Pediatrics

Special Issue

Variation and Variability: Key Words in

Human Motor Development
Mijna Hadders-Algra
M. Hadders-Algra, MD, PhD, is
Professor of Developmental Neu-
This article reviews developmental processes in the human brain and basic principles
rology, Department of Pediatrics–
underlying typical and atypical motor development. The Neuronal Group Selection Developmental Neurology, Uni-
Theory is used as theoretical frame of reference. Evidence is accumulating that versity Medical Center Groningen,
abundance in cerebral connectivity is the neural basis of human behavioral variability University of Groningen, Hanz-
(ie, the ability to select, from a large repertoire of behavioral solutions, the one most eplein 1, 9713 GZ Groningen, the
Netherlands. Address all corre-
appropriate for a specific situation). Indeed, typical human motor development is
spondence to Dr Hadders-Algra
characterized by variation and the development of adaptive variability. Atypical at: [email protected].
motor development is characterized by a limited variation (a limited repertoire of nl.
motor strategies) and a limited ability to vary motor behavior according to the
[Hadders-Algra M. Variation and
specifics of the situation (ie, limited variability). Limitations in variation are related variability: key words in human
to structural anomalies in which disturbances of cortical connectivity may play a motor development. Phys Ther.
prominent role, whereas limitations in variability are present in virtually all children 2010;90:xxx–xxx.]
with atypical motor development. The possible applications of variation and variabil- © 2010 American Physical Therapy
ity in diagnostics in children with or at risk for a developmental motor disorder are Association
discussed.

Post a Rapid Response to

this article at:
ptjournal.apta.org

December 2010 Volume 90 Number 12 Physical Therapy f 1

Variation and Variability in Human Motor Development

H
uman behavior is character- the human brain. Sections on theo- the subplate. Neuronal differentia-
ized by variation: each human retical considerations and typical tion includes the formation of den-
individual has a large reper- and atypical motor development fol- drites and axons, the production of
toire of motor, cognitive, and social low. The emphasis is on the early neurotransmitters and synapses, and
actions that can be arranged in phases of development and the Neu- the elaboration of the intracellular
virtually endless combinations. This ronal Group Selection Theory signaling machinery and complex
repertoire allows for a flexible ad- (NGST) is used as a frame of refer- neural membranes.11,12 The process
justment to changing conditions, ence. The NGST was chosen because of differentiation is particularly ac-
including the creation of new it highlights that variation and vari- tive in the few months prior to birth
solutions. ability are key elements of typical and the first postnatal months, but it
development. Variation implies the takes many years before the adult
The wealth of distinctly human be- presence and expression of a broad state of differentiation is achieved.5
havior is attributed to the neocortex, repertoire of behaviors for a specific Besides neural cells, glial cells are
the part of the brain that expanded motor function. Variability denotes generated. The peak of glial cell pro-
greatly during evolution.1,2 For in- the capacity to select from the rep- duction occurs in the second half of
stance, in insectivores such as the ertoire the motor strategy that fits gestation. Some of the glial cells take
hedgehog, the neocortex occupies the situation best. The article con- care of axonal myelination. Myelina-
10% to 20% of total brain volume, cludes with possible applications of tion takes place especially between
whereas this proportion has risen to variation and variability in diagnos- the second trimester of gestation and
about 80% in humans.3 The enlarge- tics in infants with or at risk for a the end of the first postnatal year.
ment of the neocortex has been developmental motor disorder. Thereafter, myelination continues
brought about mainly by expansion till the age of about 40 years, when
of the surface area and not so much Development of the the last intracortical connections
by an increase in cortical thickness.2 Human Brain complete myelination.13
The expansion of cortical surface al- The development of the human
lowed for the emergence of new ar- brain, and in particular, that of the Brain development consists not only
eas (eg, language-related areas) and neocortical circuitries, lasts about 4 of creation of components, but also
the extension of the prefrontal cor- decades.5 It starts during the early of an elimination of elements. About
tex and association areas. Interest- phases of gestation with the prolifer- half of the created neurons die off
ingly, the volume of the white mat- ation of neurons. The majority of tel- by means of apoptosis. Apoptosis is
ter—mostly consisting of cortico-cor- encephalic neurons are produced in brought about by interaction be-
tical connections—increased more the germinal layers near the ventri- tween endogenous programmed
during the evolutionary expansion cles.2,6 Once neurons have been gen- processes and chemical and electri-
of the cortex than the volume of gray erated, they move from their place of cal signals induced by experience14;
matter.3,4 origin to their final destination, the it occurs in particular during mid-
cortical plate.6,7 Before the cortical gestation.5 Similarly, axons and syn-
The development of the human plate is formed, however, neurons apses are eliminated, the latter espe-
brain is an intricate and long-lasting halt in the subplate. The subplate is a cially between the onset of puberty
process, which is mirrored by a mul- temporary layer between the ven- and early adulthood. As a result, the
titude of developmental changes in tricular zones plus intermediate zone adult level of synaptic density in
behavior. The latter include the (the future white matter) and the the cortex is reached first in early
changes involved in the transfor- cortical plate.8 The subplate emerges adulthood.5
mation of non– goal-directed fetal in early fetal life, is thickest at around
motility into the accurate and goal- 29 weeks postmenstrual age (PMA), For a long time, it had been debated
directed movements of an adult per- and disappears gradually until it is whether brain development is
son, such as those involved in writ- absent at around 6 months post- driven by endogenous processes or
ing a letter or riding a bike. The aim term.9,10 The major proportion of its by external input. Gradually, how-
of this article is to discuss putative afferent and efferent connections ever, it became clear that genetic in-
mechanisms and principles underly- run through the (future) periven- struction (“nature”) and environ-
ing developmental changes in motor tricular white matter. The subplate mental information (“nurture”) both
behavior. Particular attention is paid mediates fetal behavior. play an important role, albeit with
to the notions of “variation” and different weights during different
“variability.” The article starts with a Neurons start to differentiate during phases of development. In the early
short overview of the ontogeny of migration and during their stay in phases, the role of the genome dom-

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 Variation and Variability in Human Motor Development

inates; later on, environment and ex- and compensatory skillful foot use NGST and Typical Motor
perience become crucial. The impor- had extended beyond the classical Development
tance of genetic instruction in early foot area into the vicinity of the lat- The NGST was developed by Gerald
development is reflected by animal eral hand area. Edelman. He described motor devel-
studies that indicated the primary opment as characterized by 2 phases
cortical areas, their connections, Theoretical Considerations of variability: primary and second-
their modular organization, and their Various Theoretical Frameworks ary.28,29 The borders of variability are
size are largely determined by differ- Despite increasing knowledge of the determined by genetic instruc-
ential gene expression in the neural developmental processes in the hu- tions.1,15 During the phase of pri-
stem cells.1,15 Thus, the genetically man brain, our understanding of the mary variability, motor behavior is
specified areas attract specific inputs neural mechanisms underlying mo- characterized by abundant variation.
instead of inputs specifying the ar- tor development is limited. As a re- The variation is brought about by
eas.2 This means that the functional sult, multiple theories of motor de- explorative activity of the nervous
topography of the brain is primarily velopment have been produced, all system. The system explores all mo-
driven by genetic instruction (ie, the aiming to facilitate the understand- tor possibilities. The exploration
fact that occipitally located neurons ing of typical and atypical motor de- generates a wealth of self-produced
virtually always become involved in velopment. During the major part of afferent information, which, in turn,
the processing of visual information the previous century, motor devel- is used for further shaping of the
and frontally located networks in ac- opment basically was regarded as an nervous system. The exploration re-
tivities such as planning and atten- innate, maturational process,23,24 but flects the continuous, dynamic inter-
tion). A primary genetic determina- during the century’s last 2 decades, it action between genes and experi-
tion, however, does not preclude became increasingly clear that motor ence, including experience with
variation, as each individual has his development is largely affected by changing body proportions. Initially,
or her own sets of genes. Moreover, experience. however, the afferent information
the primary genetic determination is is not used for adaptation of motor
only the starting point for epigenetic Currently, 2 theoretical frameworks behavior to environmental con-
cascades, allowing for abundant in- are most popular: Dynamic Systems straints. In other words, the phase of
teraction with the environment and Theory25–27 and NGST.28,29 The primary variability is characterized
activity-dependent processes.16 –18 frameworks share the opinion that by variation in motor behavior and
Note that the interaction is bidirec- motor development is a nonlinear the absence of the ability to adapt
tional: experience affects gene ex- process with phases of transition the various movement possibilities
pression, and genes affect how the that is affected by many factors. The to the specifics of the situation (ie,
environment is experienced.18 factors may vary from features of the by the absence of variability in sensu
child to external influences such as strictu, as defined in the introduc-
Virtually all of the neurodevelop- housing conditions, the presence of tion of the article).24
mental processes described above stimulating caregivers, and the pres-
are affected by experience, includ- ence of toys. In other words, both At a certain point in time, the ner-
ing motor experience. Animal stud- theories acknowledge the impor- vous system starts to use the afferent
ies have demonstrated that the effect tance of experience and the rele- information produced by behavior
depends on the type of experience vance of context. The 2 theories and experience for selection of the
(eg, specific versus generalized mo- differ, however, in their opinion on motor behavior that fits the situa-
tor experience), the age at exposure, the role of genetically determined tion best: the phase of secondary or
the individual’s sex, and the neural neurodevelopmental processes. adaptive variability starts. Hitherto,
area.18,19 Experience may affect, for Genetic factors play only a limited the mechanisms underlying the shift
instance, apoptosis, axon retraction, role in Dynamic Systems Theory, from primary variability to secondary
synapse elimination, and synapse for- whereas genetic endowment, epi- variability are not understood. The
mation.19 –21 It may even affect the genetic cascades, and experience process of selection, which is char-
somatotopic organization of the pri- play equally prominent roles in acteristic of variability and thus
mary motor cortex, as was indicated NGST.28,29 In the following para- the phase of secondary variability,
by the recent human study by graphs, I will use the NGST frame- is based on active trial-and-error
Stoeckel et al.22 This imaging study work to discuss principles of typical experiences that are unique to the
revealed that the motor “foot” repre- and atypical motor development. individual.30 –32 Indeed, evidence is
sentation in individuals with congen- accumulating that self-produced sen-
itally compromised hand function

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Variation and Variability in Human Motor Development

sorimotor experience plays a pivotal in motor sequence learning),32,41 ondary variability. Due to the in-
role in motor development.31,33–35 whereas the cerebellum might be genious interaction between self-
the key structure involved in the se- produced motor activities with trial-
To determine whether a movement lection of situation-specific temporal and-error learning and the long-
is most adaptive, reference values and quantitative parameters of mo- lasting developmental processes in
are used that most likely are function tor output (ie, accurate motor adap- the brain, such as dendritic refine-
specific. The solution that is selected tation).42,43 The idea that frontostria- ment, myelination, and extensive
is specific for the situation and the tal circuitries play a role in the synapse rearrangement,5 which fur-
infant’s stage of development. For selection of motor strategies is sup- nish new neuromotor possibilities, it
instance, in sitting infants whose ported by a recent birth cohort study takes until late adolescence before
balance is perturbed, information by Murray et al.44 The study indi- the secondary neural repertoire has
linked to the stability of the head in cated that an earlier development of obtained its adult configuration. In
space is used to select the postural the ability to stand independently— other words, the basic, variable mo-
adjustment in which most of the which might be interpreted as an tor repertoire that is formed during
so-called direction-specific postural earlier ability to select an appropri- the phase of primary variability con-
muscles are recruited (the en bloc ate strategy to keep balance in up- tinues to develop during the phase
pattern).36 Selection of the en bloc right stance—was associated with of secondary variability and to
pattern depends on the degree of better executive functions in adult- change throughout life.
balance perturbation—the pattern is hood. The association was specific
recruited more often during large for executive functions, which are The ongoing developmental changes
perturbations than during small subserved by frontostriatal circuit- in the nervous system, which are
perturbations—and the age of the ries; other cognitive functions such based on a never-ending interaction
child.36,37 Children select the en bloc as verbal and visual learning, which between experience and genetic in-
pattern during marked perturbations are more closely related to temporal formation, allow for increasingly
of balance especially often between cortex function, were not related to precise and complex motor skills,
the ages of 9 months and 21⁄2 years. an earlier development of standing. which may be regarded as refine-
Thereafter, similar perturbations of ments of the basic, variable reper-
balance are associated with child- The transition from primary variabil- toire. As a result, adult human beings
specific postural adaptations in ity to secondary variability occurs at are equipped with a variable move-
which fewer direction-specific mus- function-specific ages. For instance, ment repertoire with an efficient
cles are recruited.37 in the development of sucking be- motor solution for each specific
havior, the phase of secondary vari- situation.
The process of learning to select the ability starts prior to term age45; in
most appropriate motor solution the development of postural adjust- NGST and Atypical Motor
in a specific situation is based on ment, it emerges after the age of 3 Development
implicit motor learning and does not months46,47; and in the development Atypical motor development may
involve conscious decision making. of foot placement during walking, it originate from genetic aberrations
It occurs at various interdependent starts between 12 and 18 months.48 or adversities occurring during early
levels of neural organization. Animal The age at which adaptive behavior development. Both etiological path-
data indicate that at the cellular level, first can be observed depends on the ways may result in a structural anom-
selection is mediated by changes in method of investigation. For in- aly or lesion of the developing brain
synaptic strength, in which the to- stance, with the application of elec- or in a different setting of specific
pology of the cells38 and the pres- tromyographic recordings, the first neurotransmitter systems, such as
ence or absence of coincident elec- signs of adaption in postural behav- the monoaminergic systems. Accu-
trical activity in presynaptic and ior during sitting may be observed mulating evidence indicates that
postsynaptic neurons play a role.39,40 at the age of 4 months,46 but when stressful situations in the prenatal
In terms of the organization of motor simple behavioral observation is and perinatal periods may induce
control, selection occurs at the level used, signs of adaptive sitting behav- lifetime changes in dopaminergic, se-
of motor strategies and at the level of ior are first detected from 6 months rotonergic, or noradrenergic circuit-
temporal and quantitative tuning of onward.49 Around the age of 18 ries.50 The monoaminergic systems
motor output.36 Recent neurophysi- months, all basic motor functions, are widespread systems involved in
ological data indicated that the basal such as sucking, reaching, grasping, the modulation of behavior.51 The 2
ganglia might play a major role in postural control, and locomotion, sequelae—the lesion of the brain and
the selection of motor strategies (ie, have reached the first stages of sec- the different setting of the monoam-

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 Variation and Variability in Human Motor Development

inergic systems—will be discussed brain have problems with selection when tasks to be learned have func-
as different entities, but it should be of the most appropriately adapted tional significance or are enjoyable.
kept in mind that lesions of the im- strategy out of the repertoire. In
mature brain often are associated other words, they have a limited ca- NGST and an Altered Setting of
with changes in specific neurotrans- pacity to vary motor behavior in re- Monoaminergic Systems
mitter systems.52 lation to the specifics of the situation Adversities prior to term age, such as
(ie, they have a limited variability). low-risk preterm birth, intrauterine
The best example of atypical motor growth retardation, or psychological
development due to an early lesion The deficient capacity to select has a stress of the pregnant woman, may
of the brain is the motor develop- dual origin: it is related to deficits in give rise to a different setting of the
ment of children with cerebral palsy the processing of sensory informa- monoaminergic systems in the ab-
(CP). Other examples are some chil- tion that are virtually always present sence of a lesion of the brain. Most of
dren with developmental coordina- in children with an early lesion of our knowledge about the effect of
tion disorder and some children with the brain62– 67 and to the fact that the stressful conditions during early life
attention deficit hyperactivity disor- best solution may not be available on the developing brain is based on
der. It is important to note, however, due to repertoire reduction. The dif- animal data.50 The animal data indi-
that in general developmental coor- ficulties in selection have 2 practical cate that stress during early life gives
dination disorder and attention defi- consequences. First, impaired selec- rise to changes in serotonergic and
cit hyperactivity disorder cannot be tion may give rise to the paradoxical noradrenergic activity in the cerebral
attributed to a lesion of the brain.53 finding that results of motor tests of cortex and alterations in dopaminer-
In the following paragraphs, CP is children with CP often are more vari- gic activity in the striatum and pre-
used as a prototype to describe the able than those of children with typ- frontal cortex.71 These changes have
motor sequelae of a lesion occurring ical development.67,68 The variable been associated with impaired devel-
in the fetal or infant brain.54 test results are brought about by pro- opment of the maps of body repre-
longed periods of trial and error sentation in the primary somato-
NGST and an Early Lesion of needed to explore the reduced rep- sensory cortex, inappropriately
the Brain ertoire due to impaired selection. developed ocular dominance col-
According to NGST, an early lesion This consequence means that a re- umns in the visual cortex, and mild
of the brain has 2 major consequenc- duced repertoire may be associated motor problems.72–74 In terms of
es.55 First, the repertoire of motor with more variable motor output. NGST, this impaired development
strategies is reduced.56 –59 This re- Second, impaired selection induces may reflect a situation in which the
duced repertoire results in less vari- the need of ten- to hundredfold more child has a typical movement reper-
able and more stereotyped motor active motor experience than typi- toire but has difficulties in selecting
behavior (ie, in reduced variation cally needed to find the best strate- the best strategy in a specific situa-
during both phases of variability). gy.69,70 Consequentially, children tion due to the deficits in processing
The limited repertoire may result in with CP need considerably more of sensory information. In other
the absence of a specific motor strat- practice than their peers without CP words, the child has an impaired
egy, which would be available as the to learn a specific motor task. ability to vary motor behavior—an
best solution in a specific situation impaired variability—in relation to
for a child with typical development. Recall that exploratory drive is a fun- task-specific requirements. As a re-
As a consequence of the absence of damental feature of the typically de- sult, the child often exhibits more
the “best” solution, the child with CP veloping nervous system. As a result, variable behavior during motor tests
may have to choose a motor solution young infants spontaneously gener- and needs more practice—and thus
that differs from that of the child ate a wealth of everyday motor prac- more time—to learn new motor
with typical development.60 This sit- tice.35 The child with CP needs skills. Indeed, such mechanisms ap-
uation implies that the different much more practice. In addition, the pear to play a role in the frequently
motor behavior of a child with CP brain lesion responsible for CP may encountered impaired motor devel-
should not always be regarded as de- be associated with reduced explor- opment of preterm children without
viant (ie, as something that deserves atory drive.54 This reduced explor- cerebral palsy.59,75,76
to be “treated away”), as it may be atory drive creates a challenging sit-
the child’s best and most adaptive uation for the child with CP and his
solution for the situation.61 Second, or her environment. The need for
in the phase of secondary variability, much practice requires strong moti-
children with an early lesion of the vation, which is obtained most easily

December 2010 Volume 90 Number 12 Physical Therapy f 5

Variation and Variability in Human Motor Development

Early Phases of Motor dividual variation, but at about 16 and 2), variation in the duration of
Development weeks PMA, all fetuses exhibit the specific developmental phases, and
Typical Motor Development entire fetal repertoire. The reper- variation in the disappearance of in-
Non– goal-directed motility. A toire continues to be present fantile reactions, such as the Moro
recent, detailed ultrasound study on throughout gestation. reaction. The variation in develop-
the emergence of fetal motility re- ment includes the co-occurrence of
vealed that the earliest movements At birth, be it term or preterm, only different developmental phases. For
can be observed at the age of 7 minor changes in the motor reper- instance, infants of a certain age can
weeks 2 days PMA.77 The first move- toire occur. Breathing movements alternate belly crawling with crawl-
ments are slow, small, sideways become continuous instead of peri- ing on hands and knees.83,85 Infants
bending movements of head or odic, the Moro reaction can be elic- with typical development also may
trunk. A few days later, these simple ited for the first time, and the infant, exhibit a temporary regression—an
movements develop into move- who is now hampered by the forces “inconsistency”—in the develop-
ments in which 1 or 2 arms or legs of gravity, is no longer able to ante- ment of a specific function.83 As long
also participate, but the movements flex the head in a supine position.81 as the regression is restricted to a
continue to be slow, small, simple, General movements continue to be single function, it can be regarded as
and stereotyped. At the age of 9 to 10 the most frequently observed motor another expression of developmen-
weeks PMA, general movements pattern. tal variation. Large variation in the
(GMs) emerge (ie, movements in attainment of milestones in goal-
which all parts of the body partici- Between 2 and 4 months postterm, directed motor behavior (Fig. 3) im-
pate). Initially, GMs show little vari- infant behavior changes drastically. plies that the assessment of mile-
ation in movement direction, ampli- The infant is able to use smiles and stones has less clinical value than
tude, and speed. After a few days, pleasure vocalizations in social inter- previously was thought.86 Slow de-
however, the majority of GMs show action, the head can be stabilized on velopment of a single function usu-
a substantial degree of variation in the trunk, and a steady visual fixation ally has no clinical significance, but
speed, amplitude, participating body and brisk visual orienting reactions the finding of a general delay is clin-
parts, and movement direction. In- have been developed.81 Simulta- ically relevant.
terestingly, the emergence of GMs neously, GM activity is about to dis-
with movement variation and com- appear and to be replaced gradually Infancy is the period of transition
plexity at 9 to 10 weeks PMA coin- by goal-directed activity of arms and from primary variability to secondary
cides with the emergence of synap- legs. Interestingly, the final phase of variability (ie, from motor behavior
tic activity in the cortical subplate.78 GMs, which occurs at 2 to 4 months that cannot be adapted to task-
This coincidence and the finding postterm, is characterized by a spe- specific conditions to adaptive mo-
that the evolution and transient na- cific movement property: the “fidg- tor behavior). This transition occurs
ture of the subplate match that of ety” nature of GMs. The fidgety char- at function-specific ages. A recent
GM development inspired the hy- acter denotes the presence of a observational study indicated that
pothesis that variable and complex continuous stream of tiny, elegant the transition in sitting behavior oc-
GMs result from activity of the sub- movements occurring irregularly all curs between 6 and 10 months, that
plate modulating the basic activity of over the body.58 Functional neuroim- in abdominal progression occurs be-
GM networks in the spinal cord and aging studies suggest that increasing tween 8 and 15 months, that in
brain stem.79 activity in the basal ganglia, the cer- reaching movements occurs be-
ebellum, and the parietal, temporal, tween 6 and 12 months, and that in
Soon after the emergence of the first and occipital cortices plays a promi- grasping occurs between 15 and 18
movements, other movements are nent role in the behavioral transition months.49 These findings mean that
added to the fetal repertoire, such as at 2 to 4 months.82 after the transition, people observing
isolated arm and leg movements, the infants could notice a change in
startles, various movements of the Goal-directed motility. The de- their motor behavior.
head (rotations, anteflexion, and velopment of goal-directed behavior
retroflexion), stretches, periodic during infancy is characterized by in- A major accomplishment during in-
breathing movements, and sucking traindividual and interindividual vari- fancy is the development of postural
and swallowing movements.80 The ation.55,57,83,84 The variation occurs, control, resulting in the ability to
age at which the various movements for instance, as variation in the emer- stand and walk without support.87
develop shows considerable interin- gence of a function, variation in the Postural control is aimed primarily at
performance of a function (Figs. 1 the maintenance of a vertical posture

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 Variation and Variability in Human Motor Development

Figure 1.
Variation in motor behavior in a supine position at 8 months postterm. The figure consists of frames selected from a videorecording
of about 3 minutes. Figure produced with permission of the parents.

of head and trunk against the forces has an innate origin. Young infants Successful reaching is preceded by
of gravity because a vertical orienta- show a variable repertoire of various forms of prereaching activi-
tion of the proximal parts of the direction-specific adjustments from ty.91 For instance, Von Hofsten92
body provides an optimal condition which, from the age of 4 months on- demonstrated that newborn infants
for vision- and goal-directed motili- ward, they learn to select by means of move their hands closer to a nearby
ty.88 In the control of posture, 2 active trial and error the adjustment object when they visually fixate on
functional levels can be distin- that fits the situation best.46 Mean- it, than when they do not pay visual
guished. The basic level of control while, the infant learns to sit indepen- attention to the object. Reaching re-
deals with the directional specificity dently. With increasing age, the means sults in actual grasping of an object
of the adjustments: when the body to adapt postural activity become in- from about 4 months onward.93 At
sways forward, primarily the dorsal creasingly refined. A major develop- this age, reaching movements have
muscles are recruited; when the mental change is the emergence of an irregular and fragmented trajec-
body sways backward, primarily the anticipatory postural activity between tory consisting of multiple move-
ventral muscles are activated.89 A 12 to 14 months, an ability that ment units. These characteristics un-
study by Hedberg et al90 indicated that strongly promotes the development of derline the probing nature of early
1-month-old infants have direction- independent walking.87 reaches and the heavy reliance of the
specific adjustments, which suggests first reaching movements on feed-
that the basic level of postural control back control mechanisms.93 During

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Variation and Variability in Human Motor Development

Figure 2.
Variation in motor behavior in a sitting position at 11 months postterm. The figure consists of frames selected from a videorecording
of about 3 minutes. Figure produced with permission of the parents.

the following months, the reaching objects. This change in behavior im- the form of neonatal stepping move-
movement becomes increasingly flu- plies that corticomotoneuronal path- ments.96 These movements probably
ent and straight, and the orientation ways are being involved increasingly are generated by spinal pattern gen-
of the hand becomes increasingly in fine motor control.95 erators analogous to the locomotion
adapted to the object.94 After their in the hind limbs of kittens after a
first birthday, infants increasingly At birth, the infant—like the fetus— transection of the thoracic cord and
use the pincer grasp to pick up tiny shows locomotor-like behavior in the locomotor-like activity in people

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 Variation and Variability in Human Motor Development

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 variable
muscle 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 Figure 3.
longer be elicited after the age of 2 to Schematic representation of the ages at which some motor skills emerge during infancy.
3 months.83 The length of the bars reflect the interindividual variation. Adapted from Touwen.83

A period of locomotor silence fol-

lows, which is succeeded in the to make complex movement se- the achievement of milestones
third quarter of the first postnatal quences. It is the phase of secondary (which may be related to impaired
year by goal-directed progression in variability, during which matura- selection), by mild or major devia-
the form of crawling and supported tional processes in continuous inter- tions in muscle tone (velocity-
locomotion. When neonatal step- action with changing body propor- dependent resistance to stretch), by
ping is trained daily, the stepping tions and experience produce highly a persistence of infantile reactions
response can be elicited until it is adaptive secondary neuronal reper- (eg, the Moro reaction), and by a
replaced by supported locomo- toires.24,28 The creation of secondary reduced variation in motor behavior.
tion.98 This progression is perhaps repertoires is associated with exten- The latter sign may be the most spe-
not so surprising in light of the fact sive synapse rearrangement, which cific expression of an early lesion of
that the locomotor pattern of sup- is the net result of synapse formation the brain,55,58,101 whereas the other
ported locomotion is reminiscent of and synapse elimination.5 It is facili- signs may be the result of a lesion of
that of neonatal stepping— both tated by increasingly shorter pro- the brain but also may be related to
lacking the determinants of planti- cessing times, which can be attrib- other types of adversities during
grade gait.97 In addition, the mile- uted, in part, to ongoing early development, such as low-risk
stone transition into independent myelination.100 preterm birth.102–104 Reduced varia-
walking is not associated with a ma- tion in motor behavior is well ex-
jor change in specific locomotor ac- Atypical Motor Development pressed in the quality of GMs: abnor-
tivity. This finding indicates that the Developmental changes in the mal GMs are characterized by limited
emergence of independent locomo- young brain have a large impact on variation and limited complexity. In-
tion is not primarily induced by the expression of atypical motor be- terestingly, definitely abnormal GMs
changes in the locomotor networks. havior. It may happen that a lesion of are related to white matter pathol-
Presumably, the development of in- the developing brain results in neu- ogy and not to abnormalities of the
dependent walking is largely depen- romotor dysfunction in infancy but brain’s gray matter.79,105 Further-
dent on the development of postural is followed by a typical developmen- more, beyond the age of 4 months,
control,99 which, in turn, is depen- tal outcome. The reverse may also when GMs have disappeared, atypi-
dent in particular on developmental occur (ie, an apparently typical de- cal motor development is character-
changes in the subcortical-cortical velopment in the early phases of in- ized by reduced variation (Figs. 4 and
circuitries.96 fancy may be followed by the devel- 5). Well-known stereotypies are fist-
opment of CP).58 ing of the hands, extension of the
Motor development beyond infancy legs, clawing of the toes, dominant
is characterized by a gradual increase In infancy, atypical motor develop- asymmetrical tonic neck reflex pos-
in agility, adaptability, and the ability ment may be expressed by a delay in turing, hyperextension of the neck

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Variation and Variability in Human Motor Development

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

and trunk, or stereotyped asymme- postural organization is more or less flections on the significance of the
tries.106 It has been postulated that intact. However, their postural de- infant neuromotor assessment are
the degree to which movement vari- velopment is hampered—and, there- necessary. Evaluation of neuromotor
ation is reduced may reflect the ex- fore, delayed— by a limited reper- function in early life has 2 goals. First
tent to which cortical connectivity is toire of postural adjustments and a and foremost, it aims at assessing the
impaired.79,107 deficient capacity to adapt posture infant’s current capacities and limita-
to the specifics of the situation.109 tions, as the assessment offers the
Atypical motor development is asso- basis for therapeutic guidance. Sec-
ciated with postural dysfunction. Diagnostic Application of ond, an assessment at an early age
Children with a severe lesion of the Variation and Variability may assist in the prediction of the
brain who develop severe bilateral Gradually, European clinicians work- infant’s developmental prospects.
spastic CP or severe athetosis and ing in the field of developmental However, as indicated in the preced-
function at Gross Motor Function neurology realized that variation and ing paragraphs, the developmental
Classification System level V108 pre- variability may assist in the evalua- characteristics of the brain preclude
sumably lack the basic level of pos- tion of motor development. How- precise prediction. Prediction of de-
tural control.109 In infants with less- ever, before addressing the value of velopmental outcome is best when
severe forms of CP, the basic level of these parameters, some general re- multiple sources of information are

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 Variation and Variability in Human Motor Development

Figure 5.
Reduced variation in motor behavior in sitting at 10 months postterm. The figure consists of frames selected from a videorecording
of about 3 minutes. Figure produced with permission of the parents.

used, such as the infant’s history, The various instruments available to ples are the Bayley Scales of Infant
the results of neuroimaging, and evaluate the infant’s neuromotor and Development112 and the Albert In-
neurophysiological assessments in developmental status have specific fant Motor Scales.113 Neurological as-
combination with a neurological, de- aims, advantages, and disadvantages. sessments pair information on motor
velopmental, and neuromotor assess- Most instruments provide informa- performance with specific details on
ment.110 Prediction also is largely fa- tion on the child’s function in terms sensorimotor function in terms of
cilitated when longitudinal series of of age-adequate performance versus muscle tone and reflexes.110 The
assessments are used.104,111 underachievement or delay. Exam- growing awareness that the quality

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Variation and Variability in Human Motor Development

of motor behavior may assist in the The predictive value of single assess- Indeed, typical human motor devel-
evaluation of the child’s neuromotor ments increases with age. Best pre- opment is characterized by variation
condition inspired the development diction is achieved with an assess- and the development of adaptive
of 3 new assessment methods; the ment in the final phase of GMs (ie, in variability, and atypical motor devel-
Test of Infant Motor Performance the phase of “fidgety” GMs at around opment is characterized by limita-
(TIMP),114 the GM method,58,115 and 3 months postterm). In populations tions in variation and variability. Lim-
the Infant Motor Profile (IMP).116 of infants who are at risk for CP, itations in variation are based on
The TIMP and the GM method are definitely abnormal GMs at 3 months structural anomalies, in which distur-
applicable till the age of 4 months are associated with a risk of CP bances of cortical connectivity may
postterm, whereas the IMP is de- that varies between 25% and play a prominent role, whereas limi-
signed for infants aged 3 to 18 80%,79,115,117 whereas mildly abnor- tations in variability are present in
months postterm. In contrast to the mal GMs are associated with an in- virtually all children with atypical
other 2 instruments, the TIMP does creased risk of minor neurological motor development. In infants with
not use variation or variability as ex- dysfunction and psychiatric morbid- reduced variation, early intervention
plicit parameters of movement qual- ity at school age.118,119 It should be may aim to enlarge the limited move-
ity. The TIMP has good reliability, noted, however, that the predictive ment repertoire, but animal data in-
and the limited data available suggest power of mildly abnormal GMs at 3 dicate that this aim is difficult to
that it is a valuable instrument in the months is so low that mildly abnor- achieve.52 This situation implies
prediction of CP.110 The 2 methods mal GMs as a single sign have no that— despite intervention—reper-
using the concepts of variation and clinical relevance. The recent finding toire reduction most likely will re-
variability are discussed below. Vari- that the predictive value of GM qual- main a feature of the motor behavior
ation (ie, the evaluation of the size of ity is substantially higher in popula- of the child with an early lesion of
the repertoire) is a parameter that tions of infants who are at risk for CP the brain. In such a situation, equip-
may be applied in the phase of pri- than in the general population120 ment may offer a proper means to
mary and secondary variability. Vari- supports the idea that the quality of facilitate functional activity and
ability (ie, the ability to make an GMs reflects the integrity of cortical participation.
adaptive selection) is particularly rel- connectivity (ie, the integrity of the
evant from the emergence of second- brain’s white matter), as large parts The limited variability of children
ary variability onward. of the brain’s white matter are situ- with atypical motor development is
ated in the periventricular area, based on the limited ability to select
The examination of the quality of which is the site of predilection for a strategy out of the movement rep-
GMs is a reliable assessment based damage in the preterm period.121 ertoire due to deficiencies in the
on the evaluation of movement vari- processing of sensory information
ation.58,115 General movement as- The IMP is a novel instrument that brought about by self-produced ac-
sessment does not include the eval- assesses infant motor behavior in 5 tions. This fact suggests that children
uation of variability, as the non– goal- domains. Two domains are based on with limited variability may profit
directed GMs do not have a phase of the NGST: size of the repertoire from ample, variable, self-produced,
secondary variability.24 In the GM (variation) and ability to select (vari- trial-and-error activities.122,123
method, 2 aspects of variation are ability). The other 3 domains evalu-
assessed: (1) GM complexity, which ate more traditional aspects of motor Dr Hadders-Algra acknowledges the techni-
denotes the spatial aspect of move- behavior: symmetry, fluency, and cal assistance of Linze J. Dijkstra and Michiel
ment variation, and (2) GM variation, performance.76,116 The reliability and Schrier, MSc, in preparation of the figures
which represents the temporal vari- construct validity of the IMP are and Tineke Dirks, PT, for critical comments
ation of movements. Definitely ab- good, and its predictive and evalua- on a draft of the manuscript.
normal GMs are characterized by a tive power is promising.76,116 This article was submitted January 7, 2010,
severely reduced movement com- and was accepted June 24, 2010.
plexity and variation; in mildly Concluding Remarks DOI: 10.2522/ptj.20100006
abnormal GMs, complexity and vari- Accumulating evidence indicates
ation are present, but to an insuffi- that abundance in cerebral connec-
cient extent.58 The consistent pres- tivity is the neural basis of human References
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the development of CP.58,115 appropriate for a specific situation).

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