Postural control system - Science Direct

Postural control system Jean Massion Laboratory of Neurobiology

and Movements,

CNRS,

The postural control system has two main functions: and position

perception

and action with

of postural

control

as orientation internal

respect to the external world. components:

of body segments and position

inputs regulating

orientation

and stabilization

reactions or anticipations

postural

stabilization

Current

dual function values,

such

during voluntary

of body segments; and flexible

movement.

be discussed

in normal

subjects (during

relevant deficits.

Opinion

4:877-887

Introduction Body posture is built up by a set of assembled segments, each with its own mass, that are linked together by flexible joints controlled by the neuromuscular system. The central organization of posture involves interactions between external forces, such as gravity, the mechanical properties of the body and the neuromuscular forces. In order to understand the present trends in studies on postural organization, one should bear in mind that posture serves two main functions. First, it has a mechanical antigravity function whereby the reference posture (stance) is built up; equilibrium also depends on this antigravity function, which requires the center of gravity (CG) projection to remain inside the supporting surface under static conditions. Second, it serves as a reference frame for perception and action with respect to the external world. The position and orientation of body segments such as the head, trunk or arms serve as a reference frame for calculating target locations in the external world and for organizing movements toward these targets. In line with the complexity of the functions mediated by posture, central organization of its control system involves many interacting elements. On the sensory side, multisensory (visual, labyrinthine, proprioceptive and cutaneous) inputs contribute to orienting the postural segments with respect both to each other and the external world (vertical gravity vector). These classes of sensors monitor any mismatch between the intended and actual positions. A so-called ‘postural body scheme’ provides an internal representation of the body geometry, the body dynamics (support conditions) and the

or

The recent data related to

the elderly and in patients with

in Neurobiology

(an

body scheme); multisensory

for balance recovery after disturbance,

of this system will

ontogenesis),

This

reference

of the center of gravity

of the body or postural

postural

the organization

and second, to fix the

of the segments that serve as a reference frame for

is based on four

representation

France

first, to build up posture

against gravity and ensure that balance is maintained; orientation

Marseille,

1994,

body orientation with respect to verticality. The postural reactions, like the ‘anticipatory’ postural adjustments associated with voluntary movements, are organized on the basis of this internal representation, as is the whole set of interactions involved in perception and action towards the external world. Because of the complexity of the postural control system, many aspects have given rise to some debate. How are posture and equilibrium centrally organized? How does the organism adapt to changes, such as microgravity, in the environment? How is the system built up during ontogenesis? What impairments affect it in the elderly and diseased? Progress in research often depends on new methodological approaches. A new method has recently been used in this field to analyze postural control in the absence of external disturbances. Classical methods of analysis, such as recording the center of pressure oscillations from a force platform under normal stance, have been re-examined. The stationary properties of postural sway have been questioned [l]. New techniques of analysis using the chaotic dynamic approach have been proposed in order to identify putative ‘attractors’ in postural sway [2]. Collins and De Luca [3’] have carried out stochastic analyses on the center of pressure oscillations during quiet stance to identify the open-loop and closed-loop components of these oscillations. A cross-correlation method has been used on simultaneously recorded kinematic parameters at various levels of the multijoint chain involved in erect posture, with a view to identif+ng the kinematic strategies used under various sensory conditions ([4*], see also IS]). Several mathematical analyses have been carried out on multijoint changes to elucidate

Abbreviations CC-center

0 Current

of gravity;

Biology

EMG-electromyograph,

Ltd ISSN

0959-4388

877

878

Neural

control

Postural control

1 Orienta’;‘;’

1

1 ;;““ility

1

__..-,_- _. fX3y

Feedback control of posture

Cunent Opinion in Neurobiology

Fig. 1. Central organization of postural control. This schematic diagram summarizes the main components involved in the central organization of postural control. There are two sets of reference values, one is related to body segment orientation and the other is related to whole body stability (equilibrium control). These references values, and their maintenance against external or internal disturbances, are based on a body schema or internal representation of the body, which include several components, namely, body geometry and kinetics, representation of verticality and reference frame. In addition, postural networks contribute to the execution of the postural tasks. Multisensory inputs are used for building up the body schema. These inputs also act as error-detecting sensors for evaluating the mismatch between the prescribed orientation and stability, and the actual posture. The postural reactions in the presence of an error message, as well as the anticipatory postural adjustments in association with voluntary movements, are exerted through the postural networks on one or several segments. The execution of the postural reactions or anticipations are controlled on line by local feedbacks.

the control processes involved in the kinematic control of posture [6*,7*]. Biomechanical modelling is another interesting means of studying the postural strategies developed, depending on the constraints [8*,9’,10-121. This review will focus on four aspects of the postural control system, where the main contributions have been made recently. These advances are related to the control of the center of gravity, the concept of postural body schema, postural reactions and anticipation, and age-related changes.

Center of gravity control versus body geometry When stance is disturbed in bipeds or quadrupeds, the resulting postural reactions tend to move the body back toward its initial position, as long as the imposed disturbance does not overcome given limits. During stance, there is thus a reference position that is stabilized. Some controversy has arisen as to whether the reference value stabilized to preserve balance is the center of gravity position with respect to the ground, or whether the body geometry is the main value regulated.

In the former situation, the fictive point (CG), which is the result of the masses of the individual body segments, would be directly regulated, whereas in the latter, this fictive point would be regulated secondarily as a result of body geometry control. Lacquaniti has provided evidence (see [13]) that in the cat under normal stance, it is the body geometry rather than the CG that is regulated. First, the length and angle of the limb axis with respect to the vertical were kept constant when the supporting platform was tilted in the sagittal plane. Second, the CG moved when a load was added in front of the CG position, indicating that no direct regulation of the CG position occurred. In a recent study, Lacquanti and Maioli [14**] identified two separate control systems, one regulating limb length and axis with respect to the vertical, and the other the horizontal contact forces (lever component) exerted by fore and hindlimbs in order to stabilize the body. This kinetic control system presumably plays a role in maintaining the CG within the support area. In fact two parallel control systems therefore exist, the one focusing on the body geometry and the other on stability [14*-l (Fig. 1). Is the limb axis, with respect to the vertical, the geometrical reference value which is regulated during

Postural

stance? An alternative explanation has been proposed by Macpherson [15**] and by Fung and Macpherson [PI. By changing the interlimb distance in the sagittal and frontal plane, they concluded that the length and the orientation of the trunk with respect to the supporting surface, i.e. an external reference frame, is actually regulated, the legs being used as levers to maintain the trunk length constant, while the interlimb distance is varied. These authors concluded that the preferred interlimb distance during natural stance corresponds to the distance involving the least energy consumption [Y]. Is the CG regulated in human? In human bipedal stance, the narrow support surface provided by the foot area and height of the body with respect to the ground make for a much smaller safety margin than in quadrupeds. It has been established previously that after stance disturbances, one of the strategies used, namely the hip strategy, consists of flexing or extending the hip, in order to keep the CG within the stability limits [lb]. The same change in body geometry occurs when a voluntary movement of the upper trunk is performed; this would entail a movement of the CG in the same direction if no corrective processes intervened. Opposite displacements of the lower segments then occur however, which results in the maintenance of CG within the support area. This has been termed ‘synergy’ by Babinski [17] but a more appropriate name might be ‘kinematic strategy’, in line with the hip strategy known to counteract imposed disturbances. These findings indicate that in humans, the body geometry changes in order to regulate the CG position. The question then arises as to how the CG is regulated, especially when a voluntary movement is performed which would induce imbalance. The kinematic strategy observed during upper trunk bending has been analyzed using the principal components analysis method. Surprisingly, both the movement and the CG regulation carried out using the kinematic strategy were expressed by the first principal component as fully as 99% in the case of forward upper trunk movements [7’] and 96% in backward movements. This indicates that a single central control fixes the ratios between angular changes in the hip, knee and ankle joints and synchronizes their changes with time. The axial kinematic changes associated with upper trunk movements thus constitute an automatic control, probably learned in childhood, whereby the movement and the CG position are controlled simultaneously This would explain why angular changes associated with upper trunk movements remain unchanged under microgravity, in the absence of any equilibrium constraints [ 181. In addition to the stabilization of the CG position, the orientation of several body segments has also been reported to be regulated simultaneously during stance, movement or locomotion. For example, the head axis is often stabilized with respect to the vertical during locomotion [19,20]. This stabilization provides a reference value aligned with the vertical axis, used for monitor-

control

system Massion

ing, via visual and vestibular inputs, the head and body movements with respect to the environment. Head- and trunk-centered reference Ii-ames are also used for target location and movement trajectory planning (see [21]). The trunk axis is actively stabilized during locomotion in both the frontal and sagittal planes, due to the action of the hip muscles [22*,23]. The trunk stabilization in the frontal plane is increased in labyrinthine defective patients [24]. The trunk axis also remains vertically oriented during leg raising, especially in dancers [25]. As the trunk axis serves as an egocentric reference frame for calculating leg position [26*], vertical orientation of the trunk may be used for direct calculation of the leg position with respect to space. To conclude, the results of recent investigations indicate that in cats and humans, two control systems can be identified: one fixes the orientation of the body segments with respect to the external world, while the other ensures the stability of the body and contributes to stabilizing the CG (Fig. 1).

Postural body scheme According to Gurfinkel [27], there is an internal representation of the body, or postural body scheme, which is not primarily based on sensory information and deals with the body kinematics and kinetics as well as the orientation of the body with respect to the vertical. This representation is “used for the perception of body position and its orientation in space and is also used for motor control, including reactions directed towards maintaining stable body position”[27]. The body scheme remains quite stable during drastic changes in environmental conditions, such as those occurring under microgravity, where the vestibular and proprioceptive inputs are greatly modified (see [28-l). As ascertained by testing subjects’ perception of complex tactile stimuli [29] or by asking them to draw ellipses with prescribed orientations [30], the egocentric reference frame is still used in the absence of gravity to perform perceptual and spatial orientation tasks efficiently. The amplitude of forearm movements in the vertical and horizontal planes remains roughly unchanged under microgravity, except in the case of slow movements, which are disturbed because they are controlled by proprioceptive feedbacks, which are depressed under microgravity [28*]. The ability of subjects to point to remembered target positions deteriorates in space [31]. The sensors that contribute to estimating the body’s orientation, configuration and support conditions have been further investigated. One of the questions currently under debate concerns the estimation of the gravity vector. Besides the well-known contribution of labyrinthne inputs and vision to monitoring the vertical axis, a putative role of body graviceptors has been suggested in the past [32,33], and this idea has recently been indi-

879

880

Neural

control

rectly supported. By adding loads under water, where the body’s weight is cancelled by the water pressure, or by adding a horizontal force equal to the body weight while the subject is lying down, the previously absent postural reaction to ‘support’ disturbances can be restored. These results argue in favour of the presence of graviceptors distributed among the segments. Which sensors are used to monitor the load? One possible explanation might be that the muscle effort opposing the effects of gravity or other forces may be estimated by the Golgi tendon organs, whose discharge pattern correlates with the number of active motor units [34,35]. U sm . g a d’1ff erent approach, based on a subjective estimation of verticality, Riccio, Martin and Stoffregen [36] reached similar conclusions by artificially dissociating the gravity vector horn the axis of the ground reaction forces that have to be controlled in order to maintain equilibrium. These authors concluded that the subjective vertical depends on both the gravity vector and the direction of the ground reaction forces needed to control balance. Interactions between the orientation of the visual reference frame and somatosensory inputs relating to the body orientation with respect to the vertical in the perceived subjective vertical have also been found to occur by Nemire and Cohen [37], indicating the importance of the trunk axis (idiotropic vector) in the perceived vertical [33]. Under microgravity, the perception of the subjective vertical in the absence of vision may depend on the ‘saccular’ Z bias, that is, on the difference between the mean resting discharges of saccular units polarized in the rostra1 and caudal directions. Other cues - such as tactile, visual and proprioceptive - also play an important role in body orientation under microgravity [38]. One of the most clearly emerging properties of the sensory inputs that contributes to the body scheme is the marked dependence of these inputs on context, particularly on the reference frame used for their analysis (see discussion in DiZio it a/. [39-l). For example, the illusory or effective body sways that result horn artificial Ia inputs produced by vibrating bilaterally the tendon of either the gastrocnemius or tibialis anterior muscle in a standing subject tend to disappear under microgravity [40*]. These ‘postural’ illusions or reactions are therefore gravity-dependent. The role played by vestibular and proprioceptive inputs in human self-motion perception in space also depends on the reference frame. Mergner ETal. [41*], using various combinations of head, trunk and feet rotation, have proposed a model in which the vestibular signal and the proprioceptive input arising along the whole body axis were used to reconstruct the perception of head, trunk and feet position in space. In vestibular patients, the perception of trunk rotation in space with the head free is deficient contrary to normal subjects, indicating that vestibular inputs are normally responsible for this perception [42*]. With the head fixed during trunk rotation, patients perceived an illusory head movement

(due to the nuccal afferents). As soon as a fixed visual or tactile reference frame was used, the same patients with vestibular deficits perceived the real trunk rotation. Similar results were obtained by Guxfinkel and Levik [43-l in normal subjects, using very slow trunk rotations that were not perceived at all with the head f?ee. With the head fixed, illusory head rotation is perceived; whereas when the hand is in contact with a rigid handle fixed to the wall, the real trunk rotation is perceived [43*]. How the proprioceptice input is interpreted by the subject is therefore highly dependent on the reference frame used at the same time. Postural responses are also markedly context-dependent. This is illustrated by the responses induced by labyrinthine stimulation [44*]. A standing subject’s response to galvanic stimulation of the labyrinth consists of a postural sway in the direction of the ear behind which the anode is placed. As previously established, the direction of the sway changes with the head position with respect to the trunk, and that of the trunk with reference to the legs; the direction of sway therefore depends on the body geometry at the time of stimulation. The electrbmyograph (EMG) response associated with the sway (the late component of the response) depends on the support conditions: it occurs in the arm muscles when part of the body support is exerted by the hands, and disappears in the soleus in the sitting subject. It therefore occurs in the muscles that are actively engaged in balance. Moreover, reduced responses were observed when other sources of afferent information are available, for example when the subjects touched a fixed support or when their eyes were open.

Postural reactions Postural reactions are elicited on the basis of sensory signals that indicate a disturbance ofposture and/or equilibrium. Experimental stance disturbances are usually produced by moving the supporting platform. Disturbances restricted to the hip level have also been tested and conpared between normal and hemiparetic patients [45]. Discrete disturbances have usually been used; pseudorandom disturbances have also been tested [46]. The central organization of the postural reactions will not be specifically discussed here (see Jankowska and Edgley [47] on the spinal cord organization). It is worth mentioning however that chronic spinal cats show very poor postural control [48]. One of the emerging ideas about the organization of postural reactions is that the central nervous system is unable to control individual muscles separately and that it controls only a small number of degrees of freedom by activating functional synergies, involving a set of muscles regulated as a whole [49,50]. Synergies have commonly been observed in postural reactions. They appear to be flexible and depend on external constraints such as the

Postural control system Massion

direction of the forces disturbing posture. The bifunctional muscles that extend across two joints contribute largely to this flexibility, because their activity depends more strongly on sensory inputs than the single joint muscles, and they might serve to orient the force vector exerted by the single joint muscles depending on the requirements of the postural task [51*]. It has been suggested by Horak and Nashner [16] that a higher level of organization may be involved in the postural reactions to stance disturbance: at this level strategies are selected that each define a given type of action for restauring balance. Hip strategy (torques and movement at the hip joint), ankle strategy (torques and movement at the ankle joint), and stepping are different ways of restoring balance, depending on the intensity of the balance disturbance and the constraints. The muscle synergy may be a lower level of organization, implementing the strategy by providing the appropriate muscle forces. Recent data tend to show that the strategy level is also flexible and adaptable to task constraints. For example, the hip and ankle strategies are not ‘all or none’ reactions but rather form a continuum under progressively changing external constraints. Horak and Moore [52*] have observed that a continuum occurs in postural changes involving gradually more hip strategy and less ankle strategy when leaning forward is increased. The postural response to stance disturbance is also adapted when a disturbance to equilibrium is used as a signal for gait initiation; in this situation, goal-directed changes in postural responses were found to occur [53]. Conclusions on the same lines were reached by Allum et al. [54-l, who disturbed standing posture by random combinations of rotation (triggering the hip strategy) and translation (triggering the ankle strategy) of a supporting surface. On the basis of kinematic and EMG analysis, they established that one out of two discrete muscle synergies was selected on the basis of leg afferent input. In addition, segmental velocity related inputs continuously update the initial pattern. A comparable updating of the basic pattern by segmental inputs was also reported by Forssberg and Hirschfeld [55-l during disturbance of the sitting position. A dependence on the biomechanical constraints was also found in the case of the ‘force constraint strategy’ observed in the cat, whatever the direction of the stance disturbance [9*,15**]. This strategy does not depend on prior experience and is therefore part of the animal’s repertoire [56]. It is characterized by the fact that the force directions exerted to restore balance under individual paws are always oriented forward and backward whatever the direction of the balance disturbance. This strategy disappears with small interpaw distances. On the basis of a biomechanical analysis, Macpherson and Fung [9*] have proposed that this strategy may be aimed at preventing a lateral bending of the trunk, thus maintaining the back length invariant when lateral disturbing forces are present. With shorter interlimb distances, the back incurvation seems to be prevented by an increase in back stiffiless [9*].

There is also some flexibility in compensatory stepping observed in response to stance disturbance. This response depends on the velocity of the disturbance as well as on the instructions given to the subjects. Aborted reactions are also observed where only the initial weight transfer toward the supporting limb occurs [57,58]. The stepping response is thus composed of several stages, each of which includes a decision made on the basis of sensory cues.

Role of sensory inputs

Some recent investigations have been carried out on the respective roles of the various categories of sensory inputs involved in postural stability. To what extent do the vestibular inputs contribute to the postural reactions to stance disturbance? In cats, with bilateral labyrinthectomy, no change in the force constraint strategy nor in the muscle synergy afier stance disturbance was detected [59]. Hypermetric responses are seen early after the operation. In humans, a special device for producing phasic vestibular linear stimulation by displacing the head was tested. This stimulation induced postural responses in leg and trunk muscles in standing subjects. These responses were rather weak, however, suggesting that vestibular inputs do not contribute strongly to early postural reactions to balance stance disturbances [60*]. The vestibular system plays a role in organizating hip strategy [61]. Imposed ankle joint rotation induces a hip strategy in normal subjects, which disappears in vestibular patients and is replaced by a rather inefficient ankle strategy [54*]. It should also be mentioned that no vestibular deficits were detected in Parkinsonian patients with impaired balance [62], and that, generally speaking, the usual multisensory inputs are properly integrated in these patients [63]: this suggests that the disorder affects only the control of the postural reactions. The role of leg somatosensory inputs in postural stability has also been investigated. For example, longitudinal platform oscillations at 8-24 Hz markedly increased the subjects’ postural instability [64]. The somatosensory inputs are not only involved in postural stability: somatosensory inputs Gem the lower leg also contribute directly to the stabilization of the head as do the visual and vestibular inputs 1651. Are the somatosensory inputs from the leg needed to trigger and scale human automatic postural responses? In patients with lower limb neuropathy, the postural reactions to stance disturbance are still present, but their latency increases (2@3Oms) [66*]. This suggests that leg somatosensory inputs are actually used to trigger and scale the postural reactions; however, other inputs (trunk, vestibular and visual) may replace the missing inputs. How are somatosensory inputs used to scale the postural response in ccrebellar patients [67’]! Interestingly, in patients with anterior lobe pathology, feedback-controlled scaling, depending on the velocity of the disturbance, is

881

882

Neural

control

still possible. In contrast, scaling of the response amplitude, which depends on presetting before the disturbance onset, disappears and is replaced by tendency towards hypermetria. Concerning the role of vision in postural control, it has been shown that postural sway is equally controlled by peripheral and central visual fields [68].The effects of a moving visual environment on postural oscillations have been investigated by Previc et al. [69] and Dijkstra et al. [70]. The latter paper concludes that retinal slip minimization does not explain the coupling between a moving visual environment and postural sway, and that a dynamic coupling between the two must exist. Vision has been found to shorten the latency of postural responses [71]. Vection has been shown to shorten or delay the onset of balance recovery in unexpected forward falls, depending on the direction of the moving scene [72]. Lastly, the respective roles of the somatosensory and visual inputs in stabilizating body motion depend on the stance width. With a larger supporting base, the role of vision in body stabilization in the frontal plane decreases in favor of somatosensory inputs [ll]. Visual motion compensates in the cat for loss of vestibular input during the early stages of recovery after unilateral labyrinthectomy. The vestibular nucleus response to optokinetic stimuli on the deafferented side shows an increased band width [73].

Anticipatory

postural adjustments

Unlike the postural reactions in response to the onset of posture or balance disturbances, the anticipatory postural adjustments precede the disturbance onset and therefore minimize the effects of the forthcoming disturbance in a feedforward manner. Anticipatory postural adjustments usually occur in association with voluntary movements, which are one of the main sources of posture and balance disturbance. Anticipatory adjustments can also be observed, however, when imposed disturbance is recurrent, as in the case of human stance on a sinusoidally translating platform. The anticipatory adjustments which are then observed serve to orient the body so as to minimize the effects of gravitoinertial forces. When the frequency of the platform translation is changed, the feedforward mode is replaced by a feedback mode of control for a few oscillations and the feedforward control then reappears [74’]. This anticipatory postural control is impaired in Parkinsonian patients [75]. Anticipatory postural adjustments before the disturbance of a single joint position caused by the voluntary movement of another segment have been described. For example, when a subject is tapping with a hammer on the radial muscle of his other forearm, there is a silent period in the muscle response pattern before the actual me-

chanical impact. This inhibition may minimize impact effect on forearm posture by reducing muscle stiffness in advance of the disturbance [76]. The mechanisms responsible for anticipatory postural adjustments have been investigated. In a bimanual load lifting task, where one arm was supporting the load and the other voluntary lifting the load, anticipatory postural adjustments were observed in the postural arm (see [77]). Interestingly, the sarne adjustments were observed in a patient with forearm-afferent deprivation, indicating that these adjustments result from feedforward control. The limb afferents are necessary, however, for new anticipatory postural adjustrnent when unloading the postural forearm is triggered by new movement [78]. Anticipatory postural adjustments aimed at maintaining balance have been observed with upper trunk movements (see [77]). These adjustments are impaired in cerebellar anterior lobe patients; the main deficit involves a lack of feedforward activation in the thigh muscles at the onset of the movement [79]. Respiratory oscillations can also lead to balance disturbance. As the respiratory oscillation estimated from the center of pressure sway path recorded from a force platform is larger in sitting than in standing subjects, anticipatory control seems to be more efficient when standing than when sitting [80]. The last specific type of postural adjustment occurs with movements involving the legs, such as gait initiation, standing on tip toe or the heels and lifting or raising a leg. With motor acts of this kind, the movement is preceded by postural changes that shift the CG toward a new position compatible with equilibrium maintenance during the leg movement. These types ofpostural adjustments are impaired in patients with hemiparesis. When asked to lift a leg, they are not able to use the paralyzed limb to exert the appropriate horizontal ground reaction forces needed to move the CG toward the supporting leg [81]. When asked to stand on tip toe, the temporal sequence is disturbed on both sides [82]. Standing on tip toe is also markedly impaired in anterior lobe cerebellar patients [83] and Parkinsonian [84]. The scaling of the amplitude and duration of the preparatory postural phase is abnormal in cerebellar patient (low amplitude, prolonged duration) and the temporal relationship between the postural and movement phase is lost.

Age-related

changes

Ontogenesis

Successive steps have been described during the development of posture: postural control of the head, postural control of the trunk, sitting position, standing and locomotion. The emergence of these various stages depends on the evolutional state of several systems, such as the musculo-skeletal system, the sensori-motor system, the level of motivation and of behavioral development, and the internal and environmental constraints [85].

Postural control

Both the visual and somatosensory systems are crucial for stabilization of head, trunk and whole body posture, but vision is effective earlier than the somatosensory system. At each stage in postural development, moving visual information contributes to maintaining posture and equilibrium. It has been established that vision and optic flow influence spontaneous head oscillation as early as 2 to 3 days after birth, and head posture as early as 5 months of age [86]. A response to optic flow occurs with a supported standing posture as early as 5 months of age and increases considerably later on. The somatosensory system is mainly involved in reactions to support disturbances. Head stabilization is observed from 3 to 4 months of age and head-trunk stabilization in sitting posture at 5 months [87]. Hirschfeld and Forssberg [88*] have observed that in sitting children who undergo a forward horizontal balance disturbance, the EMG pattern is roughly comparable to the adult one [55*], since the activation of the front muscles induced by backward trunk imposed displacement is similar to what occurs in adults, although this is not so in the case of the back muscles. These authors suggested that two levels of control might exist: basic one present in children, and that which develops in adults as the result of learning. At 9 months of age, the classical distal-proximal EMG pattern present in adults subjects to platform disturbances is present in standing children. It is preceded by a stage where only the ankle joint muscles are activated and standing without support is not possible [89,90]. The vestibular contribution to postural reactions has turned out to be apparently less important than the somatosensory one early in life, but further investigations will be necessary to elucidate this point. Special attention has been paid to equilibrium control during locomotion. As soon as locomotion starts, stabilization of the hip in the frontal plane with respect to space is observed [91*,92]. After two months of walking experience, stabilization of the shoulders improves. This suggest that a hip-centered temporal organization of balance control occurs while walking. Long-term maturation of locomotor balance has also been investigated. During the first stage (3-6 years), the head is stabilized on the trunk whenever constraints makes equilibrium difficult. By 7-8 years, the head is also stabilized in space during locomotion when facing equilibrium constraints. Adults use similar stabilization of the head in the frontal plane while walking on a narrow support (see [85]). Does the head stabilization in space depend on visual inputs or is it based on vestibular cues? Although peripheral vision and movement visual cues play an important part in balance control, especially in young children, head stabilization in space does not depend to any great extent on visual cues and may therefore mostly depend on vestibular cues [20]. Head stabilization in space in children as in adults [93] is a basis for ‘top-down’ postural control on basis of visual and vestibular cues.

system

Massion

Ageing

The balance deficits that occur with ageing have been extensively studied over recent years. Authors of three recent papers [94-961 have emphasized the multiple sources of balance deficits in the elderly and the need to adopt a systemic approach. For example, sensory receptors deteriorate with ageing. Sensory deprivation or sensory conflicts have more drastic effects on balance in the elderly than in younger subjects [97]. Mechanical properties of the tendons and muscles are also affected in terms of their force and elasticity. Postural responses are delayed and weaker with more co-activation in the elderly [98]. Ability to adapt changing external perturbations such as shifting from a translation to a rotational disturbance is impaired. Postural responses associated with voluntary movements are also impaired (increased latenties, excessive co-contractions, etc.) [99]. Furthermore, the attentional demands of postural tasks are increased in the elderly [loo]. Generally speaking, the impairment of balance that develops in the elderly results from the degradation of multiple systems that participate, either directly or indirectly, in the task of balance control.

Conclusions The overall picture of postural organization that emerges horn recent investigations is a long way off the picture of classical postural reflexes presented by the Sherringtonian School. While the old description of these reflexes is still valid and their analysis is still a useful means of experimentation and neurological evaluation, the enphasis now is on the flexibility of postural control and its adaptability to different contexts. Such flexibility is reflected in the multisensory integration which is involved in postural orientation and stabilization. The multisensory aspect of postural control was first pointed out as early phylogenetically as in the lamprey [lOl*], but its ability to adapt to context and task is characteristic of higher vertebrates. This explains the large range of compensatory possibilities available in the case of selective sensory deficits, and also the fact that a given sensory input can induce various perceptions or postural reactions, depending on the reference frame selected and the external constraints such as gravity This flexibility is under the control of the internal representation of the body or postural body scheme, which remains quite stable under changing conditions. Postural reactions show a similar degree of flexibility. Some invariant aspects of postural reactions, such as strategies and synergies, appear to be less fixed than was first thought to be the case, and change depending on the constraints. The external constraints, as well as the biomechanical properties of the body segments, impose choice of control. One of the main criteria for the emergence of a postural pattern after training is that

883

884

Neural

control

it should be as economical as possible in terms of energy consumption. This does not mean that the brain is merely a passive player in the game. Its role is to utilize passive forces to organize the most suitable spatiotemporal pattern in order to carry out a task. It plays a crucial role in coordinating postural tasks with various aspects of the ongoing action. The coordination between posture, equilibrium and movement is certainly one of the main functions of the postural control system.

lenburg DJ, Harris FP, Probst R. Amsterdam: Elsevier Science Publishers B.V.; 1993:349-358. The authors proposed a theoretical framework for studying coordination strategies in standing posture. This framework consists of a musculoskeletal model of human lower extremity in the sag&al plane and a technique to visualize, geometrically, how constraints internal and external to the body affect the movement. The model predicts that the hip strategy is most effective at controlling the center of mass with minimal muscle activation.

Acknowledgements

10.

The author wish to thank S Zakarian for the very efficient help in the preparation of this review paper, and F Horak and J Macpherson for their critical reading of the manuscript. The CNES (Centre National d’etudes Spatiales) is acknowledged for

Lee WA, Russo AM: Constraints and coordination in wholebody actions. In lnterlimb coordination: neural, dynamical, and cognitive constrainfs. Edited by Swinnen S, Heuer Ii, Massion J, Casaer P. San Diego: Academic Press; 1994537-569.

11.

Day BL, Steiger MJ, Thompson PD, Marsden CD: Effect of vision and stance width on human body motion when standing: implications for afferent control of lateral sway. J Physiol (Londl 1993, 469:479-499.

12.

Merfeld DM, Young LR, Oman CM, Shelhamer MJ: A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J Vest Res 1993, 3:141-161.

13.

Lacquaniti F: Automatic control of limb movement ture. Curr Opin Neurobiol 1992, 2:807-814.

9. .

Fung J, Macpherson JM: Determinants of postural orientation in quadrupedal stance. J Neurosci 1994, in press. The determinants of postural orientation in the standing cat were investigated by examining stance kinematics and kinetics at various interpaw distances. The authors show that the trunk orientation is kept constant due to maintaining a constant intralimb geometry.

its support.

References and recommended

reading

Papers of particular interest, published within review, have been highlighted as: . of special interest .. of outstanding interest

the annual period of

and pos-

1.

Carroll JP, Freedman W: Nonstationary sway. ) Biomech 1993, 26:409-416.

2.

Newell KM, Van Emmerik REA, Lee D, Sprague RL: On postural stability and variability. Cair & Posture 1993, 4:225-230.

Lacquaniti F, Maioli C: Independent control of limb position and contact forces in cat posture. / Neurophysiol 1994, 72:1476-l 495. The main aim of this study was to assess whether or not control of limb position in the standing cat is independent of control of contact forces at the feet. By tilting the support surface, changing interfeet distance and head orientation, or by adding a load to the back, the authors showed that two independent controls do exist, one addressed to limb length and orientation, the other to the lever component oftangential contact forces.

3. .

Collins JJ, De Luca CJ: Open-loop and closed-loop control of posture: a random-walk analysis of center of pressure trajectory. Exp Brain Res 1993, 95:308-318. The center of pressure trajectories during quiet stance (steady states behavior) are modelled as fractional Brownian motion. This analysis reveals two modes of postural control: open loop and feedback.

Macpherson JM: Changes in a postural strategy with inter-paw 15. .. distance. J Neurophysiol 1994, 71:931-940. The postural strategy during stance disturbance in the cat is characterized by a forward or backward orientation of the ground reaction forces. This strategy is lost for short interlimb distance. The author suggests that the strategy is aimed at controlling the back orientation.

4. .

Amblard 8, Assaiante C, Lekhel H, Marchand A: A statistical approach to somatosensorimotor strategies: conjugate crosscorrelations. / Motor Behav 1994, 26: 103-l 12. A method based on cross-correlation function between two time series of kinematic measurements is proposed for the analysis of multisegmental movements. It can be used for defining postural strategies during stance.

16.

Horak FB, Nashner LM: Central programming of postural movements: adaptation to altered support surface configurations. / Neurophysiol 1986, 55: 1369-l 381.

17.

Babinski J: De 7:806-816.

5.

18.

Massion J, Curfinkel V, Lipshits M, Obadia A, Popov K: Axial synergies under microgravity conditions. J Vestibular Res 1993, 3~275-287.

19.

Berthoz A, Pozzo T: Head and body coordination during locomotion and complex movements. In Interlimb coordination: neural, dynamical, and cognitive constraints. Edited by Swinnen S, Heuer H, Massion J, Casaer P. San Diego: Academic Press; 1994: 147-l 65.

20.

Assaiante C, Amblard B: Ontogenesis of head stabilization in space during locomotion in children: influence of visual cues. Exp Brain Res 1993, 93:499-515.

21.

Andersen RA, Snyder LH, Li CS, Stricanne 6: Coordinate transformations in the representation of spatial information. Curr Opin Neurobiol 1993, 3:171-l 76.

properties

of postural

Allum JHJ, Honegger F: Synergies and strategies underlying normal and vestibulary deficient control of balance: implication for neuroprosthetic control. In Progress in brain research, vol 97. Edited by Allurn JHJ, Allum-Mecklenburg DJ, Harris FP, Probst R. Amsterdam: Elsevier Science Publishers B.V.; 1993:33 l-348.

14. ..

6. .

Lacquaniti F, Maioli C: Coordinate transformations in the control of cat posture. / Neuro,ohysio/ 1994, 72: 1496-l 515. The authors have tested a number of different hypotheses on the nature of the processing stage that transforms end point coordinates of the limbs specified by limb length and orientation into the angular coordinates of the joints (inverse mapping). 7. .

Alexandrov A, Frolov A, Massion J: Voluntary forward bending movement in human: a principal component analysis of axial synergies. In Vestibular and neural iron&. Edited by Taguchi K, Igarashi M, Mozi S. Amsterdam: Elsevier; 1994:345-348. Principal component analysis was used to determine the intersegmentat constraints during upper trunk movement. A single component (PClJ fixes the ratio of angle changes, and the amplitude and time course of the movement. 8. .

Kuo AD, Zajac FE: Human standing posture: multi-joint movement strategies based on biomechanical constraints. In Progress in brain research, vol 97. Edited by Allum JHJ, Allum-Meck-

I’asynergie

c&+belleuse.

Rev Neural

1899,

Mackinnon CD, Winter DA: Control of whole body balance in the frontal plane during human walking. / Biomechanics 1993, 26:633-644. The authors use a whole-body inverted pendulum model to investigate control of balance and posture in the frontal plane during human walking.

22. .

23.

Winter DA, Mackinnon CD, tegrated EMC/biomechanical

Ruder CK, Wieman C: An inmodel of upper body balance

Postural control and posture during human gait. In Progress in brain research, vol 97. Edited by Allum JHJ, Allum-Mecklenburg DJ, Harris FP, Probst R. Amsterdam: Elsevier Science Publishers B.V.; 1993:359-367. 24.

25.

Glasauer S, Amorim MA, Vitte E, Berthoz A: Coal-directed linear locomotion in normal and labyrinthine-defective subjects. Exp Brain Res 1994, 98:323-335. Mouchnino L, Aurenty R, Massion J, Pedotti A: Coordination between equilibrium and head-trunk orientation during leg movement: a new strategy built up by training. / Neurophysiol 1992, 67:1587-l 598.

Mouchnino L, Aurenty R, Massion J, Pedotti A: Is the trunk a reference frame for calculating leg position? Neuroreporf 1993, 4:125-l 27. By comparing leg angle with respect to trunk during leg raising in dancers (keepingthe trunk axis vertical) and untrained subjects (trunk inclination). The authors concluded that leg position is estimated with respect to the trunk axis. 26. .

27.

Curfinkel VS: The mechanisms of postural regulation in man. Soviet Scientific Reviews F Phys Gen Biol 1994, 7:59-89.

Fisk j, Lackner JR, Dizio P: Gravitoinertial force level influences arm movement control. / Neurophysiol 1993, 69:504-511. The ability to move the forearm between remembered elbow joint angle after rapid changes of the gravitoinertial forces (G) level was measured. C changes only influenced the movement amplitude for slow movements that rely on proprioceptive information, suggesting a decrease of spindle activity in 0 C. 28. .

29.

Curfinkel VS, Lestienne F, Levik YuS, Popov KE: Egocentric references and human spatial orientation in microgravity. I. Perception of complex tactile stimuli. Exp Brain Res 1993, 95:339-342.

30.

Curfinkel VS, Lestienne F, Levik YuS, Popov KE, Lefort L: Egocentric references and human spatial orientation in microgravity. II. Body-centred coordinates in the task of drawing ellipses with prescribed orientation. Fxp Brain Res 1993, 95:343-348.

31.

Young LR, Oman CM, Merfeld D, Watt D, Roy S, Deluca C, Balkwill D, Christie J, Groleau N, Jackson DK ef al.: Spatial orientation and posture during and following weightlessness: human experiments on spacelab life sciences 1. / Vestibular Res 1993, 3:231-239.

32.

Gurfinkel VS, Lipshits YuS, Popov KE: Stabilization of body position as the main task of postural regulation. Fiziologya Cheloveka 1981, 7:40&410.

33.

Mittelstaedt H: A new solution to the problem of the subjective vertical. Nafurwissenschaften 1983, 70:272-281.

34.

Dietz V: Neuronal basis of stance regulation. Interlimb coordination and antigravity receptor function. In lnferlimb coordination: neural, dynamical, and cognifive constraints. Edited by Swinnen SP, Heuer H, Massion J, Casaer P. New York: Academic Press; 1994:167-l 78.

35.

Dietz V, Gollhofer A, Kleiber M, Trippel M: Regulation of bipedal stance: dependency on ‘load’ receptors. Exp Brain Res 1992, 89:229-231.

36.

Riccio GE, Martin El, Stoffregen T: The role of balance dynamics in the active perception of orientation. / Exp Psycho/ (HPPJ 1992, 18~624-644.

37.

Nemire K, Cohen MM: Visual and somesthetic influences on postural orientation in the median plane. Perception 8. Psychophysics 1993, 53:106-l 16.

38.

Mittelstaedt H, Glasauer S: Crucial effects of weightlessness on human orientation. / Vesfibular Res 1993, 3:307-314.

Dizio P, Lathan CE, Lackner JR: The role of brachial muscle spindle signals in assignment of visual direction. / Neurophysiol 1993, 70:1578-l 584. The illusion of target light displacement (oculobrachial illusion) is perceived when a target light is attached to the unseen stationary hand and an illusory forearm motion is elicited by brachial muscle vibration. When two targets are fixed, one on each hand, and both biceps 39. .

system Massion

vibrated simulatneously, the perceived distance between the targets increases significantly. These findings indicate that brachial muscle spindle signals can contribute to an independent representation of felt target location in head-centric coordinates. The authors propose a model of these representations. 40. .

Roll JP, Popov K, Gurfinkel V, Lipshits M, Andre-Deshays C, Gilhodes JC, Quoniam C: Sensorimotor and perceptual function of muscle proprioception in microgravity. 1 Vesfibular Res 1993, 3:259-273. During long-term exposure to microgravity, the postural responses or the illusory postural displacements induced by vibratory stimulation of Tibialis anterior or Gastrocnemius tendons are reduced or disappear and are replaced by body lift illusion. They reappear by artificially increasing the foot support by means of braces.

41. Mergner T, Hlavacka F, Schweigart G: Interaction of vestibular . and proprioceptive inputs. / Vestibular Res 1993, 3:41-57. The study investigates the interaction of leg proprioceptive and vestibular affe’rents for human self perception in space. 42. .

Schweigart G, Heimbrand S, Mergner T, Becker W: Perception of horizontal head and trunk rotation: modification of neck input following loss of vestibular function. Exp Brain Res 1993, 95:533-546. The horizontal head and trunk rotation perception is investigated in patients with chronic vestibular loss. In these patients, the trunk rotation with respect to a stationary head is perceived as a rotation of the head with respect to a stationary trunk. The normal perception is restored when visual or somatosensory space reference is presented.

43. .

Gurfinkel VS, Levik YuS: The suppression of the cervico-ocular response by the haptokinetic information about the contact with a rigid, immobile object. Fxp Brain Res 1993, 95:359-364. Super slow trunk rotation with respect to a stationary head is perceived as a head rotation with respect to a stationary trunk. Eye movements in phase with the illusory head rotation are seen. Grasping a rigid handle (haptic contact) restores perception of trunk rotation with respect to the head. 44. .

Britton TC, Day BL, Brown P, Rothwell JC, Thompson PD, Marsden CD: Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Fxp Brain Res 1993, 94:143-151. The effect of galvanic vestibular stimulation in man depends on support conditions (feet, hands). Early and late EMG responses are described, which are computed independently. 45.

Wing AM, Goodrich S, Virji-Babul N, Jenner JR, Clapp S: Balance evaluation in hemiparetic stroke patients using lateral forces applied to the hip. Arch Phys Med Rehabil 1993, 74:292-299.

46.

Maki BE, Ostrovski G: Do postural responses to transient and continuous perturbations show similar vision and amplitude dependence? / Biomech 1993, 26: 1181-l 190.

47.

Jankowska E, Edgley S: Interaction between pathways controlling posture and gait at the level of spinal interneurones. in Progress in brain research, vol 97. Edited by Allum JHJ. AllumMecklenburg DJ, Harris FP, Probst R. Amsterdam: Elsevier Srience Publishers B.V.; 1993:161-l 71.

48.

Pratt CA, Fung J, Macpherson JM: Stance control in the chronic spinal cat. J Neurophysiol 1994, 71:1981-1985.

49.

Bernstein N: The coordination and regulafion London: Pergamon Press; 1967.

50.

Macpherson JM: How flexible are muscle synergies? In Mofor control: concepts and issues. Edited by Humphrey DR, Freund H-J. Chichester: John Wiley & Sons; 1991:33-47.

oi movemenf.

Van lngen Schenau GJ, Pratt CA, Marpherson JM: Differential use and control of mono- and biarticular muscles. Human MOV Sci 1994, In press. The respective role of mono- and biarticular muscles In multIJoIn’s movements is analyzed in various tasks, in cat and human. As a whole, the bialticular muscle activity is more flexible under the influence of motionrelated feedback and aimed at fine regulation of the distribution of net moments over the limb joints.

51. .

52. .

Horak FB, Moore SP: The effect of prior leaning on human postural responses. C;ait & Posfure 1993, 1:203-210.

885

886

Neural

control

This study examines how human postural responses to stance disturbance are altered by leaning about the ankles to five different initial stance POsitions. 53.

normal subjects. The main deficit was the lack of anticipatory scaling of the amplitude of the responses. 68.

Straube A, Krafczyk S, Paulus W, Brandt T: Dependence of visual stabilization of postural sway on the cortical magnification factor of restricted visual fields. Exp Brain Res 1994, 99:501-506.

69.

Previc FH, Kenyon RV, Boer ER, Johnson BH: The effects of background visual roll stimulation on postural and manual control and self-motion perception. Perception & Psychophysics 1993, 54:93-l 07.

70.

Dijkstra TMH, Schoner C, Cielen CUM: Temporal stability of the action-perception cycle for postural control in a moving visual environment. Exp Brain Res 1994, 97:477-486.

71.

Timmann D, Belting C, Schwarz M, Diener HC: Influence of visual and somatosensory input on leg EMG responses in dynamic posturography in normals. Electroencephalogr C/in Neurophysiol 1994, 93:7-l 4.

72.

Hoshiyama M, Watanabe S, Kaneoke Y, Koike Y, Takahashi A: Effecl of optokinetic stimulation on human balance recovery in unexpected forward fall. Neurosci Res 1993, l&121-127.

73.

Zennou-Azogui Y, Xerri C, Harlay F: Visual sensory substitution in vestibular compensation: neuronal substrates in the alert cat. Exp Brain Res 1994, 98:457-473.

Burleigh AL, Horak FB, Malouin F: Modification of postural responses and step initiation: evidence for goal directed postural interactions. J Neurophysiol 1994, in press.

Allum JHJ, Honegger F, Schicks H: Vestibular and proprioceptive modulation of postural synergies in normal subjects. J Vestibular Res 1993, 3:59-85. The different muscle synergies underlying human balance control were tested by combining rotation and translation of the support surface. 54. .

Forssberg H, Hirschfeld H: Postural adjustments in sitting humans following external perturbations: muscle activity and kinematics. Exp Braain Res 1994, 97:515-527. Translation and rotation disturbances were tested in sitting subjects. The results suggest that two levels of control can be identified: first, a pattern of muscle activation is generated centrally, and second, the pattern is shaped and timed by interaction from the entire somatosensory, vestibular and visual input. 55. .

56.

Macpherson JM: The force constraint strategy for stance is independent of prior experience. Exp Brain Res 1994, 101:397-405.

57.

Mcllroy WE, Maki BE: Task constraints on foot movements and the incidence of compensatory stepping following perturbation of upright stance. Brain Res 1993, 616:30-38.

58.

Maki BE, Whitelaw RS, Mcllroy WE: Does frontal-plane asymmetry in compensatory postural responses represent preparation for stepping? Neurosci Lett 1993, 149:87-90.

59.

Macpherson JM, lnglis JT: Stance and balance following bilateral labyrinthectomy. In Progress in brain research, vol 97. Edited by Allum JHJ, Allum-Mecklenburg DJ, Harris FP, Probst R. Amsterdam: Elsevier Science Publishers B.V.; 1993:219-228.

Horak FB, Shupert CL, Dietz V, Horstmann C: Vestibular and somatosensory contributions to responses to head and body displacements in stance. Exp Brain Res 1994, 100:93-l 06. The relative contribution of vestibular and somatosensory information to triggering postural responses to external body displacements was investigated by comparing responses to displacements of the head alone with responses to displacement of head and body, in healthy subjects and patients with vestibular deficits. 60. .

61.

Horak FB, Nashner LM, Diener HC: Postural synergies associated with somatosensory and vestibular loss. Exp Brain Res 1990, 82:167-l 77.

62.

Pastor MA, Day BL, Marsden CD: Vestibular induced postural responses in Parkinson’s disease. Brain 1993, 116:1177-l 190.

63.

Wasterton )A, Hawken MB, Tanyeri S, Jantti P, Kennard C: Influence of sensory manipulation on postural control in Parkinson’s disease. J Neural Neurosurg Psychiatry 1993, 56:1276-1281.

Dietz V, Trippel M, lbrahim IK, Berger W: Human stance on a sinusoidally translating platform: balance control by feedforward and feedback mechanisms. Exp Brain Res 1923, 93:352-362. Body inclination and EMC activity was tested in subjects standing on a treadmill moving sinusoidally backward and forward. Both feedback reactions to changes in sinusoidal frequency and feedforward control during repeated cycles at the same frequency were analyzed. The authors conclude that feedforward control acts on CC position relative to the feet in order to minimize forces acting on the body during treadmill movement. 74. .

75.

Dietz V, Zijlstra W, Assaiante C, Tripple M, Berger W: Balance control in Parkinson’s disease. Gait & Posture 1993, 1:77-84.

76.

Struppler A, Gerilovsky L, Jakob C: Self-generated rapid taps directed to opposite forearm in man: anticipatory reduction in the muscle activity of the target arm. Neurosci Lett 1993, 159:115-118.

77.

Massion J: Movement, posture and equilibrium: interaction and coordination. Progress Neurobiol 1992, 38:35-56.

78.

Forget R, Lamarre Y: Postural adjustments associated with different unloading of the forearm: effects of proprioceptive and cutaneous afferent deprivation. Can J Pbysiol Pharmacol 1994, in press.

79.

Viallet F, Massion J, Bonnefoi-Kyriacou B, Aurenty R, Obadia A, Khalil R: Approche quantitative de I’asynergie posturale en pathologie cMbelleuse. Rev Neural 1994, 150:55-60.

64.

Pyykko I, Aalto H, Starck J, lshizaki H: Postural stabilization on a moving platform oscillating at high frequencies. Aviat Space Environ Med 1993,64:300-305.

80.

Bouisset S, Duchene JL: Is body balance more perturbated by respiration in seating than in standing posture! Neuroreport 1994, 5:957-960.

65.

Di Fabio RP, Anderson JH: Effect of sway-referenced visual and somatosensory inputs on human head movement and postural patterns during stance. J Vestibular Res 1993, 3:409-417.

81.

Rogers MW, Hedman LD, Pai YC: Kinetic analysis of dynamic transitions in stance support accompanying voluntary leg flexion movements in hemiparetic adults. Arch Phys Med Rehabil 1993, 74:19-25.

82.

Diener HC, Bather M, Guschlbauer B, Thomas C, Dichgans J: The coordination of posture and voluntary movement in patients with hemiparesis. J Neural 1993, 240:161-167.

83.

Diener HC, Dichgans J, Guschlbauer 8, Bather M, Rapp H, Klockgether T: The coordination of posture and voluntary movement in patients with cerebellar dysfunction. Mov Dis 1992, 7:14-22.

84.

Horak F, Frank J: Three separate postural systems affected in Parkinsonism. In Motor control VII. Edited by Stuart DC, Cantcher GN, Curfinkal VS, Wiesendangez M. Tucson, Arizona: Motor Control Press; in press.

85.

Woollacott M, Assaiante C, Amblard B: Development of balance and gait control. In Clinical aspects oi balance and gait

lnglis IT, Horak FB, Shupert CL, Jones-Rycewicz C: The importance of somatosensory information in triggering and scaling automatic postural responses in humans. fxp Brain Res 1994, 100:159-164. The role of lower limb somatosensory information in triggering and scaling the postural responses in patients with sensory peripheral neuropathy was tested. The postural response was delayed by 20-30ms and the scaling of the response to both velocity and amplitude of surface translation impaired. The lower limb sensory afferents play a role in both triggering and scaling the postural responses.

66. .

Horak FB, Diener HC: Cerebellar control of postural scaling 67. . and central set in stance. J Neurophysiol 1994, in press. The scaling of the automatic postural response was studied in patients with anterior cerebellar deficits. Although the responses were hypermetric, the earliest postural responses were scaled to platform velocity as

Postural disorders. Edited by Bronstein A, Brandt T, Wooliacott M. City?: Arnold Publ; 1994, in press. 86.

87.

Jouen F: Head position and posture in newborn infants. In The head-neck sensory-motor system. Vol 7: Evolution, biomechanits and basic aspects. Edited by Berthoz A, Graf W, Vidal PP. Chichester: John Wiley; 1994, in press. Woollacott MH, Sveistrup H: The development of sensorimotor integration underlying posture control in infants during the transition to independent stance. In hterlimb coordination: neural, dynamical, and cognitive constrain&. Edited by Swinnen S, Heuer H, Massion J, Casaer P. San Diego: Academic Press; 1994:371-389.

aa. .

Hirschfeld H, Forssberg H: Epigenetic development of postural responses for sitting during infancy. Exp Brain Res 1994, 97:52a-540. The ontogenesis of the postural reactions to platform translation is analyzed in sitting toddlers. 89.

90.

Sveistrup H, Woollacott MH: Systems contributing to emergence and maturation of stability in postural development. In The development of coordination in infancy. Edited by Savelsbergh GJP. Amsterdam: Elsevier; 1993:319-336. Woollacott MH, Sveistrup H: Changes in the sequencing and timing of muscle response coordination associated with devel.. opmental transItIons in balance abilities. Human Movement Science 1992, 11:23-36.

Assaiante C, Thomachot B, Aurenty R: Hip stabilization and lateral balance control in toddlers during the first four months of autonomous walking. Neuroreport 1993, 4:875-878. The stabilization on hip, shoulder and head is analyzed during the first four months of autonomous walking in toddlers. 91. .

92.

Breniere Y, Bril B, Fontaine R: Analysis of the transition from upright stance to steady state locomotion in children with under 200 days of autonomous walking. / Motor Behav 1989, 21:20-37.

control

system Massion

93.

Pozzo T, Berthoz A, Lefort L, Vitte E: Head stabilization during various locomotor tasks in humans. II. Patients with bilateral peripheral vestibular deficits. Exp Brain Res 1991, 85:208-2 17.

94.

Woollacott MH: Age-related changes in posture ment. / Gerontology 1993, 48:5&60.

95.

Alexander NB: Postural control 50~ i 994, 42:93-i 08.

96.

Horak FB, Shupert CL, Mirka A: Components of postural dyscontrol in the elderly: a review. Neurobiol Aging 1989, io:727-738.

97.

Whipple R, Wolfson L, Derby C, Singh D, Tobin I: Altered sensory function and balance in older persons. / Geronrology 1993, 48:71-76.

98.

Keshner EA, Allum JHJ, Honegger F: Predictors of less stable postural responses to support surface rotation in healthy human elderly. / Vestibular Res 1993, 3:419-429.

99.

Maki BE: Biomechanical approach to quantifying anticipatory postural adjustments in the elderly. Med Go/ Eng Comput 1993, 31:355-362.

100.

Teasdale N, Bard C, Larue J, Fleury M: On the cognitive penetrability of posture control. Exp Aging Res 1993, 19:1-13.

and move-

in older adults. / Am Geriat

101. .

Deliagina TG, Grillner S, Orlovsky CN, Ullen F: visual input affects the response to roll in reticulospinal neurons of the lamprey. Exp Brain Res 1993, 95:421-428. The role of visual input in body orientation and on reticulospinal neurons activity is investigated in the lamprey.

J Massion,

31, Chemin

Laboratory

Joseph

of Neurobiolob? and Movements, CNRS Aiguier, 13402 Marseille Cedrx 20, France.

887