stance phase, and overall shape was more triangular than that of the more parabolic profile generated by ordinary monkeys. Comparisons of vertical fluctuation of the center of body mass calculated from the measured profiles suggest that this was larger in the trained monkeys, indicating that storage and release of potential energy actually took place in their bipedal walking. This energetic advantage seems limited, however, because efficient exchange of potential and kinetic energy during walking were not completely out of phase as in human walking. We suggest that anatomically restricted range of hip-joint motion impedes the inherently quadrupedal monkeys from generating humanlike bipedal locomotion, and that morphological rearrangement of the hip joint was an essential precondition for protohominids to acquire humanlike bipedalism.     

Spatio-temporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus)

Spatio-temporal gait characteristics (step and stride length, stride frequency, duty factor) were determined for the hind-limb cycles of nine bonobos (Pan paniscus) walking quadrupedally and bipedally at a range of speeds. The data were recalculated to dimensionless quantities according to the principle of dynamic similarity. Lower leg length was used as the reference length. Interindividual variability in speed modulation strategy of bonobos appears to be low. Compared to quadrupedal walking, bipedal bonobos use smaller steps to attain a given speed (differences increase with speed), resulting in shorter strides at a higher frequency. In the context of the ("hybrid") dynamic pattern approach to locomotion (Latach, 1998) we argue that, despite these absolute differences, intended walking speed is the basic control variable which elicits both quadrupedal and bipedal walking kinematics in a similar way. Differences in the initial status of the dynamic system may be responsible for the differences in step length between both gaits. Comparison with data deduced from the literature shows that the effects of walking speed on stride length and frequency are similar in bonobos, common chimpanzees, and humans. This suggests that (at least) within extant homininae, spatio-temporal gait characteristics are highly comparable, and this in spite of obvious differences in mass distribution and bipedal posture.     

Validity of trunk extensor and flexor torque measurements using isokinetic dynamometry

This study aimed to evaluate the validity and test–retest reliability of trunk muscle strength testing performed with a latest-generation isokinetic dynamometer. Eccentric, isometric, and concentric peak torque of the trunk flexor and extensor muscles was measured in 15 healthy subjects. Muscle cross sectional area (CSA) and surface electromyographic (EMG) activity were respectively correlated to peak torque and submaximal isometric torque for erector spinae and rectus abdominis muscles. Reliability of peak torque measurements was determined during test and retest sessions. Significant correlations were consistently observed between muscle CSA and peak torque for all contraction types (r = 0.74−0.85; P < 0.001) and between EMG activity and submaximal isometric torque (r ⩾ 0.99; P < 0.05), for both extensor and flexor muscles. Intraclass correlation coefficients were comprised between 0.87 and 0.95, and standard errors of measurement were lower than 9% for all contraction modes. The mean difference in peak torque between test and retest ranged from −3.7% to 3.7% with no significant mean directional bias. Overall, our findings establish the validity of torque measurements using the tested trunk module. Also considering the excellent test–retest reliability of peak torque measurements, we conclude that this latest-generation isokinetic dynamometer could be used with confidence to evaluate trunk muscle function for clinical or athletic purposes.     

Comparison of erector spinae and hamstring muscle activities and lumbar motion during standing knee flexion in subjects with and without lumbar extension rotation syndrome

The aim of this study was to compare the activity of the erector spinae (ES) and hamstring muscles and the amount and onset of lumbar motion during standing knee flexion between individuals with and without lumbar extension rotation syndrome. Sixteen subjects with lumbar extension rotation syndrome (10 males, 6 females) and 14 healthy subjects (8 males, 6 females) participated in this study. During the standing knee flexion, surface electromyography (EMG) was used to measure muscle activity, and surface EMG electrodes were attached to both the ES and hamstring (medial and lateral) muscles. A three-dimensional motion analysis system was used to measure kinematic data of the lumbar spine. An independent-t test was conducted for the statistical analysis. The group suffering from lumbar extension rotation syndrome exhibited asymmetric muscle activation of the ES and decreased hamstring activity. Additionally, the group with lumbar extension rotation syndrome showed greater and earlier lumbar extension and rotation during standing knee flexion compared to the control group. These data suggest that asymmetric ES muscle activation and a greater amount of and earlier lumbar motion in the sagittal and transverse plane during standing knee flexion may be an important factor contributing to low back pain.     

A functional-morphometric analysis of forelimbs in bipedal and quadrupedal heteromyid rodents

The rodent family Heteromyidae contains bipedal hoppers and quadrupedal runners. The possibility that bipedalism is associated with forelimb specialization for nonlocomotory functions, such as burrowing and seed-gathering, motivated a static functional-morphometric and interspecific allometric analysis of 18 metric characters of the forelimb skeleton. A principal-components analysis, across 28 species in six genera, showed that lengths of proximal (scapula, humerus) and distal (ulna, radius, metacarpal) elements were negatively allometric, and widths were positively allometric. Quadrupedal and bipedal species groups showed qualitatively similar allometric patterns, except that scapula width anterior to the spine was positively allometric in quadrupeds and negatively allometric in bipeds; scapula width posterior to the spine was positively allometric in bipeds and isometric in quadrupeds; and olecranon length was isometric in bipeds and positively allometric in quadrupeds. Most morphometric characters varied significantly among species within genera, even when effects of size variation were reduced by reconstructing all species to a common general size (as indicated by their score on the first principal component). These shape differences caused species to vary in the mechanical advantage of the forelimb, of possible importance for digging and seed-harvesting performance. Relative to quadrupeds, bipedal species tended to have greater mechanical advantage for proximal forelimb elements and smaller mechanical advantage for distal forelimb elements, but only the distal pattern remained in reconstructed forms, and no functional character was significantly different when tested over variation among genera nested within locomotion type. Cluster analysis confirmed that forelimb characters related to digging or seed-harvest are not coincident with mode of locomotion. Forelimb characters were, however, associated with digging or seed-harvest performance. Mechanical advantage of the proximal forelimb was positively related to an index of the compaction of soils with which 26 desert-dwelling species are associated, and also to relative use of heavy vs. light soils by nine species in the laboratory. Across 10 species, deviations in seed-harvest rate from expected allometric values were negatively correlated with mechanical advantage of the distal forelimb.     

Comparison of hind limb muscle mass in neonate and adult prosimian primates

Little ontogenetic data exist to indicate whether muscular organization of neonates reflects adult locomotion (e.g., leaping) or infant activities like clinging or the initial quadrupedal phase of locomotion that typifies most infant primates. In the present study, five species of primates with contrasting modes of locomotion were examined. Twenty-eight preserved neonatal and adult cadavers were studied by careful dissection of the hip, thigh, and leg muscles. Wet weights were taken of limb muscles after removal, and the muscles were combined into major functional groups (e.g., flexors, extensors) of each limb segment. Results demonstrate that the distribution of muscle mass within the thigh and within the leg are similar between neonates and adults for all species, with major groups varying by 5% or less in all but two age comparisons. Crural indices of the neonates are nearly identical to those of the adults, but leg/thigh muscle mass ratios were higher in the neonates. Species vary greatly in the percentage of adult limb segment muscle mass present in neonates, with Tarsius syrichta having the greatest percentage for all segments and two lemurids showing the least. These results primarily track differences in relative body mass at birth rather than developmental differences. The adaptive distribution of muscle, as discussed previously for adult prosimians, appears to be established at birth. Neonates of leaping species already have much larger quadriceps muscles than quadrupeds. Differences between large- and small-bodied leapers (e.g., pronounced superficial plantarflexor masses in tarsiers and pronounced deep plantarflexor masses in sifakas) also are present in neonates. Ratios of muscle mass over body mass are smaller in all neonates than in their adult counterparts, suggesting that the neonates are relatively poorly muscled, and that muscle mass must increase with positive allometry during growth.     

Electromyography of the gluteal muscles in Hylobates,Pongo, and pan: Implications for the evolution of hominid bipedality

The gluteal musculature of primates has been a focus of great research interest among those who study human evolution. Most current theorists agree that gluteus superficialis (= maximus) need not have changed its action in the step from pongid to hominid, but dispute has arisen over a purported change in action and role of the gluteus medius. To clarify the functions of gluteus medius, gluteus superficialis, and tensor fasciae femoris during ape locomotion, we conducted a telemetered electromyographic study of these muscles in two gibbons, one orangutan, and four chimpanzees as they walked bipedally on the ground and on a horizontal tree trunk, walked quadrupedally on the same substrates, and climbed a vertical tree trunk. The results indicate that the gluteus medius of apes is not, as has been previously suggested, primarily an extensor of the thigh; its action is chiefly that of medial rotation. The role of the gluteus medius during bipedality is the same in apes and humans–to provide side-to-side balance of the trunk at the hip. The change in the hominid lateral balance mechanism can be viewed as primarily osteological, allowing preservation of the same muscle function with an extended thigh. As a result, the stride length is increased and there occurs a diminution of the demands placed on other muscles to maintain anteroposterior balance at the hip and knee. Our data also support the view that vertical climbing may be specifically preadaptive to bipedalism. One may picture the earliest hominid as part biped, when on the ground traveling between scattered food trees, and part climber, when moving from the ground to food.     

The role of trunk muscles in sitting balance control in people with low back pain

The purpose of this study was to examine the muscular activities and kinetics of the trunk during unstable sitting in healthy and LBP subjects. Thirty-one healthy subjects and twenty-three LBP subjects were recruited. They were sat on a custom-made chair mounted on a force plate. Each subject was asked to regain balance after the chair was tilted backward at 20°, and then released. The motions of the trunk and trunk muscle activity were examined. The internal muscle moment and power at the hip and lumbar spine joints were calculated using the force plate and motion data. No significant differences were found in muscle moment and power between healthy and LBP subjects (p > 0.05). The duration of contraction of various trunk muscles and co-contraction were significantly longer in the LBP subjects (p < 0.05) when compared to healthy subjects, and the reaction times of the muscles were also significantly reduced in LBP subjects (p < 0.05). LBP subjects altered their muscle strategies to maintain balance during unstable sitting, but these active mechanisms appear to be effective as trunk balance was not compromised and the internal moment pattern remained similar. The changes in muscle strategies may be the causes of LBP or the result of LBP with an attempt to protect the spine.     

New method of three-dimensional analysis of bipedal locomotion for the study of displacements of the body and body-parts centers of mass in man and non-human primates: Evolutionary framework

The current biomechanical interpretation of the chimpanzee's bipedal walking argues that larger lateral and vertical displacements of the body center of mass occur in the chimpanzee's “side-to-side” gait than in the human striding gait. The evolutionary hypothesis underlying this study is the following: during the evolution of human bipedalism one of the necessary changes could have been the progressive reduction of these displacements of the body center of mass. In order to quantitatively test this hypothesis, it is necessary to obtain simultaneously the trajectories of the centers of mass of the whole body and of the different body parts. To solve this problem, a new method of three-dimensional analysis of walking, associated with a volumetric modelling of the body, has been developed based on finite-element modelling. An orthogonal synchrophotographic device yielding four synchronous pictures of the walking subject allows a qualitative analysis of the photographic sequences together with the results of their quantitative analysis. This method was applied to an adult man, a 3-year-old girl and a 9-year-old male chimpanzee. Our results suggest that the trajectory of the body center of mass of the human is distinguished from that of the chimpanzee not by a lower movement amplitude but by the synchronization of the transverse and vertical displacements into two periodic curves in phase with one another. The non-human primate uses its repertoire of arboreal movements in its bipedal terrestrial gait, provisionally referred to as a “rope-walker” gait. We show that the interpretation of a “side-to-side” gait is not applicable to the chimpanzee. We argue that similarly this interpretation and the initial hypothesis presuppose a basic symmetric structure of the gait, in relation to the sagittal plane of progression, similar to the human one. This lateral symmetry of the right and left displacements of the center of gravity, in phase with the right and left single supports of walking, is probably a very derived feature of the human gait. We suggest that low lateral and vertical displacements of the body center of mass are not indicative of a progressive bipedal gait and we discuss the new evolutionary implications of our results. © 1993 Wiley-Liss, Inc.     

Dynamics and stability of muscle activations during walking in healthy young and older adults

To facilitate stable walking, humans must generate appropriate motor patterns and effective corrective responses to perturbations. Yet most EMG analyses do not address the continuous nature of muscle activation dynamics over multiple strides. We compared muscle activation dynamics in young and older adults by defining a multivariate state space for muscle activity. Eighteen healthy older and 17 younger adults walked on a treadmill for 2 trials of 5 min each at each of 5 controlled speeds (80–120% of preferred). EMG linear envelopes of v. lateralis, b. femoris, gastrocnemius, and t. anterior of the left leg were obtained. Interstride variability, local dynamic stability (divergence exponents), and orbital stability (maximum Floquet multipliers; FM) were calculated. Both age groups exhibited similar preferred walking speeds (p=0.86). Amplitudes and variability of individual EMG linear envelopes increased with speed (p<0.01) in all muscles but gastrocnemius. Older adults also exhibited greater variability in b. femoris and t. anterior (p<0.004). When comparing continuous multivariate EMG dynamics, older adults demonstrated greater local and orbital instability of their EMG patterns (p<0.01). We also compared how muscle activation dynamics were manifested in kinematics. Local divergence exponents were strongly correlated between kinematics and EMG, independent of age and walking speed, while variability and max FM were not. These changes in EMG dynamics may be related to increased neuromotor noise associated with aging and may indicate subtle deterioration of gait function that could lead to future functional declines.