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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 principles
underlying typical and atypical motor development. The Neuronal Group Selection
Theory is used as theoretical frame of reference. Evidence is accumulating that
abundance 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 most
appropriate for a specific situation). Indeed, typical human motor development is
characterized by variation and the development of adaptive variability. Atypical
motor development is characterized by a limited variation (a limited repertoire of
motor strategies) and a limited ability to vary motor behavior according to the
specifics of the situation (ie, limited variability). Limitations in variation are related
to structural anomalies in which disturbances of cortical connectivity may play a
prominent role, whereas limitations invariabilityare 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 are
discussed.
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.]
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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 been
brought 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 the
changes 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 motor
behavior. 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 the
cortical 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 subplate
mediates 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 intracellular
signaling 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 connections
complete 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 programmed
processes 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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and early adulthood. As a result, the
adult level of synaptic density in
the cortex is reached first in early
adulthood.5
For a long time, it had been debatedwhether brain development is
driven by endogenous processes or
by external input. Gradually, how-
ever, it became clear that genetic in-
struction (nature) and environ-
mental information (nurture) both
play an important role, albeit with
different weights during different
phases of development. In the early
phases, 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 animal
studies that indicated the primary
cortical areas, their connections,
their modular organization, and their
size are largely determined by differ-
ential gene expression in the neural
stem cells.1,15 Thus, the genetically
specified areas attract specific inputs
instead of inputs specifying the ar-
eas.2 This means that the functional
topography of the brain is primarily
driven by genetic instruction (ie, thefact that occipitally located neurons
virtually always become involved in
the processing of visual information
and 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 his
or her own sets of genes. Moreover,
the primary genetic determination is
only the starting point for epigenetic
cascades, allowing for abundant in-
teraction with the environment and
activity-dependent processes.1618
Note that the interaction is bidirec-
tional: experience affects gene ex-
pression, and genes affect how the
environment is experienced.18
Virtually all of the neurodevelop-
mental processes described above
are affected by experience, in-
cluding motor experience. Animal
studies have demonstrated that the
effect depends on the type of expe-
rience (eg, specific versus general-
ized motor experience), the age at
exposure, the individuals sex, and
the neural area.18,19
Experience mayaffect, for instance, apoptosis, axon
retraction, synapse elimination, and
synapse formation.1921 It may even
affect the somatotopic organization
of the primary motor cortex, as was
indicated by the recent human study
by Stoeckel et al.22 This imaging
study revealed that the motor foot
representation in individuals with
congenitally compromised hand
function and compensatory skillful
foot use had extended beyond the
classical foot area into the vicinity ofthe lateral hand area.
Theoretical ConsiderationsVarious Theoretical FrameworksDespite increasing knowledge of the
developmental processes in the hu-
man brain, our understanding of the
neural 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 of
the previous century, motor devel-
opment basically was regarded as an
innate, maturational process,23,24 but
during the centurys last 2 decades, it
became increasingly clear that motor
development is largely affected by
experience.
Currently, 2 theoretical frameworks
are most popular: dynamic systems
theory2527 and NGST.28,29 The
frameworks share the opinion that
motor development is a nonlinear
process with phases of transition
that is affected by many factors. The
factors may vary from features of the
child to external influences such as
housing conditions, the presence of
stimulating caregivers, and the pres-
ence of toys. In other words,
both theories acknowledge the
importance of experience and the
relevance of context. The 2 theo-
ries differ, however, in their opin-
i on on the r ol e of genetically
determined neurodevelopmental
processes. Genetic factors playonly a limited role in dynamic sys-
tems theory, whereas genetic en-
dowment, epigenetic cascades, and
experience play equally prominent
roles in NGST.28,29 In the following
paragraphs, I will use the NGST
framework to discuss principles of
typical and atypical motor
development.
NGST and Typical MotorDevelopment
The NGST was developed by GeraldEdelman. He described motor devel-
opment as characterized by 2 phases
of variability: primary and second-
ary.28,29 The borders of variability are
determined by genetic instruc-
tions.1,15 During the phase of pri-
mary variability, motor behavior is
characterized by abundant variation.
The variation is brought about by
explorative activity of the nervous
system. The system explores all mo-
tor possibilities. The explorationgenerates a wealth of self-produced
afferent information, which, in turn,
is used for further shaping of the
nervous system. The exploration re-
flects the continuous, dynamic inter-
action between genes and experi-
ence, including experience with
changing body proportions. Initially,
however, the afferent information
is not used for adaptation of motor
behavior to environmental con-
straints. In other words, the phase of
primary variability is characterized
by variation in motor behavior and
the absence of the ability to adapt
the various movement possibilities
to 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 secondaryvariability are not understood. Theprocess of selection, which is char-acteristic of variability and thusthe phase of secondary variability,is based on active trial-and-error
experiences 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 function
specific. 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 perturbations
of 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 the
most 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 temporal
cortex 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; in
the 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 increasingly
precise 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 structural
anomaly or lesion of the developing
brain or in a different setting of spe-
cific neurotransmitter systems, such
as the monoaminergic systems. Ac-
cumulating evidence indicates thatstressful situations in the prenatal
and perinatal periods may induce
lifetime changes in dopaminergic, se-
rotonergic, or noradrenergic circuit-
ries.50 The monoaminergic systems
are widespread systems involved in
the modulation of behavior.51 The 2
sequelaethe lesion of the brain and
the different setting of the monoam-
inergic systemswill be discussed
as different entities, but it should be
kept in mind that lesions of the im-
mature brain often are associatedwith changes in specific neurotrans-
mitter systems.52
The best example of atypical motor
development due to an early lesion
of 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 with
attention deficit hyperactivity disor-
der. It is important to note, however,that in general developmental coor-
dination disorder and attention defi-
cit hyperactivity disorder cannot be
attributed to a lesion of the brain.53
In the following paragraphs, CP is
used as a prototype to describe the
motor sequelae of a lesion occurring
in the fetal or infant brain.54
NGST and an Early Lesion ofthe Brain
According to NGST, an early lesion
of the brain has 2 major consequenc-
es.55 First, the repertoire of motor
strategies is reduced.5659 This re-
duced repertoire results in less vari-
able and more stereotyped motor
behavior (ie, in reduced variation
during both phases of variability).
The limited repertoire may result in
the absence of a specific motor strat-
egy, which would be available as the
best solution in a specific situation
for a child with typical development.
As a consequence of the absence
of the best solution, the child with
CP 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 with
CP should not always be regarded as
deviant (ie, as something that de-
serves to be treated away), as it
may be the childs best and most
adaptive solution for the situation.61
Second, in the phase of secondary
variability, children with an early le-
sion of the brain have problems with
selection of the most appropriately
adapted strategy out of the reper-
toire. In other words, they have alimited capacity to vary motor behav-
ior in relation to the specifics of the
situation (ie, they have a limited
variability).
The deficient capacity to select has a
dual origin: it is related to deficits in
the processing of sensory informa-
tion that are virtually always present
in children with an early lesion of
the brain6267 and to the fact that the
best solution may not be availabledue to repertoire reduction. The dif-
ficulties in selection have 2 practical
consequences. First, impaired selec-
tion may give rise to the paradoxical
finding that results of motor tests of
children with CP often are more vari-
able than those of children with typ-
ical development.67,68 The variable
test results are brought about by pro-
longed periods of trial and error
needed 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 induces
the need of ten- to hundredfold more
active motor experience than typi-
cally needed to find the best strate-
gy.69,70 Consequentially, children
with CP need considerably more
practice than their peers without CP
to 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 spontaneously
generate a wealth of everyday motor
practice.35
The child with CP needsmuch more practice. In addition, the
brain lesion responsible for CP may
be associated with reduced explor-
atory drive.54 This reduced explor-
atory drive creates a challenging sit-
uation for the child with CP and his
or her environment. The need for
much practice requires strong moti-
vation, which is obtained most easily
when tasks to be learned have func-
tional significance or are enjoyable.
NGST and an Altered Setting ofMonoaminergic Systems
Adversities prior to term age, such as
low-risk preterm birth, intrauterine
growth retardation, or psychological
stress of the pregnant woman, may
give rise to a different setting of the
monoaminergic systems in the ab-
sence of a lesion of the brain. Most of
our knowledge about the effect of
stressful conditions during early life
on the developing brain is based on
animal data.50
The animal data indi-cate that stress during early life gives
rise to changes in serotonergic and
noradrenergic activity in the cerebral
cortex and alterations in dopaminer-
gic activity in the striatum and pre-
frontal cortex.71 These changes have
been associated with impaired devel-
opment of the maps of body repre-
sentation in the primary somato-
sensory cortex, inappropriately
developed ocular dominance col-
umns in the visual cortex, and mild
motor problems.7274 In terms of
NGST, this impaired development
may reflect a situation in which the
child has a typical movement reper-
toire but has difficulties in selecting
the best strategy in a specific situa-
tion due to the deficits in processing
of sensory information. In other
words, the child has an impaired
ability to vary motor behavioran
impaired variabilityin relation to
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task-specific requirements. As a re-sult, the child often exhibits more
variable behavior during motor tests
and 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 or
trunk. 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 as
isolated 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, elegant
movements 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 of
specific developmental phases, andvariation 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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months.49 These findings mean that
after the transition, people observing
the infants could notice a change in
their motor behavior.
A major accomplishment during in-
fancy is the development of pos-
tural control, resulting in the ability
to stand and walk without sup-
port.87 Postural control is aimed
primarily at the maintenance of a
vertical posture of head and trunk
against the forces of gravity be-
cause a vertical orientation of the
proximal parts of the body provides
an optimal condition for vision- and
goal-directed motility.88 In the con-
trol of posture, 2 functional levels
can be distinguished. The basic level
of control deals with the directional
specificity of the adjustments: when
the body sways forward, primarily
the dorsal muscles are recruited;
when the body sways backward, pri-
marily the ventral muscles are acti-
vated.89 A study by Hedberg et al90
indicated that 1-month-old infants
have direction-specific adjustments,
which suggests that the basic level of
postural control has an innate origin.
Young infants show a variable reper-
toire of direction-specific adjustments
from which, from the age of 4 months
onward, they learn to select by
means of active trial and error the ad-
justment that fits the situation best.46
Meanwhile, the infant learns to sit in-
dependently. With increasing age, the
means to adapt postural activity be-
come increasingly refined. A major de-
velopmental change is the emergence
of anticipatory postural activity be-
tween 12 to 14 months, an ability that
strongly promotes the development of
independent walking.87
Successful reaching is preceded by
various forms of prereaching activi-
ty.91 For instance, Von Hofsten92
demonstrated that newborn infants
move their hands closer to a nearby
object when they visually fixate on
it, than when they do not pay visual
attention to the object. Reaching
Figure 1.Variation in motor behavior in a supine position at 8 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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results in actual grasping of an object
from about 4 months onward.93 At
this age, reaching movements have
an irregular and fragmented trajec-
tory consisting of multiple movement
units. These characteristics under-
line the probing nature of early
reaches and the heavy reliance of the
first reaching movements on feed-
back control mechanisms.93 During
the following months, the reaching
movement becomes increasingly flu-
ent and straight, and the orientation
of the hand becomes increasingly
adapted to the object.94 After their
first birthday, infants increasingly
use the pincer grasp to pick up tiny
objects. This change in behavior
implies that corticomotoneuronal
pathways 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 fetus
shows locomotor-like behavior in
the form of neonatal stepping move-
ments.96 These movements probably
are generated by spinal pattern gen-
erators analogous to the locomotionin the hind limbs of kittens after a
transection of the thoracic cord and
the locomotor-like activity in people
with a spinal cord injury.96 The in-
fant stepping movements are rather
primitive in character and differ from
the flexible plantigrade gait of adult-
hood.97 This non goal-directed neo-
natal stepping is characterized by a
lack of segment-specific movements,
implying that the legs tend to flex
and extend as a single unit; by the
absence of a heel-strike; by a variablemuscle activation with a high degree
of antagonistic coactivation; and by
short-latency bursts of electromyo-
graphic activity at the foot contact
due to segmental reflex activity.96,97
In the absence of specific training,
the stepping movements can no
longer be elicited after the age of 2 to
3 months.83
A period of locomotor silence fol-
lows, which is succeeded in thethird quarter of the first postnatal
year by goal-directed progression in
the form of crawling and supported
locomotion. When neonatal step-
ping is trained daily, the stepping
response can be elicited until it is
replaced by supported locomo-
tion.98 This progression is perhaps
not so surprising in light of the fact
that the locomotor pattern of sup-
ported locomotion is reminiscent
of that of neonatal steppingboth
lacking the determinants of planti-
grade gait.97 In addition, the mile-
stone transition into independent
walking is not associated with a ma-
jor change in specific locomotor ac-
tivity. This finding indicates that the
emergence of independent locomo-
tion is not primarily induced by
changes in the locomotor networks.
Presumably, the development of in-
dependent walking is largely depen-
dent on the development of postural
control,99 which, in turn, is depen-
dent in particular on developmental
changes in the subcortical-cortical
circuitries.96
Motor development beyond infancy
is characterized by a gradual increase
in 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 highly
adaptive secondary neuronal reper-
toires.24,28 The creation of secondary
repertoires is associated with exten-
sive synapse rearrangement, which
is the net result of synapse formation
and 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 on
the expression of atypical motor be-
havior. It may happen that a lesion of
the developing brain results in neu-
romotor dysfunction in infancy but
is followed by a typical developmen-
tal outcome. The reverse may also
occur (ie, an apparently typical de-
velopment in the early phases of
infancy may be followed by the de-
velopment of CP).58
In infancy, atypical motor develop-
ment may be expressed by a delay
in the achievement of milestones
(which may be related to impairedselection), by mild or major devia-
tions in muscle tone (velocity-
dependent resistance to stretch), by
a persistence of infantile reactions
(eg, the Moro reaction), and by a
reduced variation in motor behavior.
The latter sign may be the most spe-
cific expression of an early lesion of
the brain,55,58,101 whereas the other
signs may be the result of a lesion of
the brain but also may be related to
other types of adversities during
early development, such as low-risk
preterm 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 GMs
are related to white matter pathol-
ogy and not to abnormalities of the
brains 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 and
5). Well-known stereotypies are fist-
ing of the hands, extension of the
legs, clawing of the toes, dominant
asymmetrical tonic neck reflex pos-
turing, hyperextension of the neck
and trunk, or stereotyped asymme-
tries.106 It has been postulated that
the degree to which movement vari-
ation is reduced may reflect the ex-
tent to which cortical connectivity is
impaired.79,107
Atypical motor development is asso-
ciated with postural dysfunction.
Children with a severe lesion of the
brain who develop severe bilateral
spastic CP or severe athetosis and
function at Gross Motor Function
Classification 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 of
postural organization is more or less
intact. However, their postural de-
velopment is hamperedand, there-
fore, delayedby a limited reper-
toire of postural adjustments and a
deficient capacity to adapt posture
to the specifics of the situation.109
Diagnostic Application ofVariation and VariabilityGradually, European clinicians work-
ing in the field of developmental
neurology realized that variation and
variability may assist in the evalua-tion of motor development. How-
ever, before addressing the value of
these parameters, some general re-
flections on the significance of the
infant neuromotor assessment are
necessary. Evaluation of neuromotor
function in early life has 2 goals. First
and foremost, it aims at assessing
the infants current capacities and
limitations, 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 early
age may assist in the prediction of
the infants developmental pros-
pects. However, as indicated in the
preceding paragraphs, the develop-
mental characteristics of the brain
preclude precise prediction. Predic-
tion of developmental outcome is
best when multiple sources of infor-
mation are used, such as the infants
history, the results of neuroimaging,
and neurophysiological assessments
in combination with a neurological,
developmental, and neuromotor as-
sessment.110 Prediction also is largely
facilitated when longitudinal series
of assessments are used.104,111
The various instruments available to
evaluate 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 specific
aims, advantages, and disadvantages.
Most instruments provide informa-
tion on the childs function in terms
of age-adequate performance versus
underachievement or delay. Exam-ples are the Bayley Scales of Infant
Development112 and the Albert In-
fant Motor Scales.113 Neurological as-
sessments pair information on motor
performance with specific details on
sensorimotor function in terms of
muscle tone and reflexes.110 The
growing awareness that the quality
of motor behavior may assist in the
evaluation of the childs neuromotor
condition inspired the development
of 3 new assessment methods; the
Test of Infant Motor Performance(TIMP),114 the GM method,58,115 and
the Infant Motor Profile (IMP).116
The TIMP and the GM method are
applicable till the age of 4 months
postterm, whereas the IMP is de-
signed for infants aged 3 to 18
months postterm. In contrast to the
other 2 instruments, the TIMP does
not 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 the
prediction of CP.110 The 2 methods
using the concepts of variation and
variability are discussed below. Vari-
ation (ie, the evaluation of the size of
the repertoire) is a parameter that
may be applied in the phase of pri-
mary and secondary variability. Vari-
ability (ie, the ability to make an
adaptive selection) is particularly rel-
evant from the emergence of second-
ary variability onward.
The examination of the quality of
GMs is a reliable assessment based
on 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 of
secondary variability.24 In the GM
method, 2 aspects of variation are
assessed: (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 mildly
abnormal GMs, complexity and vari-
ation are present, but to an insuffi-
cient extent.58 The consistent pres-
ence of definitely abnormal GMs
during the first postnatal months is
associated with a very high risk for
the 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 around
3 months postterm). In populations
of infants who are at risk for CP,
definitely abnormal GMs at 3 months
are associated with a risk of CP
that varies between 25% and
80%,79,115,117 whereas mildly abnor-
mal GMs are associated with an in-
creased risk of minor neurological
dysfunction and psychiatric morbid-
ity at school age.118,119 It should be
noted, however, that the predictivepower of mildly abnormal GMs at 3
months is so low that mildly abnor-
mal GMs as a single sign have no
clinical relevance. The recent finding
that the predictive value of GM qual-
ity is substantially higher in popula-
tions of infants who are at risk for CP
than in the general population120
supports the idea that the quality of
GMs reflects the integrity of cortical
connectivity (ie, the integrity of the
brains white matter), as large parts
of the brains white matter are situ-
ated in the periventricular area,
which is the site of predilection for
damage in the preterm period.121
The IMP is a novel instrument that
assesses infant motor behavior in 5
domains. Two domains are based on
the NGST: size of the repertoire
(variation) and ability to select (vari-
ability). The other 3 domains evalu-
ate more traditional aspects of motor
behavior: symmetry, fluency, and
performance.76,116 The reliability and
construct validity of the IMP are
good, and its predictive and evalua-
tive power is promising.76,116
Concluding RemarksAccumulating evidence indicates
that abundance in cerebral connec-
tivity is the neural basis of human
behavioral variability (ie, the ability
to select from a large repertoire of
behavioral solutions the one most
appropriate for a specific situation).
Indeed, typical human motor devel-
opment is characterized by variation
and 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 on
structural anomalies, in which distur-
bances of cortical connectivity may
play a prominent role, whereas limi-
tations in variability are present in
virtually all children with atypical
motor development. In infants with
reduced variation, early intervention
may aim to enlarge the limited move-
ment repertoire, but animal data in-dicate that this aim is difficult to
achieve.52 This situation implies
thatdespite interventionreper-
toire reduction most likely will re-
main a feature of the motor behavior
of the child with an early lesion of
the brain. In such a situation, equip-
ment may offer a proper means to
facilitate functional activity and
participation.
The limited variability of childrenwith atypical motor development is
based on the limited ability to select
a strategy out of the movement rep-
ertoire due to deficiencies in the
processing of sensory information
brought about by self-produced ac-
tions. This fact suggests that children
with limited variability may profit
from ample, variable, self-produced,
trial-and-error activities.122,123
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