Comprehensive reviewLocomotion and dynamic posture: neuro-evolutionary basis of bipedal gait
Introduction
Dynamic balance is an essential feature of animal movements, and displacements require at each moment the integrated coordination of all body segments. But what is the difference between static balance and dynamic balance and what are the biological processes that allow the body to adapt posture appropriate for an ongoing behavior? As a general definition, under dynamic equilibrium, the amount of energy released by the system towards the environment is equal to the amount of energy released in the opposite direction. The conservation of balance during locomotion depends on a complex interaction between external (gravity, reaction forces) and internal forces generated by muscle activities and by their close interactions with the musculoskeletal system including bones and connective tissues [70]. In this perspective, the concept of tensegrity [80], which is the ability of a structure to stabilize itself through an interplay of the forces that are distributed within it, is central to consider when addressing balance. Our bodies constitute a biomechanical system in which tension and pressure are permanently at work in order to stabilize it in space, and this is achieved through the action of fasciae (bands of connective tissue) and the skeleton. Three main components can therefore be identified that allow organisms to permanently and harmoniously switch from one state (dynamic vs static) to the other (Fig. 1): (1) the nervous system; (2) skeletal tissue ; and (3) connective tissues, which act as an interface between the skeletal muscle tissue and nervous system. Fasciae are present throughout the body, enveloping all organs including muscles and which allow forces to be transmitted to bones. In vertebrates, the viscoelastic properties of collagenous fasciae have undergone continuous changes in accordance with an organism’s particular lifestyle and/or changing external environment. On the other side is the nervous system which when activated, can set in motion the myo-connective tissues and skeleton according to spatially and temporally determined motor patterns.
Moving from one place to another therefore requires an interruption of static posture in order to engage the body and limbs in cyclic ongoing behavior that is inherently unstable. In humans, the trunk, which represents 50% of the total body mass with a location that raises the center of gravity, permanently presents a challenge to maintaining balance. In addition, the trunk has a complex structure, with a highly articulated skeleton and a dense muscle array that enable the versatility required to accomplish a large number of different tasks during which adequate body balance is maintained. This versatility is an asset but is also a drawback, particularly during locomotion when trunk movements must be regulated in a complex way by the combination of anticipatory and reactive muscular actions. Understanding the axial dynamics that regulate activity of the trunk is therefore important, since as a pillar of body architecture, truncal activity is an essential component of locomotion.
Although many studies have addressed the role of hindlimbs during locomotion, much less work has been devoted to the interactions that take place between trunk and hindlimb control during locomotion. The aim of this review is therefore to address this issue in a comparative phylogenic perspective, by considering how the central nervous system acts dynamically on the musculoskeletal system during locomotion to allow effective coordinated behavior. The first part of this review will address the role of the central nervous system in coordinating trunk/leg movements during locomotion in animals and humans, and a final part will focus on the essential role played by connective tissues in maintaining stability, the contribution of which is often neglected.
Section snippets
Muscle organization
Is there a direct phylogenetic functional link in structures (neural and/or muscular) that emerged between 4 and 5 hundred million years ago and then became progressively adapted according to changing behavioral needs, as organisms found new habitats and lifestyles? Or has evolution continuously imposed a tabula rasa of pre-existing systems and their de novo reassembly in order to optimally satisfy these new demands? Answering these questions is complicated by the fact that, concomitant with
Lower vertebrates
In the lamprey and Xenopus embryo, swimming is the result of successive bilaterally alternating segmental muscle contractions that propagate in a rostral-to-caudal wave along the body, allowing the animal to be propelled forward [38], [65]. The delay between adjacent segments is ∼1% of the cycle time (for about 100 vertebral segments [54];). The major importance of these models is that so-called "fictive" locomotion can be induced in isolated spinal cord preparations in vitro, by activating
Trunk/hindlimb interactions in humans
Motor wave propagation along the axial musculature is not only restricted to quadrupeds. Electromyography (EMG) recordings from human back muscles during walking have shown a temporal organization that in terms of motor burst onsets and phase relationships are comparable to those of quadruped species [Fig. 2B and Fig. 3B; [24] [61],]. When the arms and legs are active together in human walking, two bursts of activity are recorded in the axial musculature during each locomotor cycle.
Connective tissue and motor function
In this part, we will briefly address the role of an essential component of motricity, namely the connective tissues, whose function is often neglected. To date, the functional link between all the various components illustrated in Fig. 1 is not clear, but there is no doubt that, in addition to their cohesive function they also play a major task in transmitting forces and organizing movement.
Characteristics and mechanical role of connective tissue
Connective tissues perform supportive roles by constituting the “deformable skeleton” of an individual as they ensure a movable continuity between individual structures, guaranteeing their stability while conveying mechanical tension generated by muscular activities or external forces throughout the body. Any voluntary mobilization or reflex includes a passive component, the support, constituted by the bone skeleton, and four basic active components - acceleration, braking/reception,
Neurological characteristics and roles of connective tissues
Connective structures, in their various forms, are not only essential to the harmony and efficiency of movement but also play a fundamental role in transmitting information about tissue deformations. Their response selectivity and sensitivity will depend on the sensors embedded in the tissue. Our understanding of the respective contributions of such sensory pathways is still fragmentary due to the diversity of associated tissues, their location and their relationship with other anatomical
Vestibulospinal regulation of locomotion
As the CNS also integrates sensory inputs to achieve optimal movement, studying sensory regulation of the axial-hindlimb system has provided further important information on the evolutionary changes undergone by locomotor systems. The vestibular system provides reliable information about head movement and orientation and can evoke reflex responses and other postural adjustments in trunk and limb muscles [7], [32]. However, as for locomotion per se, limited attention has been paid to
Conclusion
Preserving dynamic equilibrium requires the merging control of two separate subsystems that are generally considered to rely on different mechanisms. First, locomotor activity that is produced by specialized rhythmogenic spinal circuits called CPGs and which cyclically drive axial and leg muscle activity in both animals and humans [12], [28], [53], [66]. Secondly, posture control systems which involve long spinal/supraspinal loops and the integration of various sensory inputs (e.g.
Conflict of interest
The authors declare no conflict of interest.
Acknowledgements
The authors warmly thank Dr. J. Simmers for his English language editing of the manuscript.
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