Bipedal locomotion: toward unified concepts in robotics and neuroscience

This review is the result of a joint reflection carried out by researchers in the fields of robotics and automatic control on the one hand and neuroscience on the other, both trying to answer the same question: what are the functional bases of bipedal locomotion and how can they be controlled? The originality of this work is to synthesize the two approaches in order to take advantage of the knowledge concerning the adaptability and reactivity performances of humans and of the rich tools and formal concepts available in biped robotics. Indeed, we claim that the theoretical framework of robotics can enhance our understanding of human postural control by formally expressing the experimental concepts used in neuroscience. Conversely, biological knowledge of human posture and gait can inspire biped robot design and control. Therefore, both neuroscientists and roboticists should find useful information in this paper.     

Bipedal behavior and the emergence of erect posture in man

Bipedal behavior is present to some degree in most of the higher primates. Field studies of living pongids have shown that an upright stance and various types and degrees of bipedal progression are not uncommon and are thus presumably advantageous. Bipedal behavior similar to that in living pongids could also have been, and probably was, present in pre-hominids. As the environment of the pre-hominids changed, the increased use of bipedalism was of survival value. That is, it was a behavioral response to environmental circumstances and not just a random event. Once bipedal behavior became habitual, it formed part of a pattern of natural selection which shaped a physical type adapted for erect, bipedal posture.     

Sex differences in adult chimpanzee positional behavior: The influence of body size on locomotion and posture

Focal animal instantaneous sampling of adult male and female chimpanzee positional behavior was conducted during a 7-month study in the Tai Forest, Ivory Coast, in order to determine whether there are sex differences in the locomotion, posture, substrate use, and height preference of sexually dimorphic adult chimpanzees, and if so, whether these differences support predictions based on body size differences. Results indicate that as predicted, adult male and female chimpanzees differ in their arboreal locomotor behavior, with the larger males using less quadrupedalism and more climbing, scrambling, and aided bipedalism than females during feeding locomotion. There is a sex difference in height preference as well, with female chimpanzees consistently using more arboreal behavior than males, primarily during resting. Although it has been previously demonstrated that separate primate species of differing body size differ in locomotor and postural activities (Fleagle and Mittermeier, 1980; Crompton, 1984), this study clearly demonstrates that body size differences within a species can also be correlated with differences in locomotor behavior. These findings may influence how we interpret sex differences in body size of extinct species. © 1993 Wiley-Liss, Inc.     

Relationship between osteology and aquatic locomotion in birds: determining modes of locomotion in extinct Ornithurae

The evolutionary history of aquatic invasion in birds would be incomplete without incorporation of extinct species. We show that aquatic affinities in fossil birds can be inferred by multivariate analysis of skeletal features and locomotion of 245 species of extant birds. Regularized discriminant analyses revealed that measurements of appendicular skeletons successfully separated diving birds from surface swimmers and flyers, while also discriminating among different underwater modes of swimming. The high accuracy of this method allows detection of skeletal characteristics that are indicative of aquatic locomotion and inference of such locomotion in bird species with insufficient behavioural information. Statistical predictions based on the analyses confirm qualitative assessments for both foot‐propelled (Hesperornithiformes) and wing‐propelled (Copepteryx) underwater locomotion in fossil birds. This is the first quantitative inference of underwater modes of swimming in fossil birds, enabling future studies of locomotion in extinct birds and evolutionary transitions among locomotor modes in avian lineage.     

Load sensing and control of posture and locomotion

This article reviews recent findings on how forces are detected by sense organs of insect legs and how this information is integrated in control of posture and walking. These experiments have focused upon campaniform sensilla, receptors that detect forces as strains in the exoskeleton, and include studies of sensory discharges in freely moving animals and intracellular characterization of connectivity of afferent inputs in the central nervous system. These findings provide insights into how campaniform sensilla can contribute to the adjustment of motor outputs to changes in load. In this review we discuss (1) anatomy of the receptors and their activities in freely moving insects, (2) mechanisms by which inputs are incorporated into motor outputs and (3) the integration of sensory signals of diverse modalities. The discharges of some groups of receptors can encode body load when standing. Responses are also correlated with muscle-generated forces during specific times in walking. These activities can enhance motor outputs through reflexes and can affect the timing of motoneuron firing through inputs to pattern generating interneurons. Flexibility in the system is also provided by interactions of afferent inputs at several levels. These mechanisms can contribute to the adaptability of insect locomotion to diverse terrains and environments.     

Bipedal locomotion as a feeding adaptation in gelada baboons,and its implications for hominid evolution

Bipedal locomotion by gelada baboons is used for travelling between adjacent feeding sites. The same could be true of its origins in man.     

The consistency of maximum running speed measurements in humans using a feedback-controlled treadmill,and a comparison with maximum attainable speed during overground locomotion

Consistent measurement of maximum running speed overground is problematic due to the difficulty in precise, continual measurement of speed, and the substantial workload in accelerating the body promoting the onset of fatigue. Treadmills remove the requirement for acceleration which enables more repeats. They also allow experiments to be carried out in controlled environments and where space is limited, but they usually depend on manual and subjective speed control. Here we used a draw-wire position sensor and a proportional–derivative (PD) controller to automatically adjust treadmill belt speed of a large equine treadmill. The feedback loop took the real-time position and velocity of the runner relative to the front of the treadmill as input. This control system allowed runners to accelerate from walking speed to a peak running speed within a few strides and then decelerate as quickly as they wished. We used the system to evaluate the variation in maximum speed determination that results from one trial to 10 trials, in eleven individuals. Three trials gave a maximum speed 97.8% of that achieved after ten. The approach used is appropriate for any treadmill where the running zone length is greater than three metres and the speed controller can be externally controlled. Subjects ran 11.5% faster on the treadmill than overground, part of which can be explained by the removal of aerodynamic drag and the fatigue of overground running. Additional factors may, however, contribute to athletes running faster on a treadmill, for instance some aspect of stability or control.     

Effect of posture and locomotion on energy expenditure

Energy expenditure for human adults and infants and for dogs was measured in resting (supine or lateral) posture, in bipedal posture and locomotion, and in quadrupedal posture and locomotion. Variations in respiratory and heart rate and in body temperature were utilized in this comparative study. Oxygen consumption was also measured in human adults. In human adults, bipedal posture and locomotion were shown to be much less energy-consuming than corresponding quadrupedal posture and locomotion. The opposite was observed in adult dogs, where bipedalism was shown to be much more energy-consuming than quadrupedalism. In addition, this study demonstrated, for human adults in their natural erect posture, an energy expenditure barely higher than in supine or lateral resting posture, while the dogs in their natural quadrupedal stance, the energy expenditure is much higher than in their resting posture. With respect to energy, therefore, humans are more adapted to bipedalism than dogs to quadrupedalism. Human children, at the transitional stage between quadrupedalism and bipedalism, have high and almost equal requirements for all postures and locomotions. This demonstrates, in term of energy, their incomplete adaptation to erect behavior.     

The effect of locomotion speed on the anterior tibial intramuscular pressure of normal humans

We examined the hypothesis that anterior tibial intramuscular pressure increases with the speed of locomotion. A solidstate pressure transducer was placed near the tip of an intramuscular fluid-filled catheter and each of ten normal subjects walked, jogged and ran barefoot, at 1.5, 2.5 and 3.5 m s-1 respectively, on a treadmill to which they had been previously familiarized. The pressure signals during ten gait cycles from each subject were sampled at 600 Hz and were averaged at each speed. The peak pressures increased in magnitude as a function of increasing locomotion speed, while the mean pressure remained constant.     

Optimal coordination and control of posture and locomotion.

This paper presents a theoretical model of stability and coordination of posture and locomotion, together with algorithms for continuous-time quadratic optimization of motion control. Explicit solutions to the Hamilton-Jacobi equation for optimal control of rigid-body motion are obtained by solving an algebraic matrix equation. The stability is investigated with Lyapunov function theory, and it is shown that global asymptotic stability holds. It is also shown how optimal control and adaptive control may act in concert in the case of unknown or uncertain system parameters. The solution describes motion strategies of minimum effort and variance. The proposed optimal control is formulated to be suitable as a posture and stance model for experimental validation and verification. The combination of adaptive and optimal control makes this algorithm a candidate for coordination and control of functional neuromuscular stimulation as well as of prostheses.     

Optimal locomotion modes of foraging birds in trees

This paper compares the energy costs of various modes of locomotion of birds foraging in trees. For birds moving vertically in trees by climbing and hopping (but not by flying) the best choice of locomotion mode depends on the distance between visited trees in relation to the height h of the zone searched for food in trees.
When the distance between successively visisted trees is longer than about half the distance coverable in gliding flight with height loss h , then it is cheapest in energy to hop or climb upwards in a tree and fly downwards to the next tree. When the distance between successively visited trees is shorter than about half the distance coverable in gliding flight with height loss h , then it is cheapest in energy to move alternately downwards and upwards in trees (downwards in the first, upwards in the second, downwards in the third tree, etc.) and to fly level between trees.
Treecreepers and woodpeckers are adapted morphologically to the former mode, but more generalized tree foragers might use either mode depending on the spacing of trees.     

Cost and speed of locomotion for rotifers

Summary The hypothesis that the ciliary locomotion of rotifers is size limited and that it accounts of a significant portion of the energy budget was investigated using the genera Brachionus and Asplanchna. Speed of movement was measured among clones of different size in Brachionus, which shows little size variation through development. The same tests were done among individuals of different size within a clone of Asplanchna, which shows significant postembryonic size increase. In both cases, relative speed (body lengths per second) decreased significantly as body size increased. On this basis, and ecologically limiting size for ciliary locomotion is proposed. The actual cost of locomotion was measured for Brachionus; it is 62% of total metabolism, even though the theoretical (calculated) power requirements are well below 1% of total metabolism. Ciliary locomotion in the Rotifera thus appears to be extremely inefficient (low ratio of theoretical to actual power requirements). This hypothesis is supported indirectly by the sensitivity of speed to total metabolic rate in Brachionus: both plateau over the temperature range 20–32°C and decline in parallel outside this range. Unexpectedly high actual cost of locomotion is proposed as an important disadvantage of the Rotifera, partly offsetting the advantages accruing to them from small body size.     

Automatic control of limb movement and posture

Studies are reviewed that address the problem of the variables controlled by the central nervous system in the maintenance of body posture and limb movement against disturbing forces. The role of global variables of control, which take into account the dynamic state of the limb, is discussed. Neural substrates that are involved in the distributed control of kinematic and dynamic parameters are also considered.     

Climate,body condition and spleen size in birds

Climatic conditions may impact on the body condition of animals and thereby affect their survival prospects. However, climate may also impact directly on the survival prospects of animals by affecting the size of immune defence organs that are used for defence against parasites. We used a large long-term database on body condition and size of the spleen in birds to test for immediate and delayed relationships between climatic conditions as indexed by the North Atlantic Oscillation (NAO) and body condition and spleen mass, respectively. Across 14 species of birds, spleen mass was significantly positively correlated with the NAO index, while the delayed effect of NAO on spleen mass was not significant. Spleen mass was positively related to body condition, but body condition did not depend significantly on NAO or delayed NAO effects. Bird species with a strong positive effect of NAO on spleen mass tended to have small spleens for their body size, while species with a strong negative effect of NAO on spleen mass tended to have relatively large spleens. Since bird species with relatively large spleen have been shown to suffer more from the negative effects of parasites, we can infer that the effects of climate as indexed by NAO on the size of the spleen depends on the importance of parasite-mediated natural selection.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking

Although the hindlimb is widely considered to provide the propulsive force in lizard locomotion, no study to date has analysed kinematic patterns of hindlimb movements for more than one stride for a single individual and no study has considered limb and axial kinematics together. In this study, kinematic data from several individuals of the Sceloporus clarkii are used to describe the movement patterns of the axial skeleton and hindlimb at different speeds, to analyse how kinematics change with speed, and to compare and contrast these findings with the inferred effects of speed cited in the literature. Angular limb movements and axial bending patterns (standing wave with nodes on the girdles) did not change with speed. Only the relative speed of retracting the femur and flexing the knee during limb retraction changes with speed. Based on these data and similar results from a recent study of salamanders, it appears that, over a range of speeds involving a walking trot, sprawling vertebrates increase speed by simply retracting the femur relatively faster, thus this simple functional adjustment may be a general mechanism to increase speed in tetrapods. The demonstration that femoral retraction alone is the major speed effector in Sceloporus clarkii lends strong functional support to ecomorphological implications of limb length (and especially femur length and caudifemoralis size) in locomotory ecology and performance in phrynosomatid lizards. It also lends support to inferences about the caudifemoralis muscle as a preadaptation to terrestrial locomotion and as a key innovation in the evolution of bipedalism.     

Behavioral and cellular effects of serotonin on locomotion and male mating posture in Ascaris suum (Nematoda)

The site and mode of action of serotonin on locomotion were investigated in the parasitic nematode Ascaris suum. Injection of serotonin into Ascaris immediately caused paralysis in animals that were generating locomotory waveforms. Injected serotonin also increased body length and decreased the number of propagating body waves. Similar injections into the male tail produced a ventral tail curl. Injection of N-acetyl-serotonin had no effect on the generation of locomotory waveforms, but increased the body length and decreased the number of body waves in the waveform. Other biogenic amines were also tested but were much less potent.Serotonin decreased the amplitude of a submaximal acetylcholine-induced muscle contraction and increased the time to attain this contraction. The time course of this effect on the response to ACh was much slower than the action of injected serotonin on locomotory waveforms, suggesting that additional elements are involved in the action of serotonin on locomotory behavior.Serotonin abolished spontaneous slow potentials in VI motor neurons and decreased the frequency of EPSPs in DE2 motor neurons, probably by a pre-synaptic mechanism. In the male tail, serotonin depolarized the male-specific transverse ventral muscle cells, but did not affect either dorsal or ventral longitudinal muscle cells.Abbreviations ACh acetylcholine - cAMP cyclic adenosine monophosphate - DA dopamine - DE dorsal excitatory motor neuron - DI dorsal inhibitory motor neuron - DM dorsal muscle - ELP egg-laying pore - EPSP excitatory post synaptic potential - GABA gamma aminobutyric acid - HRB head restricted behavior - IPSP inhibitory post synaptic potential - 5-HT 5-hydroxytryptamine, serotonin - NA-5-HT N-acetyl-5-hydroxytryptamine - NE norepinephrine - OA octopamine - PBS phosphate buffered saline - PCF pseudocoelomic fluid - tVM malespecific transverse ventral muscle - TRYP tryptamine - VI ventral inhibitory motor neuron     

Brain size, development and metabolism in birds and mammals

Recent hypotheses that variation in brain size among birds and mammals result from differences in metabolic allocation during ontogeny are tested.
Indices of embryonic and post-embryonic brain growth are defined. Precocial birds and mammals have high embryonic brain growth indices which are compensated for by low post-embryonic indices (with the exception of Homo supiens ). In contrast, altricial birds and mammals have low embryonic and high post-embryonic indices. Altricial birds have relatively small brains at hatching and develop relatively large brains as adults, but among mammals there is no equivalent correlation between variation in adult relative brain sizes and state of neonatal development.
Compensatory brain development in both birds and mammals is associated with compensatory parental metabolic allocation. In comparison with altricial development, precocial development is characterized by higher levels of brain growth and parental metabolic allocation prior to hatching or birth and lower levels subsequently. Differences between degrees of postnatal investment by the parents in the young of precocial birds versus precocial mammals may result in the different patterns of adult brain size associated with precociality versus altriciality in the two groups.
The allometric exponent scaling brain on body size differs among taxonomic levels in birds. The exponent is higher for some parts of the brain than others, irrespective of taxonomic level. Unlike mammals, the exponents for birds do not show a general increase with taxonomic level. These pattcrns call into question recent interpretations of the allometric exponent in birds. and the reason for changes in exponent with taxonomic level.