(1)
Faculty of Medicine of Montpellier, Montpellier, France
Abstract
Human locomotion is based on a bipedal mode requiring two functions: the propulsion made by the scissor movement of hip joint increased by the additional force given by the feet and the dynamic automated stabilisation realised through four inputs: vision, skin, vestibule and muscles. Walking requires a high level of control for starting and stopping, speed and trajectory control and a low level of control for managing the gait sequences with an oscillator in the spinal cord for quadrupeds and in the brainstem for primates and humans. Posturology and gait analysis have made substantial progresses and represent at the moment very useful clinical tools to analyse normal or pathological locomotion.
3.1 Introduction
Locomotion is a complex function that must be clearly explained in order to get a good perception of the related technical problems. For human beings, moving means using a bipedal mode of locomotion, but he is not the only one.
The fowl stands also on two legs and although they almost all have the ability to fly, they move on the floor with an alternating sequence of two leg supports. As a special case, we can report the ostrich that walks and runs on two legs with a perfect dynamic balance, but cannot fly. Auk is another example of a bird with a special waddling walking as if it had a double dislocation of the hip. It cannot fly in the air, but perfectly in the water. This diversion is made to reaffirm that being a biped is not, as some still believe, the determinant factor in human emergence.
3.2 The Two Aspects of Locomotion
They are, firstly, the vertical posture preparatory to walking (stato-dynamic aspect) and, secondly, walking and its variants: running, jumping and climbing (dynamic and kinematic aspects).
3.2.1 Upright Posture
It can be done on two feet (bipodal) or on one foot (monopodal). In both cases, it is strongly automated, still owing to the same reason: the technical incompetence of the pilot.
Posture is defined as a mechanical condition of a stabilised body segment. Human being, unlike a lead soldier put on a table that really stands in a static domain, is characterised by an equilibrium between forces and moments. Man is a polyarticulated viscoelastic structure that cannot remain in a vertical position, in a real static condition, because he continuously requires more or less important corrections of the oscillations, of the centre of gravity, which all can be measured and recorded. This represents the areas of posturology, posturography and stabilometry, which explore stato-dynamic field to comply with the rigour of mechanics [1–5].
As we have already seen about spinal stabilisation, it is really a postural servomechanism with an input and an output in the form of muscular contractions operating by impulses with anticipation.
3.2.1.1 Postural Servomechanism Inputs
We can define four inputs: visual, cutaneous, muscular and utricular. The last two have already been described in the spinal postural servomechanism, and it is necessary to focus on the two inputs able to ensure the balance: the vision and the skin through the plantar force plate.
Visual Input
We have already mentioned the power of neural foveal fixation of gaze which enables taking a fixation point in the space and to move around (turn head top or bottom, move the whole body in rotation, …) by activating a number of muscles while keeping the same visual fixed point in space. However, this function is automatically used to ensure an unconscious equilibration of the body by taking a reference line in space (vertical or horizontal). To support this assertion, we can provide some evidence:
firstly, if we put in a vertical position a person with a reduced skin sensibility of the foot, like in tabes, or even more easier to find, in diabetes with micro-angiopathies clinically detectable (retina or sole), we observe that the person is well balanced with eyes open, even while turning the head. However, if asked to close his eyes, the subject oscillates and loses his balance. This manoeuvre has been described by Romberg [1] who explains that the vision only cannot ensure balance;
secondly, the subject feels a certain discomfort accompanied by dizziness when standing in front of a monument occupying the whole visual field and having a general inclination of several degrees (as is the case with the Guadalupe Church in Mexico City). This can be explained by the discordance between the visual input having a false reference line and the cutaneous plantar sole input getting the true reference from contact with the ground. We repeated this experiment in our laboratory by placing some subjects in a room without any indication of linear geometric angles or sides, and some others in a completely dark room with a vertical or horizontal light line inclined until the dizziness appears. Physiologically it is equivalent to a typical optical vertigo.
Similarly, an intersensory discrepancy including vertigo can be observed in a fisherman, focusing all his attention on trying to put a worm bait into his hook, while sitting in a boat moving at the low frequency of the oscillations from the surface of the water. The discrepancy between visual input and labyrinthine vestibular signals reflects a conflict within the brainstem, generating a vertigo with a possible activation of the central vomiting centre [6]. This approximates the seasickness of a tourist lying in his cabin and reading a book, while the boat oscillates in pitch and roll resulting in a dizziness coming with nausea and optionally vomiting. The solution is to go out and find a fixed reference line (horizon) to reset the vestibule.
Skin Input: The Plantar Force Plate
This entry also provides a full control of postural balance. The sole is equipped with a real dynamometric platform, which sensors are the strings of Pacinian corpuscles scattered throughout the plantar support area [7]. These corpuscles are similar to ant eggs with about the same dimensions (4 mm × 2 mm) that can then be dissected under a microscope. They present an ovoid shape formed by an external fibrous capsule with, inside, concentric lamellae in “onion bulb”. The neural sole placed in the centre is formed by a nerve fibre spread having left its myelin sheath (Fig. 3.1).
Fig. 3.1
The Pacini mechanoreceptors. (a) Microdissection of the Pacini corpuscles (2–4 mm): 1. Sensitive plantar nerve; 2. Corpuscles; 3. Triceps tendon. (b) Graphic reconstruction of a corpuscle (after Tood and Bowman): 1. Concentric lamellas; 2. Neural plate; 3. Arterial microvessels (responsible for renitency and sensibility of the transducer); 4. Myelinated sensitive fibre losing myelin after penetration within the corpuscle. (c) Histological section of a corpuscle: 1. Fibrous capsule; 2. Neural plate; 3. Concentric onion shape lamellas
The amazing fact is that it exists within the corpuscle fine capillaries with a liquid exudate filling more or less the sensor and creating thus a variable sensitivity. The more it is renitent, the more it is sensitive. It may therefore partly explain the impaired balance observed in diabetic patients with a microangiopathy affecting these fine capillaries and greatly reducing the sensitivity of the sensor [3]. These corpuscles are also present in the palm of the hand to ensure automatic control of grasping forces, as we shall see later.
It is clear that a proper posturologic investigation must take into account these facts altogether. It is not a problem to place a subject on a force plate for less than a minute, to record a posturogramme, analyse it and possibly make the Fourier transformed of collected data, but the conclusions are then very often extrapolated. It is rather necessary to study the subject eyes open and closed, in bipodal and monopodal stations, and what is even better, with a complete study of walking by measurement of centres of pressure, using if possible a treadmill in order to ensure exploring the automatic walking phase as well [8].
3.2.1.2 The Balance Corrections by Muscular Impulses
By placing a subject on a dynamometric platform using strain gauges and having EMG skin electrodes put on the anterior and posterior muscles of the leg, as was done in our Unit 103 of INSERM, it is possible to record the equilibration muscular reactions automatically triggered by imbalance measured by the foot platform. The muscle reaction appears with a certain threshold and reaches a maximum at the maximum of anterior and posterior unbalance. The acceptable limit of equilibration is possible up to about 7° of inclination. Over this limit, the gravity line no longer falls in the area of plantar lift and equilibration is not possible. It is mainly the leg muscles that are involved: tibialis anterior and toes extensor for posterior imbalance and tibialis posterior, soleus and flexor digitorum longus for anterior imbalance.
In the light of these experiences, it seems that the term “tonic-postural system” to describe these mechanisms of automatic balance corrections is not correct. The definition of tone has always been a subject of controversy, and it appears that it characterises the viscoelastic state of a muscle at rest, capable of exerting a minor elastic tension, very different from the active contraction of the muscle. Establishing a difference between tonic and phasic is not very clear with respect to the muscle reactions recorded on a platform, which are real contractions unrelated to muscle tone. This is why we prefer to speak about postural servomechanism.
3.2.2 Walking
Walking is the semi-automatic management of maintained imbalances. This definition deliberately focuses on the automatic sequence of operation, each phase being unstable and requiring a permanent stabilisation in a dynamic mode. This acquisition is pre-programmed in the sense that a normal child at a certain age, even abandoned, will stand up and walk after a few failed attempts resulting in a minor fall on the buttocks due to the mass distribution at this age, even if it is much more enjoyable for parents to believe that they had him make his first steps. After 1 year, the child walk better and it is clear that he has no knowledge in physiology which validates the automated character of walking. The early registration in the nervous system of this function explains also that it can be used up till the extreme stage of life, even with highly degraded systems (muscular atrophy, diverse arthrosis, use of crutches, …).
It is also interesting to observe that a natural ability exists to find the right functional compensation as may be seen in polio children, different lameness (hip, knee, foot) or amputation. However, it is clear that the movement-trained therapists (doctors and physiotherapists) are able to exploit the most of this natural ability.
There are two functions in walking: propulsion (put one foot before the other and again) and stabilisation, using control loops involving interacting complex systems.
3.2.2.1 Control Levels of Walking
This is one of the technical aspects we need to understand well. Specialists in automation control speak about high level and low level, which applies perfectly to walking.
High Level Control
It is what the “pilot” uses to manage consciously, regardless the automation of the sequence running, the progress including the numerous technical problems arising.
Starting and Stopping
It is a decision that must be made in the premotor area, mobilising also the subcortical structures containing the motor library. Thus, subjects with Parkinson have a clear hesitation; they usually start with a series of short and quick steps. Stopping is also a technical complex procedure since we slow down and have to end up in a stable position. We studied these processes in the INSERM Unit and observed that the brutal stop on an obstacle requires the involvement of many muscles and crossing the obstacle shows the important role of visual guidance. Therefore vision records unconsciously topographical parameters, allowing the movement of the foot, which is not seen by the subject, at 1 cm from the edge of the obstacle in the case of a box 60 cm high. This is the same problem when walking on a rough terrain, where the foot placement must avoid obstacles (emerging stone, depression, …), which is done without too much effort thanks to the anticipation power of visual guidance. The blind replaces it with a guide touch, using a stick more or less sophisticated. In this regard, advanced automation walking is limited in a sequence of obstacles like the steps of a staircase because, as we have seen, having in the sequence a step 2 cm higher (not visible by the subject) leads necessarily to stumbling or falling.
Speed Control
It is a semi-automatic control in the sense that one can voluntarily change its walking speed. Two parameters are changed: firstly, cadence (number of steps) and secondly, the length of the step.
It should be remembered that a step is defined as being the same distance between two supports of the same foot (heel contact of the right and left foot). Some schools talk about a half-step to designate the distance between left and right support. This value can be asymmetric in some lameness. Trained walkers generally adopt a “comfort” rate level in flat ground, but it is interesting to note that there is an automatic regulation of the link cadence/step length, which is manifested in the rise of a slope usually with a decrease of both parameters or of one of them.
The military, normally prepared to obey without discussion, know how to walk in step, with or without music, but in this case, the perfect rhythmic answer demonstrates the power of the rhythm generation imposed by the hearing function. This is also the case for all forms of dance, from classical with strict traditional rules to modern with unbridled rhythmic fluttering and lonely on night clubs (like in a zoo).
Trajectory Control
Apparently simple, it is in fact quite complicated. We have seen that the quadruped performs its track changes by lateral bending of the spine (justifying the role of the epispinatus muscle). This also explains why their humerus and femur have no neck. Human beings in bipedal walking are changing direction with the hip, fully justifying the femoral neck lever operated by many muscle rotators. In reality, the changes are not always of large amplitude, but turning on the spot, which is apparently simple, requires the use of a differential length of left/right steps or vice versa, depending on the direction of rotation. We studied this problem when we produced, with the assistance of the Automation Division of Renault car factory, a “walking machine” operating in master-slave system for paraplegic patients. It was using a pneumatic splint with four hydraulic motors (hip/knee activation) driven by a physiotherapist coated with the same brace and with four potentiometers on hips and knees. In this model, the therapist allowed the patient to walk through appropriate control software. This allowed us to make two interesting observations:
firstly, the patient who had a complete paraplegia with no sensitivity in the lower limbs tended to look at his feet in order to see what was happening to the lower limbs. This represents a quite normal form of compensation for the lack of goniometric perception of movement. But it was perturbing the execution of the gait sequence. This was a valuable lesson for our research programme of restoration of locomotion in paralysed patients by implanted electrostimulation. In fact, the patient has to have full confidence in technology not to look at what is happening in their insensitive body area;
secondly, the artificial use of a right/left differential step length to change direction is too complicated and unreliable. So the best solution is to make a usable rotation on one foot by turning the trunk.
Low Level Control
It lies at an unconscious level located mainly in the spinal cord in which lies a complex functional architecture due to several factors:
firstly, during embryogenesis, the segmentation of the neural tube in metamers (from Greek meron, the segment) gives rise to a series of spinal nerves. They are formed, because of the separation of sensitive inputs and motor outputs, with the junction of a sensory root with spinal ganglion (the first relay of the sensory pathway) and a motor root containing motor fibres coming from the anterior horn of the spinal cord (alpha and gamma motor neurons);
secondly, the need to link the various segments by a functional interconnection system fully justifies the interneurons. This can be explained by the fact that most muscles have a multi-root innervation requiring to activate at the same time several metameric levels. The spinal cord has also an important reflex activity not only monosegmental but also plurisegmental like the flexor withdrawal reflex of the lower limbs after painful stimulation of the skin which also exists in paraplegic patient or like alternated flexion/extension reflex;
thirdly, this raises the issue of a possible gait pattern spinal generator, ensuring the automatic sequences of gait. This is still subject to controversy, and to understand, it is important to know the specific difference in the neurophysiology of an animal opposed to a man.
In animal, knowing nothing in neurophysiology, it is important to maintain a high level control as we defined before in order to enable them to voluntarily choose speed and trajectory, and still without being capable of complex voluntary conscious actions with limbs. That may explain why the corticospinal tract connecting the cortical motor keyboard to spinal cord stops at the cervical level in ungulates and herbivores, and at the level of lamina V (in the terminology of Rexed) of the sensory dorsal horn in carnivores and rats.
It happens only in humans and primates that the corticospinal tract is connected to each metameric level of the motor anterior horn of the spinal cord. This indisputable biological fact explains the predominance in the animal of a spinal cord automation, able to generate the sequence of forelimbs and hindlimbs in several possible modes used in quadrupedal locomotion, very useful to catch mobile provender. But for a quadruped walking on two hind legs, it is not a natural phenomenon and it requires a careful and very prolonged training by a human trainer.
In humans, the direct connection to each metameric level of motor control centre explains the wide variety of actions of upper limbs and lower limbs, although the relatively small size of its cortical representation implies less variability of cortical control.
Therefore, it is clear that in the human central nervous system it necessarily exists a walking oscillator delivering rhythmic sequences. Several experimental arguments allow to find out its location:
firstly, a beheaded duck, frequently experienced when living in the countryside, can do a few steps before collapsing completely;
secondly, in the hands of a good physiologist, a decerebrate cat can still walk on a treadmill;
thirdly, thanks to the French doctor Guillotin, inventor during the French Revolution of a cleaner and more efficient instrument than the axe, we have in France a great experience for the beheading of humans. A headless man standing up and making a few steps has never been observed (except in some exceptional miracle). Nowadays, public beheading is still practised in some countries. A man carrying a sword standing behind a condemned man executes the task, but nobody reported the victim running afterward;
fourthly, the newborn automatic gait described by André Thomas (1952) can be observed by putting a newborn immediately after delivery on his feet. The alternating movements of flexion of the lower limbs observed are in reality not comparable to real walking, but are, as the phenomenon disappears at about the age of 2 months, spinal flexor withdrawal reflexes in connection with an incomplete myelination of the major pathways of the nervous system.
This allows us to understand that animals have their locomotion automation centre within the spinal cord, but man has his walking oscillator into a supraspinal level in the brainstem. It is therefore unrealistic to expect to stimulate the spinal cord of a paraplegic patient to restore locomotion. In addition, the vision, so often shown, of a spinal transected rat, and even with the inclusion of various neuronal components, walking on a treadmill is not particularly convincing except for researchers who continue to work in these quadruped animals without showing positive results in humans.
The newborn automatic gait described by André Thomas (1952) can be observed by putting a newborn immediately after delivery on his feet. The alternating movements of flexion of the lower limbs observed are in reality not comparable to real walking, but are, as the phenomenon disappears at the age of 2 months, spinal flexor withdrawal reflexes in connection with an incomplete myelination of the major pathways of the nervous system.
3.2.2.2 Biomechanics of Walking
Without going into tedious technical details, it is important to know the various phases of walking and the role of each motor unit: hip (cyclic motor), knee (length control) and foot (stabiliser and additional propellant).
Gait Phases
There is a certain consensus in all gait analysis laboratories to define the different phases of a step as follows:
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