NEURAL PLASTICITY VOLUME 12, NO. 2-3, 2005

Development of Postural Control in Healthy Children:A Functional Approach

Christine Assaiante, Sophie Mallau, S6bastien Viel, Marianne Jover and Christina Schmitz

DPA Group, UMR 6196, CNRS, 31 Chemin Joseph Aiguier 13402 Marseille, Cedex 20 France

SUMMARY

From a set of experimental studies showinghow intersegmental coordination developsduring childhood in various posturokinetic tasks,we have established a repertoire of equilibriumstrategies in the course of ontogenesis. Theexperimental data demonstrate that the firstreference frame used for the organization ofbalance control during locomotion is the pelvis,especially in young children. Head stabilization

during posturokinetic activities, particularlylocomotion, constitutes a complex motor skill

requiring a long time to develop duringchildhood. When studying the emergence ofpostural strategies, it is essential to distinguishbetween results that can be explained bybiomechanical reasons strictly and thosereflecting the maturation of the central nervoussystem (CNS). To address this problem, we havestudied our young subjects in situations

requiring various types of adaptation. Thestudies dealing with adaptation of posturalstrategies aimed at testing short and long-termadaptation capacity of the CNS during imposedtransient external biomechanical constraints in

healthy children, and during chronic internal

constraints in children with skeletal pathologies.In addition to maintenance of balance, anotherfunction of posture is to ensure the orientation of

Reprint requests to: Christine Assaiante, DPA Group,UMR 6196,CNRS, 31 Chemin Joseph Aiguier 13402Marseille, Cedex 20 France; e-mail: christine.assaiante@dpm.cnrs-mrs.fr

a body segment. It appears that the control oforientation and the control of balance bothrequire the trunk as an initial reference frameinvolving a development from egocentric toexocentric postural control. It is concluded thatthe first step for children consists in building arepertoire of postural strategies, and the secondstep consists in learning to select the mostappropriate postural strategy, depending on theability to anticipate the consequence of themovement in order to maintain balance controland the efficiency of the task.

KEYWORDS

human development, balance strategies, segmentalstabilization, orientation, adaptation

INTRODUCTION

Postural control is integral to the execution ofgoal-directed action. The most important functionof posture is to ensure the maintenance ofequilibrium during the initiation and continuationof movement. In addition, posture serves as areference frame for the production of accuratemovements. Therefore, postura! strategies have to

be adapted to various contexts and environments.Our contribution to this field lies in a functionalapproach to motor development. This functionalapproach involves a gradual mastering of coordi-

nation, anticipation, and adaptation in posturalcontrol in the course of ontogenesis, from babies

(C) 2005 Freund & Pettman, U.K. 109

11o C. ASSAIANTE ET AL.

to teenagers (Assaiante, 2000).According to their ontogenetic model of

balance control, Assaiante and Amblard (1995)assumed that the various balance strategiesadopted by children, as well as by adults, involvetaking into account two main functional principlesof spatial organization. The first concerns thechoice of the stable reference frame on which theequilibrium control is based, and the secondconcerns the gradual mastery of the degrees offreedom of the various body joints. The choice ofthe stabilized anatomical segment of reference, aswell as the character of coupling betweenarticulations, depends on (a) the dynamicconstraints determining the difficulty of a motortask, (b) the environment, and (c) the character-istics of each developmental period.

In many posturokinetic activities, the contactwith the support is intermittent. During locomotion,for example, the lower limbs cannot serve as astable reference frame for the organization of thewhole-body balance. Thus, it is necessary tostabilize, at least one anatomical segment, whichthen constitutes the reference value around whichmovements can be built up. The reference framecan be either the pelvis to allow a better control ofthe center of gravity or the head to allow clearvision and better visual and vestibular processing,or both segments, according to the difficulty of thetask. Moreover, human stance involves super-imposed modules from the feet to the head, eachwith its own specific central and peripheralregulation, which can be controlled more or lessindependently (Gurkinkel et al., 1971; Massion,1992). Classically, two modes of control are

possible. The "en bloc" strategy consists ofminimizing the number of degrees of freedom tobe controlled simultaneously during the movement,according to Bernstein’s theory (1967). The"articulated" strategy consists of controllingindependently a couple of consecutive anatomicalsegments and requires the mastery of the degreesof freedom ofthe corresponding joint.

The various balance strategies also involve

taking into account two main functional principlesof temporal organization (Assaiante & Amblard,1995). These authors assumed that the stabilizedanatomical segment constitutes the origin of thetemporal organization of balance control. Segmentsare involved in movement in an ascending or

descending sequence, depending upon the anatom-ical segment that serves as the reference frame.For example, on a standing task on a stable supportsurface, the balance control is organized from thefeet to the head, in ascending order. In contrast, ina more dynamic situation, as walking on a narrowbeam, the stabilized reference frame can be thehead, as it is the case in adults and in childrenfrom 7 years of age onward (Assaiante &Amblard, 1993). Balance control is thus organizedfrom the head to the feet, in descending order. Inaddition, this multi-segmental control also impliesan efficient coordination between posture andmovement that can be organized in a feed-forwardor a feed-back mode.

BUILDING A REPERTOIRE OFBALANCE STRATEGIES

The early stage of independent walking intoddlers offers an excellent opportunity forequilibrium studies. Maintaining balance duringlocomotion is a complex task because it involves

achieving a compromise between the forwardpropulsion of the body, which is a highlydestabilizing force, and the need to maintain thelateral stability of the body. Even simple walkingon a flat surface, free of obstacles, poses a

considerable balance problem to young walkers.Indeed, the difficulty of maintaining equilibriumduring locomotion is further accentuated by thefact that the weight of the whole body must be

supported by one leg at a time during the swingphase of gait. This is the most difficult balanceproblem encountered by infants learning to walk

POSTURAL CONTROL IN HEALTHY CHILDREN" A FUNCTIONAL APPROACH III

(Assaiante, 1998; Assaiante & Amblard, 1993;Breni6re et al., 1989; Thelen, 1984).

We have studied the lateral balance control ofthe upper body segments during locomotion, ininfants from week to 11 months of walkingexperience (Assaiante, 1998; Assaiante &Amblard, 1993). The first result to be noted is thatpelvis stabilization in space strategy is efficientlyused as soon as autonomous walking appears andmight be a prerequisite for the emergence ofindependent walking. Secondly, the shoulderstabilization in space appears only at the secondmonth of autonomous walking. Finally, no

preferred head stabilization, neither in space noron the shoulders, has yet appeared at the eleventhmonth of autonomous walking. The results clearlyindicate an ascending progression with age of theability to control the upper body segments during

locomotion.Figure summarizes the temporal organization

of balance control in young walkers. A calculationof the inter-correlation functions has revealed thatthe movement of shoulders precedes that of thehead and that the movement of the pelvis precedesthat of the shoulders, suggesting an ascendingtemporal organization from the pelvis to the head.Moreover, EMG recordings report that the pelvisis stabilized before foot lift-off, suggesting a

descending temporal organization of balancecontrol from pelvis to feet. Therefore, at this earlyage, rather than a simple temporal ascending org-anization, there is a pelvis-centered organization ofbalance control during locomotion. The pelvisconstitutes thus the first stable reference frame,around which locomotor balance control can bebuilt up.

Fig. I" Scheme of the organization of balance control in toddlers

112 C. ASSAIANTE ET AL.

In the literature, many authors, such as Berthozand Pozzo (1988), Pozzo et al. (1990), Grossman etal. (1988; 1989), Ripoll et al. (1986), Assaiante andAmblard (1993), have demonstrated that in adultsthe head is stabilized in space in various posturo-kinetic activities, presumably to allow better visualfixation and better vestibular processing, as well asto provide a stable reference frame around whichmovements can be built up. During childhood,controlling head stabilization during locomotoractivities constitutes a complex motor skill thattakes a long time to mature (Assaiante & Amblard,1995). In a previous developmental study, Assaianteand Amblard (1993) investigated the developmentof head control during various locomotor tasks. Infact, it is possible to discern at least three maindevelopmental phases.

The first phase includes children from 3 to 6years of age, who adopt head stabilization in spacestrategy only while walking on the fiat groundwithout any equilibrium difficulty. When the levelof equilibrium difficulty increases, these childrenshow an increase in the head-trunk stiffness,particularly in 6-year-old children. This suggestsan en bloc operation of the head-trunk unit.

The second phase includes children from 7 to8, who become able to adopt the head stabilizationin space strategy even when balance difficultyincreases, for example while walking on narrowsupports. This improvement is associated with alarge decrease in the correlations calculatedbetween the head and the trunk movements ofrotation, consistent with an articulated operation ofthe head-trunk unit.

Lastly, in adulthood, the head stabilization inspace strategy is adopted most of the time, butonly in the case of the roll, which is the mostrelevant component of rotation to control thelateral body oscillations while walking. Moreover,the development of head control is not linear. Infact, the development of the head stabilization inspace displays a transition phase between 6 and 7

years of age. In 6-year-old children, the beginningof a systematic use of the head stabilization in spacestrategy observed in 7-year-old children walking onnarrow supports was preceded by a sort ofregression to adopt the alternative head stabilizationon trunk strategy.

SHORT AND LONG TERM POSTURALADAPTATION

When studying the emergence of posturalstrategies, it is essential to distinguish betweenresults due to biomechanical reasons strictly andthose reflecting the maturation of the CNS. Toaddress this problem, we have studied various typesof postural adaptation based either on specificconstraints given by the character of the task thatcovered situations of various balance difficulty oron transitory biomechanical constraints, such asusing a splint blocking one knee to destabilize thepelvis; or on chronic skeletal abnormalities, such astorsion ofthe lower extremities (Assaiante, 2000).

Figure 2 summarizes the main adaptivestrategies, in terms of segmental stabilization inthe frontal plane and corresponding temporalorganization. 3- to 4-year-old children are able tostabilize pelvis and shoulders in space whenwalking on fiat ground. Increasing the taskdifficulty by walking on a narrow line leads to aloss of shoulder stabilization, which can, however,be re-established if the pelvis is destabilized. Earlyhead stabilization in space, as a substitution for thedestabilized pelvis that constitutes the firstreference frame, does not occur, contrary to ouroriginal hypothesis. Thus, short-term adaptationstrategies are selected strictly from the repertoirealready present at the studied age. The temporalorganization is ascending from the stabilizedpelvis to the head. If the pelvis is destabilized, theshoulders tend to become the origin of thetemporal sequence.

POSTURAL CONTROL IN HEALTHY CHILDREN: A FUNCTIONAL APPROACH !13

3-4 years

5-6 years

7-8 years

Segmental stabilizations

Flat groundNarrowsupport

Narrow supportand destabilized

pelvis

Temporal Organization

Flat ground NarrowSupport

,N’row supportand destabilized

pelvis

Fig. 2: Main adaptive strategies according to the age and the increasing difficulty of equilibrium task. The range goesfrom simple walking on flat ground to walking on a line at imposed speed by means of the treadm ill.

When walking on a flat ground or a beam, 5-to 6-year-old children show the same stabilization

patterns as the younger group does. On the otherhand, with a destabilized pelvis, no systematicshoulder stabilization in space is present, and thehead has not yet acquired this ability either. Theresults confirm that at around the age of 6, a turningpoint appears in the development of equilibriumcontrol, as already reported (Assaiante & Amblard,1993; 1995). The temporal organization is practicallyidentical to that of the 3- to 4-year-old children,with the exception of the most difficult situations,when the temporal sequence starts from thesh’oulders. In other words, the temporal organizationof balance control is shoulder-centered.

Finally, 7- to 8-year-old children stabilize the

pelvis, the shoulders, and the head, suggesting an

independent control of each anatomical segmentwhile walking on a flat surface. When balancedifficulty increases, for example during walking ona narrow surface, the shoulder stabilization dis-

appears. In the most difficult situation with the

imposed pelvis destabilization, the head remainsstabilized in space, as do the shoulders sometimes.Under the easiest conditions, the temporal organi-zation ofthe movement is still centered on the pelvis,like in younger children. When walking along a

line, the time sequence starts at the shoulders. Incontrast, with destabilized pelvis, where one would

expect a descending mode of temporal organization,the temporal pattern is completely erroneous. Infact, we observed a sort of regression in the

temporal organization of balance control that justprecedes the establishment of the descending

114 C. ASSAIANTE ET AL.

temporal organization from the head stabilized tothe feet. The latter results of the 7- to 8-year groupremind us that even though segmental stabilizationand temporal organization usually go hand in hand,in certain developmental periods it is importantto emphasize the time-lag between the mastery ofthe segmental stabilization that occurs first and themastery of the corresponding temporal organizationthat occurs in a second time. Various developmentalstudies in posture (Eliasson et al., 1995; Konczak& Dichgans, 1997; Schmitz et al., 1999; 2002) alsoreported that during childhood the control oftiming seems to be the most difficult parameter toacquire.

In a recent study, we investigated the long-term adaptability of the CNS in controlling upperbody segments during various locomotor tasks in5- to 6-year-old and 7- to 0-year-old children withinternal rotations (IR) of the lower limbs and freefrom neurological dysfunction (Mallau et al.,submitted). Their in-toeing gait results either froma persistent femoral torsion or from an internaltibial torsion. All these children, whatever their

age, showed a lower gait velocity, particularly indifficult balance conditions, associated with adecrease of yaw and roll shoulder stabilization inspace. However, in 5-to 6- year-old children, theeffect of the local biomechanical deficit remainedlimited to the lower limbs and did not affect theupper body coordination. By contrast, in the 7-to10-year-old children, the development of headstabilization in space was affected, as demonstratedby an en bloc operation of the head-trunk unitinstead of the articulated mode of operation of thehead-trunk unit systematically adopted by thecontrol group. Thus, as pelvis stabilization remainsthe main reIbrence frame to organize balance controlin older children, the biomechanical anomaly ofthe legs causes an alternative postural strategy,with respect to control children. Further investi-

gations in teenagers should help to test if theseskeletal abnormalities of the lower extremitiesonly delay the use of the head reference frame or if

they remain a life-long obstacle to the building ofthe repertoire of re ference frames.

DEVELOPMENT OF POSTURAL ORIENTATION

In addition to the maintenance of balance andsegmental stabilization, another function of postureis to ensure global body orientation and segmentalorientation. The trunk is a key segment to organizepostural stabilization and orientation control(Massion, 1998). In a previous developmental studywe tested the ability of children to maintain ahorizontal forearm position in various tasksinvolving either voluntary or involuntary trunkmotion (Assaiante, 2000; Roncesvalles et al., inpress).

We simply suggested to our 2-3 year olds toblow bubbles (Fig. 3). In the starting position, thechild was holding a tube full of liquid without anyproblem. The forearm was horizontal and the trunkvertical. In the next step, however, we asked her totake a deep breath and blow bubbles. When sheleans her trunk forward, she spills the liquid, as arelatively constant angle is maintained between theforearm and the trunk. This observation led us toconclude that until the age of 3 years, the majorpostural reference for limb orientation control isthe trunk, which is consistent with an egocentriccontrol of orientation.

The protocol was modified for older children,but the question concerning the coupling betweenthe trunk and the forearm remained the same. Thechildren were sitting in the same position, withtheir lett forearm supporting a tray on which a cupwas posed. Contrary to the experiment describedabove, the trunk was not perturbed by voluntaryinclination but rather by sinusoidal antero-posterioroscillations of the platform on which the subjectswere sitting. However, the repetition of the cycleof oscillations enabled the subjects to anticipatethe perturbation and to stabilize their forearm in ahorizontal position, as in voluntary leaning. We

POSTURAL CONTROL IN HEALTHY CHILDREN: A FUNCTIONAL APPROACH 115

Fig. 3: A 2-year-old child prepares to blow bubbles (left photo) then leans forward to complete the task (right photo).The photo shows the child’s use of an egocentric rather than an exocentric reference frame, as she maintains arelatively constant angle between the forearm and the trunk. Little effort is made to orient the forearm (andbottle) to the vertical line of gravity.

calculated an anchoring index between the forearmand trunk angular dispersions (Assaiante, 2000).

The positive values of anchoring index inadults as in 7- to 10-year-old children show thatthe forearm was stabilized in space rather than onthe trunk, which means that the movements ofthese two segments are independent. In contrast,children aged 4 to 6 years do not show a

significant positive anchoring index. This resultsuggests that younger children show much strongerforearm-trunk coupling than older children do. Theresults again evoke a transition between 6 and 7years from a more global postural control to aselective control of independent body segmentsand from an ego-centric to exocentric control oforientation.

During ontogenesis, periods of relativelystable increase in body size alternate with periodsof accelerating growth. Puberty is characterized byimportant morphological and functional changesduring a short time (Keogh & Sugden, 1985).Moreover, the body scheme, slowly built duringchildhood by the integration between vestibular,

visual, and somatosensory information, is probablyaffected during puberty. The body scheme contributesto the development of the internal representationof action that constitutes the base of feed-forwardcontrol to compensate in advance for thedestabilizing effects of the movement. In a recentstudy, we asked a question about the consequencesof the changes that occur during puberty for pos-tural control and which sensory-motor strategies doteenagers use to preserve their postural perfor-mance (Viel, 2003; Viel et al., unpublished).

To answer to these questions, 14- to 15-year-old teenagers (n 20) were asked to maintain theirvertical body orientation despite very slow lateraloscillations of the support, with or without visionin a standing position. The imposed oscillations ofthe support were chosen in amplitude and frequencyto be either above (+ 5 at 0.06 Hz) or below (+ 5at 0.001 Hz), the semicircular canal threshold.Thus, the lower frequency of the support associatedwith eyes closed provides an excellent opportunityto investigate selectively the proprioceptivecontribution to postural control in teenagers.

116 C. ASSAIANTE ET AL.

Roll Anchoring indexes0.01 Hz 0.06 Hz

With Without With Withoutvieion vision vision vision

Head .

Shoulders

Trunk

Pelvis

Fig. 4: Mean anchoring indexes and standard deviation of head, shoulders, trunk and pelvis with vision (in white circlefor girls and in white square for boys) and without vision (in black circle for girls and in black square for boys)in the case of lateral perturbation ofthe support. Grey squares represent adults without vision.

The roll-anchoring indexes presented in Fig. 4reveal that teenagers differ from young adultsconcerning the stabilization in space strategies forboth frequencies. Most of the time, the values ofthe anchoring indexes obtained in adults arepositive, indicating an independent control of thesegment with respect to the support’s perturbation.Moreover, young adults show a pelvis-stabilizationin space strategy, whereas teenagers show a pelvis-stabilization on support strategy, which is con-sistent with an en-bloc postural strategy, mainlyselected without vision. Based on this study, thestabilization in space strategies appear to improvesignificantly from teenagers to young adults, froman en bloc to articulated operations of the head-trunk unit.

Lastly, teenagers seem more dependent onvisual cues than are adults, which is consistent witha transient proprioceptive neglect hypothesis insensory integration for postural control.

CONCLUSION

In conclusion, the overall results presented inthis paper support the concept of multiple referenceframes: stabilization of the head or stabilization ofthe pelvis, which operate in a complementarymanner or in concert, associated with an en bloc orarticulated operation ofthe body joint to permit themost appropriate temporal organization of balancecontrol during action. The first step for childrenconsists of building a repertoire of postural strategies.The second step consists of learning to select themost appropriate postural strategy depending onthe ability to anticipate on the consequence of themovement in order to maintain balance control andthe efficiency of the task. Developmental studiesinvolving postural control during various posturo-kinetic tasks suggest that anticipatory control,despite its early emergence, slowly matures duringchildhood (Haas et al, 1989; Hay& Redon, 1999;

POSTURAL CONTROL IN HEALTHY CHILDREN: A FUNCTIONAL APPROACH 117

2001, Assaiante et al, 2000), as well as themastering oftiming parameters (Eliasson et al., 1995;Konczak and Dichgans, 1997; Schmitz et al., 1999;2002). Precise mastering of timing parametersseems to be one of the key factors of the antici-patory function that reflects the maturation of theCNS. Taking into account the complexity of theparameters to control, it is not surprising that thedevelopment of postural control continues up tolate periods during childhood and adolescence.The recent development of fMRI studies shouldhelp us to better understand the relations betweenthe late maturational process of the CNS and thelate development of postural control, particularlyat the periods of transition such as 6-7 years andadolescence.

ACKNOWLEDGMENTS

We are grateful to the children who participatedin these studies and their parents. We wish to thankBernard Amblard for his helpful comments and forcritically reviewing the manuscript. This work wassupported by grants from the Centre National de laRecherche Scientifique (CNRS) and l’AssistancePublique des H6pitaux de Marseille (APHM).

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