2010-hadders-algra-variation and variability- key words in human motor development

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doi: 10.2522/ptj.20100006Originally published online October 21, 2010

2010; 90:1823-1837.PHYS THER.Mijna Hadders-AlgraDevelopmentVariation and Variability: Key Words in Human Motor

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Variation and Variability: Key Words inHuman Motor DevelopmentMijna Hadders-Algra

This article reviews developmental processes in the human brain and basic principlesunderlying typical and atypical motor development. The Neuronal Group SelectionTheory is used as theoretical frame of reference. Evidence is accumulating thatabundance in cerebral connectivity is the neural basis of human behavioral variability(ie, the ability to select, from a large repertoire of behavioral solutions, the one mostappropriate for a specific situation). Indeed, typical human motor development ischaracterized by variation and the development of adaptive variability. Atypicalmotor development is characterized by a limited variation (a limited repertoire ofmotor strategies) and a limited ability to vary motor behavior according to thespecifics of the situation (ie, limited variability). Limitations in variation are relatedto structural anomalies in which disturbances of cortical connectivity may play aprominent role, whereas limitations in variability are present in virtually all children

with atypical motor development. The possible applications of variation and variabil-ity in diagnostics in children with or at risk for a developmental motor disorder arediscussed.

M. Hadders-Algra, MD, PhD, isProfessor of Developmental Neu-rology, Department of PediatricsDevelopmental Neurology, Uni-

versity Medical Center Groningen,University of Groningen, Hanz-eplein 1, 9713 GZ Groningen, theNetherlands. Address all corre-spondence to Dr Hadders-Algraat: [email protected].

[Hadders-Algra M. Variation andvariability: key words in humanmotor development. Phys Ther.2010;90:18231837.]

2010 American Physical TherapyAssociation

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Human behavior is character-ized by variation: each humanindividual has a large reper-

toire of motor, cognitive, and socialactions that can be arranged in

virtually endless combinations. Thisrepertoire allows for a flexible ad- justment to changing conditions,including the creation of newsolutions.

The wealth of distinctly human be-havior is attributed to the neocortex,the part of the brain that expandedgreatly during evolution.1,2 For in-stance, in insectivores such as thehedgehog, the neocortex occupies10% to 20% of total brain volume,

whereas this proportion has risen toabout 80% in humans.3 The enlarge-ment of the neocortex has beenbrought about mainly by expansionof the surface area and not so muchby an increase in cortical thickness.2

The expansion of cortical surface al-lowed for the emergence of new ar-eas (eg, language-related areas) andthe extension of the prefrontal cor-tex and association areas. Interest-ingly, the volume of the white mat-

termostly consisting of cortico-cortical connectionsincreased moreduring the evolutionary expansionof the cortex than the volume of graymatter.3,4

The development of the humanbrain is an intricate and long-lasting

process, which is mirrored by a mul-titude of developmental changes inbehavior. The latter include thechanges involved in the transfor-mation of nongoal-directed fetal

motility into the accurate and goal-directed movements of an adult per-son, such as those involved in writ-ing a letter or riding a bike. The aimof this article is to discuss putativemechanisms and principles underly-ing developmental changes in motorbehavior. Particular attention is paidto the notions of variation andvariability. The article starts with ashort overview of the ontogeny ofthe human brain. Sections on theo-retical considerations and typical

and atypical motor development fol-low. The emphasis is on the earlyphases of development and the Neu-ronal Group Selection Theory(NGST) is used as a frame of refer-ence. The NGST was chosen becauseit highlights that variation and vari-ability are key elements of typicaldevelopment. Variation implies thepresence and expression of a broadrepertoire of behaviors for a specificmotor function. Variability denotes

the capacity to select from the rep-ertoire the motor strategy that fitsthe situation best. The article con-cludes with possible applications of

variation and variability in diagnos-tics in infants with or at risk for adevelopmental motor disorder.

Development of theHuman BrainThe development of the humanbrain, and in particular, that of theneocortical circuitries, lasts about 4decades.5 It starts during the earlyphases of gestation with the prolifer-ation of neurons. The majority of tel-encephalic neurons are produced inthe germinal layers near the ventri-cles.2,6 Once neurons have been gen-erated, they move from their place oforigin to their final destination, thecortical plate.6,7 Before the corticalplate is formed, however, neuronshalt in the subplate. The subplate is a

temporary layer between the ven-tricular zones plus intermediate zone(the future white matter) and thecortical plate.8 The subplate emergesin early fetal life, is thickest at around

29 weeks postmenstrual age (PMA),and disappears gradually until it isabsent at around 6 months post-term.9,10 The major proportion of itsafferent and efferent connectionsrun through the (future) periven-tricular white matter. The subplatemediates fetal behavior.

Neurons start to differentiate duringmigration and during their stay inthe subplate. Neuronal differentia-tion includes the formation of den-

drites and axons, the production ofneurotransmitters and synapses, andthe elaboration of the intracellularsignaling machinery and complexneural membranes.11,12 The processof differentiation is particularly ac-tive in the few months prior to birthand the first postnatal months, but ittakes many years before the adultstate of differentiation is achieved.5

Besides neural cells, glial cells aregenerated. The peak of glial cell pro-

duction occurs in the second half ofgestation. Some of the glial cells takecare of axonal myelination. Myelina-tion takes place especially betweenthe second trimester of gestation andthe end of the first postnatal year.Thereafter, myelination continuestill the age of about 40 years, whenthe last intracortical connectionscomplete myelination.13

Brain development consists not onlyof creation of components, but alsoof an elimination of elements. Abouthalf of the created neurons die offby means of apoptosis. Apoptosis isbrought about by interaction be-tween endogenous programmedprocesses and chemical and electri-cal signals induced by experience14;it occurs in particular during mid-gestation.5 Similarly, axons and syn-apses are eliminated, the latter espe-cially between the onset of puberty

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Discussion Podcast: Special Issueauthors Linda Fetters, ReginaHarbourne, and Beatrix Vereijkendiscuss the clinical implications oftheir work. Moderator is James(Cole) Galloway.

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This article was published ahead ofprint on October 21, 2010, atptjournal.apta.org.

Variation and Variability in Human Motor Development

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and early adulthood. As a result, theadult level of synaptic density inthe cortex is reached first in earlyadulthood.5

For a long time, it had been debated whether brain development isdriven by endogenous processes orby external input. Gradually, how-ever, it became clear that genetic in-struction (nature) and environ-mental information (nurture) bothplay an important role, albeit withdifferent weights during differentphases of development. In the earlyphases, the role of the genome dom-inates; later on, environment and ex-perience become crucial. The impor-

tance of genetic instruction in earlydevelopment is reflected by animalstudies that indicated the primarycortical areas, their connections,their modular organization, and theirsize are largely determined by differ-ential gene expression in the neuralstem cells.1,15 Thus, the geneticallyspecified areas attract specific inputsinstead of inputs specifying the ar-eas.2 This means that the functionaltopography of the brain is primarily

driven by genetic instruction (ie, thefact that occipitally located neurons

virtually always become involved inthe processing of visual informationand frontally located networks in ac-tivities such as planning and atten-tion). A primary genetic determina-tion, however, does not preclude

variation, as each individual has hisor her own sets of genes. Moreover,the primary genetic determination isonly the starting point for epigeneticcascades, allowing for abundant in-teraction with the environment andactivity-dependent processes.1618

Note that the interaction is bidirec-tional: experience affects gene ex-pression, and genes affect how theenvironment is experienced.18

Virtually all of the neurodevelop-mental processes described aboveare affected by experience, in-cluding motor experience. Animal

studies have demonstrated that theeffect depends on the type of expe-rience (eg, specific versus general-ized motor experience), the age atexposure, the individuals sex, and

the neural area.18,19

Experience mayaffect, for instance, apoptosis, axonretraction, synapse elimination, andsynapse formation.1921 It may evenaffect the somatotopic organizationof the primary motor cortex, as wasindicated by the recent human studyby Stoeckel et al.22 This imagingstudy revealed that the motor footrepresentation in individuals withcongenitally compromised handfunction and compensatory skillfulfoot use had extended beyond the

classical foot area into the vicinity ofthe lateral hand area.

Theoretical ConsiderationsVarious Theoretical FrameworksDespite increasing knowledge of thedevelopmental processes in the hu-man brain, our understanding of theneural mechanisms underlying mo-tor development is limited. As a re-sult, multiple theories of motor de-

velopment have been produced, all

aiming to facilitate the understand-ing of typical and atypical motor de-

velopment. During the major part ofthe previous century, motor devel-opment basically was regarded as aninnate, maturational process,23,24 butduring the centurys last 2 decades, itbecame increasingly clear that motordevelopment is largely affected byexperience.

Currently, 2 theoretical frameworksare most popular: dynamic systemstheory2527 and NGST.28,29 Theframeworks share the opinion thatmotor development is a nonlinearprocess with phases of transitionthat is affected by many factors. Thefactors may vary from features of thechild to external influences such ashousing conditions, the presence ofstimulating caregivers, and the pres-ence of toys. In other words,both theories acknowledge the

importance of experience and therelevance of context. The 2 theo-ries differ, however, in their opin-ion on the role of geneticallydetermined neurodevelopmental

processes. Genetic factors playonly a limited role in dynamic sys-tems theory, whereas genetic en-dowment, epigenetic cascades, andexperience play equally prominentroles in NGST.28,29 In the followingparagraphs, I will use the NGSTframework to discuss principles oftypical and atypical motor development.

NGST and Typical MotorDevelopment

The NGST was developed by GeraldEdelman. He described motor devel-opment as characterized by 2 phasesof variability: primary and second-ary.28,29 The borders of variability aredetermined by genetic instruc-tions.1,15 During the phase of pri-mary variability, motor behavior ischaracterized by abundant variation.The variation is brought about byexplorative activity of the nervoussystem. The system explores all mo-

tor possibilities. The explorationgenerates a wealth of self-producedafferent information, which, in turn,is used for further shaping of thenervous system. The exploration re-flects the continuous, dynamic inter-action between genes and experi-ence, including experience withchanging body proportions. Initially,however, the afferent informationis not used for adaptation of motorbehavior to environmental con-straints. In other words, the phase ofprimary variability is characterizedby variation in motor behavior andthe absence of the ability to adaptthe various movement possibilitiesto the specifics of the situation (ie,by the absence of variabilityin sensu

strictu, as defined in the introduc-tion of the article).24

At a certain point in time, the ner-vous system starts to use the afferent



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information produced by behaviorand experience for selection of themotor behavior that fits the situa-tion best: the phase of secondary oradaptive variability starts. Hitherto,

the mechanisms underlying the shiftfrom primary variability to secondary variability are not understood. Theprocess of selection, which is char-acteristic of variability and thusthe phase of secondary variability,is based on active trial-and-errorexperiences that are unique to theindividual.3032 Indeed, evidence isaccumulating that self-produced sen-sorimotor experience plays a pivotalrole in motor development.31,3335

To determine whether a movementis most adaptive, reference valuesare used that most likely are functionspecific. The solution that is selectedis specific for the situation and theinfants stage of development. Forinstance, in sitting infants whosebalance is perturbed, informationlinked to the stability of the head inspace is used to select the posturaladjustment in which most of theso-called direction-specific postural

muscles are recruited (the en blocpattern).36 Selection of the en blocpattern depends on the degree ofbalance perturbationthe pattern isrecruited more often during largeperturbations than during smallperturbationsand the age of thechild.36,37 Children select the en blocpattern during marked perturbationsof balance especially often betweenthe ages of 9 months and 212 years.Thereafter, similar perturbations ofbalance are associated with child-specific postural adaptations in

which fewer direction-specific mus-cles are recruited.37

The process of learning to select themost appropriate motor solutionin a specific situation is based onimplicit motor learning and does notinvolve conscious decision making.It occurs at various interdependentlevels of neural organization. Animal

data indicate that at the cellular level,selection is mediated by changes insynaptic strength, in which the to-pology of the cells38 and the pres-ence or absence of coincident elec-

trical activity in presynaptic andpostsynaptic neurons play a role.39,40

In terms of the organization of motorcontrol, selection occurs at the levelof motor strategies and at the level oftemporal and quantitative tuning ofmotor output.36 Recent neurophysi-ological data indicated that the basalganglia might play a major role inthe selection of motor strategies (ie,in motor sequence learning),32,41

whereas the cerebellum might bethe key structure involved in the se-

lection of situation-specific temporaland quantitative parameters of mo-tor output (ie, accurate motor adap-tation).42,43 The idea that frontostria-tal circuitries play a role in theselection of motor strategies is sup-ported by a recent birth cohort studyby Murray et al.44 The study indi-cated that an earlier development ofthe ability to stand independently

which might be interpreted as anearlier ability to select an appropri-

ate strategy to keep balance in up-right stancewas associated withbetter executive functions in adult-hood. The association was specificfor executive functions, which aresubserved by frontostriatal circuit-ries; other cognitive functions suchas verbal and visual learning, whichare more closely related to temporalcortex function, were not related toan earlier development of standing.

The transition from primary variabil-ity to secondary variability occurs atfunction-specific ages. For instance,in the development of sucking be-havior, the phase of secondary vari-ability starts prior to term age45; inthe development of postural adjust-ment, it emerges after the age of 3months46,47; and in the developmentof foot placement during walking, itstarts between 12 and 18 months.48

The age at which adaptive behavior

first can be observed depends on themethod of investigation. For in-stance, with the application of elec-tromyographic recordings, the firstsigns of adaption in postural behav-

ior during sitting may be observedat the age of 4 months,46 but whensimple behavioral observation isused, signs of adaptive sitting behav-ior are first detected from 6 monthsonward.49 Around the age of 18months, all basic motor functions,such as sucking, reaching, grasping,postural control, and locomotion,have reached the first stages of sec-ondary variability. Due to the in-genious interaction between self-produced motor activities with trial-

and-error learning and the long-lasting developmental processes inthe brain, such as dendritic refine-ment, myelination, and extensivesynapse rearrangement,5 which fur-nish new neuromotor possibilities, ittakes until late adolescence beforethe secondary neural repertoire hasobtained its adult configuration. Inother words, the basic, variable mo-tor repertoire that is formed duringthe phase of primary variability con-

tinues to develop during the phaseof secondary variability and tochange throughout life.

The ongoing developmental changesin the nervous system, which arebased on a never-ending interactionbetween experience and genetic in-formation, allow for increasinglyprecise and complex motor skills,

which may be regarded as refine-ments of the basic, variable reper-toire. As a result, adult human beingsare equipped with a variable move-ment repertoire with an efficientmotor solution for each specificsituation.

NGST and Atypical MotorDevelopment

Atypical motor development mayoriginate from genetic aberrationsor adversities occurring duringearly development. Both etiological



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pathways may result in a structuralanomaly or lesion of the developingbrain or in a different setting of spe-cific neurotransmitter systems, suchas the monoaminergic systems. Ac-

cumulating evidence indicates thatstressful situations in the prenataland perinatal periods may inducelifetime changes in dopaminergic, se-rotonergic, or noradrenergic circuit-ries.50 The monoaminergic systemsare widespread systems involved inthe modulation of behavior.51 The 2sequelaethe lesion of the brain andthe different setting of the monoam-inergic systemswill be discussedas different entities, but it should bekept in mind that lesions of the im-

mature brain often are associatedwith changes in specific neurotrans-mitter systems.52

The best example of atypical motordevelopment due to an early lesionof the brain is the motor develop-ment of children with cerebral palsy(CP). Other examples are some chil-dren with developmental coordina-tion disorder and some children withattention deficit hyperactivity disor-

der. It is important to note, however,that in general developmental coor-dination disorder and attention defi-cit hyperactivity disorder cannot beattributed to a lesion of the brain.53

In the following paragraphs, CP isused as a prototype to describe themotor sequelae of a lesion occurringin the fetal or infant brain.54

NGST and an Early Lesion ofthe Brain

According to NGST, an early lesionof the brain has 2 major consequenc-es.55 First, the repertoire of motorstrategies is reduced.5659 This re-duced repertoire results in less vari-able and more stereotyped motorbehavior (ie, in reduced variationduring both phases of variability).The limited repertoire may result inthe absence of a specific motor strat-egy, which would be available as thebest solution in a specific situation

for a child with typical development. As a consequence of the absenceof the best solution, the child withCP may have to choose a motor so-lution that differs from that of the

child with typical development.60

This situation implies that the differ-ent motor behavior of a child withCP should not always be regarded asdeviant (ie, as something that de-serves to be treated away), as itmay be the childs best and mostadaptive solution for the situation.61

Second, in the phase of secondaryvariability, children with an early le-sion of the brain have problems withselection of the most appropriatelyadapted strategy out of the reper-

toire. In other words, they have alimited capacity to vary motor behav-ior in relation to the specifics of thesituation (ie, they have a limitedvariability).

The deficient capacity to select has adual origin: it is related to deficits inthe processing of sensory informa-tion that are virtually always presentin children with an early lesion ofthe brain6267 and to the fact that the

best solution may not be availabledue to repertoire reduction. The dif-ficulties in selection have 2 practicalconsequences. First, impaired selec-tion may give rise to the paradoxicalfinding that results of motor tests ofchildren with CP often are more vari-able than those of children with typ-ical development.67,68 The variabletest results are brought about by pro-longed periods of trial and errorneeded to explore the reduced rep-ertoire due to impaired selection.This consequence means that a re-duced repertoire may be associated

with more variable motor output.Second, impaired selection inducesthe need of ten- to hundredfold moreactive motor experience than typi-cally needed to find the best strate-gy.69,70 Consequentially, children

with CP need considerably morepractice than their peers without CPto learn a specific motor task.

Recall that exploratory drive is a fun-damental feature of the typically de-

veloping nervous system. As a re-sult, young infants spontaneouslygenerate a wealth of everyday motor

practice.35

The child with CP needsmuch more practice. In addition, thebrain lesion responsible for CP maybe associated with reduced explor-atory drive.54 This reduced explor-atory drive creates a challenging sit-uation for the child with CP and hisor her environment. The need formuch practice requires strong moti-

vation, which is obtained most easilywhen tasks to be learned have func-tional significance or are enjoyable.

NGST and an Altered Setting ofMonoaminergic Systems

Adversities prior to term age, such aslow-risk preterm birth, intrauterinegrowth retardation, or psychologicalstress of the pregnant woman, maygive rise to a different setting of themonoaminergic systems in the ab-sence of a lesion of the brain. Most ofour knowledge about the effect ofstressful conditions during early lifeon the developing brain is based on

animal data.50

The animal data indi-cate that stress during early life givesrise to changes in serotonergic andnoradrenergic activity in the cerebralcortex and alterations in dopaminer-gic activity in the striatum and pre-frontal cortex.71 These changes havebeen associated with impaired devel-opment of the maps of body repre-sentation in the primary somato-sensory cortex, inappropriatelydeveloped ocular dominance col-umns in the visual cortex, and mildmotor problems.7274 In terms ofNGST, this impaired developmentmay reflect a situation in which thechild has a typical movement reper-toire but has difficulties in selectingthe best strategy in a specific situa-tion due to the deficits in processingof sensory information. In other

words, the child has an impairedability to vary motor behavioranimpaired variabilityin relation to



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task-specific requirements. As a re-sult, the child often exhibits more

variable behavior during motor testsand needs more practiceand thusmore timeto learn new motor

skills. Indeed, such mechanisms ap-pear to play a role in the frequentlyencountered impaired motor devel-opment of preterm children withoutcerebral palsy.59,75,76

Early Phases of MotorDevelopmentTypical Motor DevelopmentNongoal-directed motility. Arecent, detailed ultrasound study onthe emergence of fetal motility re-

vealed that the earliest movementscan be observed at the age of 7

weeks 2 days PMA.77 The first move-ments are slow, small, sidewaysbending movements of head ortrunk. A few days later, these simplemovements develop into move-ments in which 1 or 2 arms or legsalso participate, but the movementscontinue to be slow, small, simple,and stereotyped. At the age of 9 to 10

weeks PMA, general movements(GMs) emerge (ie, movements in

which all parts of the body partici-pate). Initially, GMs show little vari-ation in movement direction, ampli-tude, and speed. After a few days,however, the majority of GMs showa substantial degree of variation inspeed, amplitude, participating bodyparts, and movement direction. In-terestingly, the emergence of GMs

with movement variation and com-plexity at 9 to 10 weeks PMA coin-cides with the emergence of synap-

tic activity in the cortical subplate.78

This coincidence and the findingthat the evolution and transient na-ture of the subplate match that ofGM development inspired the hy-pothesis that variable and complexGMs result from activity of the sub-plate modulating the basic activity ofGM networks in the spinal cord andbrain stem.79

Soon after the emergence of the firstmovements, other movements areadded to the fetal repertoire, such asisolated arm and leg movements,startles, various movements of the

head (rotations, anteflexion, andretroflexion), stretches, periodicbreathing movements, and suckingand swallowing movements.80 Theage at which the various movementsdevelop shows considerable inter-individual variation, but at about 16

weeks PMA, all fetuses exhibit theentire fetal repertoire. The reper-toire continues to be presentthroughout gestation.

At birth, be it term or preterm, only

minor changes in the motor reper-toire occur. Breathing movementsbecome continuous instead of peri-odic, the Moro reaction can be elic-ited for the first time, and the infant,

who is now hampered by the forcesof gravity, is no longer able to ante-flex the head in a supine position.81

General movements continue to bethe most frequently observed motorpattern.

Between 2 and 4 months postterm,infant behavior changes drastically.The infant is able to use smiles andpleasure vocalizations in social inter-action, the head can be stabilized onthe trunk, and a steady visual fixationand brisk visual orienting reactionshave been developed.81 Simulta-neously, GM activity is about to dis-appear and to be replaced graduallyby goal-directed activity of arms andlegs. Interestingly, the final phase ofGMs, which occurs at 2 to 4 monthspostterm, is characterized by a spe-cific movement property: the fidg-ety nature of GMs. The fidgety char-acter denotes the presence of acontinuous stream of tiny, elegantmovements occurring irregularly allover the body.58 Functional neuroim-aging studies suggest that increasingactivity in the basal ganglia, thecerebellum, and the parietal, tempo-ral, and occipital cortices plays a

prominent role in the behavioraltransition at 2 to 4 months.82

Goal-directed motility. The de-velopment of goal-directed behavior

during infancy is characterized byintraindividual and interindividualvariation.55,57,83,84 The variation oc-curs, for instance, as variation in theemergence of a function, variation inthe performance of a function (Figs.1 and 2), variation in the duration ofspecific developmental phases, and

variation in the disappearance of in-fantile reactions, such as the Mororeaction. The variation in develop-ment includes the co-occurrence ofdifferent developmental phases. For

instance, infants of a certain age canalternate belly crawling with crawl-ing on hands and knees.83,85 Infants

with typical development also mayexhibit a temporary regressionaninconsistencyin the develop-ment of a specific function.83As longas the regression is restricted to asingle function, it can be regarded asanother expression of developmen-tal variation. Large variation in theattainment of milestones in goal-

directed motor behavior (Fig. 3) im-plies that the assessment of mile-stones has less clinical value thanpreviously was thought.86 Slow de-

velopment of a single function usu-ally has no clinical significance, butthe finding of a general delay is clin-ically relevant.

Infancy is the period of transitionfrom primary variability to secondary

variability (ie, from motor behaviorthat cannot be adapted to task-specific conditions to adaptive mo-tor behavior). This transition occursat function-specific ages. A recentobservational study indicated thatthe transition in sitting behavior oc-curs between 6 and 10 months, thatin abdominal progression occurs be-tween 8 and 15 months, that inreaching movements occurs be-tween 6 and 12 months, and that ingrasping occurs between 15 and 18



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results in actual grasping of an objectfrom about 4 months onward.93 Atthis age, reaching movements havean irregular and fragmented trajec-tory consisting of multiple movementunits. These characteristics under-line the probing nature of early

reaches and the heavy reliance of thefirst reaching movements on feed-back control mechanisms.93 Duringthe following months, the reachingmovement becomes increasingly flu-ent and straight, and the orientationof the hand becomes increasingly

adapted to the object.94 After theirfirst birthday, infants increasinglyuse the pincer grasp to pick up tinyobjects. This change in behaviorimplies that corticomotoneuronalpathways are being involved increas-ingly in fine motor control.95

Figure 2.

Variation in motor behavior in a sitting position at 11 months postterm. The figure consists of frames selected from a videorecordingof about 3 minutes. Figure produced with permission of the parents.



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At birth, the infantlike the fetusshows locomotor-like behavior inthe form of neonatal stepping move-ments.96 These movements probablyare generated by spinal pattern gen-

erators analogous to the locomotionin the hind limbs of kittens after atransection of the thoracic cord andthe locomotor-like activity in people

with a spinal cord injury.96 The in-fant stepping movements are ratherprimitive in character and differ fromthe flexible plantigrade gait of adult-hood.97 This nongoal-directed neo-natal stepping is characterized by alack of segment-specific movements,implying that the legs tend to flexand extend as a single unit; by the

absence of a heel-strike; by a variablemuscle activation with a high degreeof antagonistic coactivation; and byshort-latency bursts of electromyo-graphic activity at the foot contactdue to segmental reflex activity.96,97

In the absence of specific training,the stepping movements can nolonger be elicited after the age of 2 to3 months.83

A period of locomotor silence fol-

lows, which is succeeded in thethird quarter of the first postnatal

year by goal-directed progression inthe form of crawling and supportedlocomotion. When neonatal step-ping is trained daily, the steppingresponse can be elicited until it isreplaced by supported locomo-tion.98 This progression is perhapsnot so surprising in light of the factthat the locomotor pattern of sup-ported locomotion is reminiscentof that of neonatal steppingbothlacking the determinants of planti-grade gait.97 In addition, the mile-stone transition into independent

walking is not associated with a major change in specific locomotor ac-tivity. This finding indicates that theemergence of independent locomo-tion is not primarily induced bychanges in the locomotor networks.Presumably, the development of in-dependent walking is largely depen-

dent on the development of posturalcontrol,99 which, in turn, is depen-dent in particular on developmentalchanges in the subcortical-corticalcircuitries.96

Motor development beyond infancyis characterized by a gradual increasein agility, adaptability, and the ability

to make complex movement se-quences. It is the phase of secondary

variability, during which matura-tional processes in continuous inter-action with changing body propor-tions and experience produce highlyadaptive secondary neuronal reper-toires.24,28 The creation of secondaryrepertoires is associated with exten-sive synapse rearrangement, whichis the net result of synapse formationand synapse elimination.5 It is facili-tated by increasingly shorter process-ing times, which can be attributed,in part, to ongoing myelination.100

Atypical Motor DevelopmentDevelopmental changes in the

young brain have a large impact onthe expression of atypical motor be-havior. It may happen that a lesion ofthe developing brain results in neu-romotor dysfunction in infancy butis followed by a typical developmen-

tal outcome. The reverse may alsooccur (ie, an apparently typical de-

velopment in the early phases ofinfancy may be followed by the de-

velopment of CP).58

In infancy, atypical motor develop-ment may be expressed by a delayin the achievement of milestones

(which may be related to impairedselection), by mild or major devia-tions in muscle tone (velocity-dependent resistance to stretch), bya persistence of infantile reactions(eg, the Moro reaction), and by areduced variation in motor behavior.The latter sign may be the most spe-cific expression of an early lesion ofthe brain,55,58,101 whereas the othersigns may be the result of a lesion ofthe brain but also may be related toother types of adversities duringearly development, such as low-riskpreterm birth.102104 Reduced varia-tion in motor behavior is well ex-pressed in the quality of GMs: abnor-mal GMs are characterized by limited

variation and limited complexity. In-terestingly, definitely abnormal GMsare related to white matter pathol-ogy and not to abnormalities of thebrains gray matter.79,105 Further-more, beyond the age of 4 months,

Figure 3.Schematic representation of the ages at which some motor skills emerge during infancy.The length of the bars reflect the interindividual variation. Adapted from Touwen.83



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when GMs have disappeared, atypi-cal motor development is character-ized by reduced variation (Figs. 4 and5). Well-known stereotypies are fist-ing of the hands, extension of thelegs, clawing of the toes, dominantasymmetrical tonic neck reflex pos-turing, hyperextension of the neckand trunk, or stereotyped asymme-tries.106 It has been postulated thatthe degree to which movement vari-ation is reduced may reflect the ex-tent to which cortical connectivity isimpaired.79,107

Atypical motor development is asso-ciated with postural dysfunction.

Children with a severe lesion of thebrain who develop severe bilateralspastic CP or severe athetosis andfunction at Gross Motor FunctionClassification System level V108 pre-sumably lack the basic level of pos-tural control.109 In infants with less-severe forms of CP, the basic level ofpostural organization is more or lessintact. However, their postural de-

velopment is hamperedand, there-fore, delayed by a limited reper-toire of postural adjustments and adeficient capacity to adapt postureto the specifics of the situation.109

Diagnostic Application ofVariation and VariabilityGradually, European clinicians work-ing in the field of developmentalneurology realized that variation and

variability may assist in the evalua-tion of motor development. How-ever, before addressing the value ofthese parameters, some general re-flections on the significance of theinfant neuromotor assessment arenecessary. Evaluation of neuromotorfunction in early life has 2 goals. Firstand foremost, it aims at assessingthe infants current capacities andlimitations, as the assessment offers

Figure 4.Reduced variation in motor behavior in a supine position at 2 months postterm. The figure consists of frames selected from avideorecording of about 3 minutes. Figure produced with permission of the parents.



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the basis for therapeutic guidance.Second, an assessment at an earlyage may assist in the prediction ofthe infants developmental pros-pects. However, as indicated in thepreceding paragraphs, the develop-mental characteristics of the brain

preclude precise prediction. Predic-tion of developmental outcome isbest when multiple sources of infor-mation are used, such as the infantshistory, the results of neuroimaging,and neurophysiological assessmentsin combination with a neurological,

developmental, and neuromotor as-sessment.110 Prediction also is largelyfacilitated when longitudinal seriesof assessments are used.104,111

The various instruments available toevaluate the infants neuromotor and

Figure 5.

Reduced variation in motor behavior in sitting at 10 months postterm. The figure consists of frames selected from a videorecordingof about 3 minutes. Figure produced with permission of the parents.



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developmental status have specificaims, advantages, and disadvantages.Most instruments provide informa-tion on the childs function in termsof age-adequate performance versus

underachievement or delay. Exam-ples are the Bayley Scales of InfantDevelopment112 and the Albert In-fant Motor Scales.113 Neurological as-sessments pair information on motorperformance with specific details onsensorimotor function in terms ofmuscle tone and reflexes.110 Thegrowing awareness that the qualityof motor behavior may assist in theevaluation of the childs neuromotorcondition inspired the developmentof 3 new assessment methods; the

Test of Infant Motor Performance(TIMP),114 the GM method,58,115 andthe Infant Motor Profile (IMP).116

The TIMP and the GM method areapplicable till the age of 4 monthspostterm, whereas the IMP is de-signed for infants aged 3 to 18months postterm. In contrast to theother 2 instruments, the TIMP doesnot use variation or variability as ex-plicit parameters of movement qual-ity. The TIMP has good reliability,

and the limited data available suggestthat it is a valuable instrument in theprediction of CP.110 The 2 methodsusing the concepts of variation and

variability are discussed below. Vari-ation (ie, the evaluation of the size ofthe repertoire) is a parameter thatmay be applied in the phase of pri-mary and secondary variability. Vari-ability (ie, the ability to make anadaptive selection) is particularly rel-evant from the emergence of second-ary variability onward.

The examination of the quality ofGMs is a reliable assessment basedon the evaluation of movement vari-ation.58,115 General movement as-sessment does not include the eval-uation of variability, as the nongoal-directed GMs do not have a phase ofsecondary variability.24 In the GMmethod, 2 aspects of variation areassessed: (1) GM complexity, which

denotes the spatial aspect of move-ment variation, and (2) GM variation,

which represents the temporal vari-ation of movements. Definitely ab-normal GMs are characterized by a

severely reduced movement com-plexity and variation; in mildlyabnormal GMs, complexity and vari-ation are present, but to an insuffi-cient extent.58 The consistent pres-ence of definitely abnormal GMsduring the first postnatal months isassociated with a very high risk forthe development of CP.58,115

The predictive value of single assess-ments increases with age. Best pre-diction is achieved with an assess-

ment in the final phase of GMs (ie, inthe phase of fidgety GMs at around3 months postterm). In populationsof infants who are at risk for CP,definitely abnormal GMs at 3 monthsare associated with a risk of CPthat varies between 25% and80%,79,115,117 whereas mildly abnor-mal GMs are associated with an in-creased risk of minor neurologicaldysfunction and psychiatric morbid-ity at school age.118,119 It should be

noted, however, that the predictivepower of mildly abnormal GMs at 3months is so low that mildly abnor-mal GMs as a single sign have noclinical relevance. The recent findingthat the predictive value of GM qual-ity is substantially higher in popula-tions of infants who are at risk for CPthan in the general population120

supports the idea that the quality ofGMs reflects the integrity of corticalconnectivity (ie, the integrity of thebrains white matter), as large partsof the brains white matter are situ-ated in the periventricular area,

which is the site of predilection fordamage in the preterm period.121

The IMP is a novel instrument thatassesses infant motor behavior in 5domains. Two domains are based onthe NGST: size of the repertoire(variation) and ability to select (vari-ability). The other 3 domains evalu-

ate more traditional aspects of motorbehavior: symmetry, fluency, andperformance.76,116 The reliability andconstruct validity of the IMP aregood, and its predictive and evalua-

tive power is promising.76,116

Concluding Remarks Accumulating evidence indicatesthat abundance in cerebral connec-tivity is the neural basis of humanbehavioral variability (ie, the abilityto select from a large repertoire ofbehavioral solutions the one mostappropriate for a specific situation).Indeed, typical human motor devel-opment is characterized by variationand the development of adaptive

variability, and atypical motor devel-opment is characterized by limita-tions in variation and variability. Lim-itations in variation are based onstructural anomalies, in which distur-bances of cortical connectivity mayplay a prominent role, whereas limi-tations in variability are present in

virtually all children with atypicalmotor development. In infants withreduced variation, early interventionmay aim to enlarge the limited move-

ment repertoire, but animal data in-dicate that this aim is difficult toachieve.52 This situation impliesthatdespite interventionreper-toire reduction most likely will re-main a feature of the motor behaviorof the child with an early lesion ofthe brain. In such a situation, equip-ment may offer a proper means tofacilitate functional activity andparticipation.

The limited variability of children with atypical motor development isbased on the limited ability to selecta strategy out of the movement rep-ertoire due to deficiencies in theprocessing of sensory informationbrought about by self-produced ac-tions. This fact suggests that children

with limited variability may profitfrom ample, variable, self-produced,trial-and-error activities.122,123



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Dr Hadders-Algra acknowledges the techni-cal assistance of Linze J. Dijkstra and MichielSchrier, MSc, in preparation of the figuresand Tineke Dirks, PT, for critical commentson a draft of the manuscript.

This article was submitted January 7, 2010,

and was accepted June 24, 2010.

DOI: 10.2522/ptj.20100006

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