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Journal of Child Psychology and Psychiatry 50:8 (2009), pp 920–930 doi:10.1111/j.1469-7610.2009.02066.x

The quality of preterm infants’ spontaneous

movements: an early indicator of intelligence
and behaviour at school age
Phillipa R. Butcher,1 Koen van Braeckel,2 Anke Bouma,2 Christa Einspieler,3
Elisabeth F. Stremmelaar,4 and Arend F. Bos4
1
Clinical and Developmental Neuropsychology, University of Groningen, The Netherlands, and Department
of Psychology, Australian National University, ACT, Australia; 2Clinical and Developmental Neuropsychology,
University of Groningen, The Netherlands; 3Institute of Physiology, Centre for Physiological Medicine, Medical
University of Graz, Austria; 4Department of Pediatrics, University Medical Centre Groningen, The Netherlands

Background: The quality of very preterm infants’ spontaneous movements at 11 to 16 weeks post-term
age is a powerful predictor of their later neurological status. This study investigated whether early
spontaneous movements also have predictive value for the intellectual and behavioural problems that
children born very preterm often experience. Methods: Spontaneous movement quality was assessed,
using Prechtl’s method, at 11 to 16 weeks post-term in 65 infants born at £ 33 weeks of gestation in a
single centre. Intelligence and behaviour were assessed with standardised tests at 7 to 11 years of age.
Neurological status was assessed with Touwen’s test. Multiple regression was used to determine the
predictive value of movement quality for intelligence and behavioural problems. The Sobel test was used
to determine if neurological status mediated associations found between early movement quality and
outcome. Results: Spontaneous movement quality at 11 to 16 weeks post-term was significantly,
positively associated with later intelligence. The number of normal postural patterns displayed
contributed most strongly to the association, which was not mediated by neurological status. Fidgety
movements, strong predictors of later neurological dysfunction, were not associated with intelligence.
Spontaneous movement quality was not associated with internalising or externalising problems but
showed a trend to an association with attention problems. Conclusion: These findings suggest that, in
children born preterm, early spontaneous movement quality has clear prognostic value for neurological
and intellectual outcome, and to a lesser extent, for attentional outcome. However, cognitive outcome
was associated with the presence of specific, age-appropriate postural patterns, while neurological
outcome has been associated with the presence of global movement abnormalities. The presence of
specific, age-appropriate postural patterns may reflect the integrity of areas of the brain involved in
cognitive processing and the regulation of attention later in childhood. Alternately, it may facilitate
cognitive and attentional development. Keywords: General movements, intelligence, behaviour,
development, preterm. Abbreviations: GMs: general movements; FMs, fidgety movements; CP: cere-
bral palsy; ATN: asymmetric tonic neck reflex.

From several weeks after conception, the young
human nervous system is able endogenously to
generate a variety of movements (Einspieler &
Prechtl, 2005). As an expression of spontaneous
neural activity, these movements are a potential
marker of neural dysfunction following brain injury.
In the last 15 years, considerable research has been
devoted to determining which movement patterns
provide most insight into the functional integrity of
the young nervous system. General movements
(GMs), the most frequent and most complex of young
infants’ spontaneous movements, are the most
promising in this regard. Early GMs involve the en-
tire body in varying sequences of neck, trunk and
limb movements. They remain similar in appearance
from early fetal life until 6 to 9 weeks post-term,
when smaller, circular movements of moderate
speed and variable acceleration known as ‘fidgety’
movements (FMs) begin to replace the more ‘writhing’
Conflict of interest statement: No conflicts declared.
movements observed earlier. At the same time, a
variety of concurrent movement and postural pat-
terns emerge. FMs remain present until 6 months
post-term, when intentional and antigravity move-
ments predominate (Einspieler, Prechtl, Bos, Ferrari,
& Cioni, 2004). Several studies have found strong
associations between the quality of GMs during the
FM period, in particular the mid-FM period
(11–16 weeks post term), and later neurological
development. Very poor quality of the motor reper-
toire, for example, the absence of FMs, is strongly
associated with the development of serious neuro-
logical disorders such as cerebral palsy (CP) (Cioni et
al., 2000; Hadders-Algra & Groothuis, 1999). Less
serious deficits in the motor repertoire, for example,
abnormality rather than absence of FMs, a monoto-
nous repertoire of concurrent movements, and the
persistence of early postural reflexes, are associated
with less serious motor disorders such as minor
neurological dysfunction (MND) (Groen, de Blecourt,
Postema, & Hadders-Algra, 2005; Zuk, Harel,

 2009 The Authors

Journal compilation  2009 Association for Child and Adolescent Mental Health.
Published by Blackwell Publishing, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA

Leitner, & Fattal-Valevski, 2004; Bruggink et al.,
2008). As a result of their powerful prognostic value,
the quality of spontaneous movements during the
FM period is considered a sensitive measure of the
integrity of the areas of the central nervous system
involved in motor control.
The quality of spontaneous movements is partic-
ularly helpful in identifying which children with a
history of pre- and perinatal medical complications
will go on to develop neurological disorders. Neuro-
logical disorders that follow pre- and perinatal
medical complications are frequently accompanied
by cognitive and behavioural problems. Children
with CP, for example, perform more poorly, as a
group, than age-mates on measures of intelligence
(Fennell & Dikel, 2001) and behaviour (Goodman &
Neville, 2001). Children born preterm perform more
poorly on measures of motor skill, intelligence and
behaviour (for reviews see Bhutta, Cleves, Casey,
Cradock, & Anand, 2002; Foulder-Hughes & Cooke,
2003). Importantly, neurological, behavioural and/
or intellectual deficits often coexist in the same child
(Volpe, 2000). This raises the question of whether
GMs also have prognostic value for intellectual and
behavioural development.
An association between early movement quality
and later behaviour and intelligence may seem less
plausible than an association between early move-
ment quality and later motor disorders. Movement
quality at all ages is strongly associated with the
nature and severity of pre- and perinatal brain
injury. Behaviour and intelligence are more closely
associated with environmental factors such as the
quality of the home environment, and the mother’s
sensitivity and perception of social support (Bend-
ersky & Lewis, 1994; Laucht, Esser, & Schmidt,
1994). Recently, however, Denckla (2005) has sug-
gested that early motor status may serve as a marker
for the integrity not only of the areas of the brain
involved in motor control, but also of neighbouring
areas involved in emotional and cognitive control.
A possible anatomical basis for an association be-
tween the quality of the early motor repertoire and
later cognition in preterm infants was suggested by
Inder and colleagues (1999), who showed that seri-
ous white matter injury, the dominant form of brain
injury in infants born preterm (Volpe, 2000), and a
primary correlate of the quality of the motor reper-
toire, is followed by impaired cortical development.
Reduced cortical volumes have been found in school-
age children born preterm, and abnormalities in
specific regions have, in turn, been found to be
associated with intelligence scores (Peterson et al.,
2000). Empirical support for an association between
the quality of the early motor repertoire and later
behaviour problems is provided by the recent finding
that mildly abnormal GMs at 10–16 weeks of age
predicted attention problems and aggression 4 to
9 years later (Hadders-Algra & Groothuis, 1999).
Spontaneous movements may therefore have prog-
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Infants’ spontaneous movements 921
nostic value not only for motor development, but also
for intelligence and behaviour problems.
Existing indices of the integrity of the central
nervous system in young infants have limited prog-
nostic value for intellectual and behavioural devel-
opment. In children born preterm, for example, early
indices of brain injury, such as ultrasound scans,
and early neurological assessments generally show
only modest associations with cognitive and
behavioural development (Vollmer et al., 2003;
Pinto-Martin, Whitaker, Feldman, van Rossem, &
Paneth, 1999). The small size of the associations
undoubtedly reflects the importance of environ-
mental factors in shaping behavioural and intellec-
tual development. However, it also reflects the
limitations of existing indices of early brain injury for
predicting intelligence and behaviour problems,
which are generally accepted to be mediated by
many subtle neural mechanisms in networks dis-
tributed widely across the brain. If the quality of the
spontaneous motor repertoire during the FM period
is associated with intelligence and behaviour prob-
lems in later childhood, then assessments of the
motor repertoire will form a valuable addition to
existing early indices, improving our ability to pre-
dict in which children with a history of pre- and
perinatal medical complications intelligence and/or
behaviour are likely to be impaired.
Our first goal was to investigate associations
between the quality of spontaneous movements
between 11 and 16 weeks post-term and intelligence
and behaviour problems in childhood. Participants
were school-age children who had been born pre-
term. Children born preterm show considerable
variability both in the quality of spontaneous move-
ments in early infancy and in intelligence and
behaviour problems in later childhood. The quality of
their spontaneous movements in infancy has con-
sistently been found to be associated with later
neurological development. They therefore constitute
an appropriate group in which to explore these
associations. If spontaneous movement quality has
broader prognostic significance, then less optimal
movement quality in infancy will be associated with
lower intelligence and more behaviour problems in
childhood.
Since less optimal movement quality in infancy is
associated with neurological disorder in childhood,
our second goal was to determine whether any
associations between movement quality and intelli-
gence and behaviour problems were mediated by
neurological status rather than directly associated
with movement quality.
Method
Participants
Sixty-five children, between 7 and 11 years of age
(M = 8.8, SD = 1.2), and their parent(s) participated
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922 Phillipa R. Butcher et al.

in the study. The children had been born in, or Table 1 Characteristics of the participants (a) Medical risk
admitted shortly after birth to, the neonatal intensive factors (b) Age and outcome at follow-up
care unit of the University Medical Centre (UMC) (a)
between 1993 and 1998. All were born pre-
term (gestational age: M = 29.9w, SD = 1.8w, Gestational age (w),
M (SD; Range; N ) 29.9 (1.83; 25.7–33.7; 65)
Range = 27.7–33.7w) and belonged to a group of 89
Birthweight (gm),
children who had participated in earlier investiga- M (SD; Range; N ) 1196 (289; 595–1800; 65)
tions of associations between spontaneous move- Small for date (yes: no) 38:27
ment quality and development (Bos, Martijn, Okken, Ultrasound status
& Prechtl, 1998; Bos et al., 1997, 1998; Hadders- Severity of intraventricular
hemorrhage1
Algra et al., 2004). Five families could not be located
(grade 0:I:II:III:IV) 46:16:0:1:2
at follow-up. Two refused participation. Fifteen Severity of periventricular
children developed CP. In 10 children, the severity of echogenicity/leukomalacia2
the CP precluded valid measurements of intelligence. (grade 0:I:II:III:IV) 32:32:1:0:0
Five children with mild CP, all attending regular Mechanical ventilation
(yes: no) 31:34
schools, were included in the analysis to increase its
(days) M (SD; Range; N ) 7.2 (6.8;1–25; 65)
power to determine the impact of neurological status Chronic lung disease (yes: no) 17:48
on associations between early motor quality and
developmental outcome. The remaining 60 children (b)
can be considered typical of preterm infants admit- Age at follow-up: 7y:8y:9y:10y:1y 15: 21:15:13:1
ted in the mid-1990s to the neonatal intensive care Touwen’s test score, M 3.23 (3.11; 0–12; 61)
unit of the UMC who did not develop severe neuro- (SD; Range; N )
logical disorders. The children’s medical character- Intelligence
TIQ, M (SD; Range; N ) 94 (11; 67–118; 65)
istics are presented in Table 1a. Educational level VIQ, M (SD; Range; N ) 93 (12; 68–125; 65)
of the mothers and fathers ranged from elementary PIQ, M (SD; Range; N ) 94 (13; 65–119; 65)
to tertiary (mothers: M = 11.5y, SD = 3.5y, Range = CBCL
0–17y, fathers M = 12.1y, SD = 2.5y, Range 0–17y). Internalising,
Measurements of motor quality were unavailable M (SD; Range; N ) 54 (11; 32–73; 65)
Externalising,
for seven children because of prolonged crying and M (SD; Range; N ) 52 (11; 32–86; 65)
fussing during the video-recording. These children Attention Problems subscale,
did not differ significantly on measures of intelli- M (SD; Range; N ) 59 (9;50–83; 65)
gence or behaviour problems from those for whom Attention Problems subscale:
data were available. Four children without CP were normal:borderline/clinical 51:14
excluded from the mediation analysis. These 1
Intraventricular hemorrhage (IVH) refers to bleeding in the
children had completed medical and neurological ventricles, where the cerebrospinal fluid is produced. When
examinations within the previous year as part of the IVH was present, four levels of severity were distinguished.
routine follow-up, and chose not to repeat these Levels III and IV are systematically associated with poorer
developmental outcome. Levels II and I are less systematically
examinations. They did not differ significantly on
associated with poorer developmental outcome.
measures of intelligence or behaviour problems from 2
Periventricular echogenicity/leukomalacia (PVE/L) refers to
the children for whom data were available. damage to the white matter tissue surrounding the ventricles.
All parents gave written consent to participate in When PVE/L was present, four levels of severity were distin-
the study, which was approved by the UMC Ethics guished. Levels III and IV are systematically associated with
poorer developmental outcome. Levels II and I are less
Committee.
systematically associated with poorer developmental outcome.

The children’s intelligence, motor skill, neurological

Procedure
Video-recordings of spontaneous movements were
made at 4 to 6 week intervals between birth and
6 months post-term. The recordings, lasting 5 to
10 minutes, were made during a period of active
wakefulness, with the infants lying supine and
naked or wearing a romper suit. Recordings of 59
infants were made at home. Recordings of the
remaining six infants were made during visits to the
Department of Developmental Psychology at
the University.
Seven to ten years later, the children participated
in a follow-up study on visuo-motor, cognitive and
behavioural development. As part of the study, par-
ent(s) and child attended a test session at the UMC.
Journal compilation  2009 Association for Child and Adolescent Mental Health.
and medical status were assessed. Parent(s) com-
pleted a questionnaire on their child’s behaviour.
The findings regarding associations between move-
ment quality and neurological development have
been reported elsewhere (Bruggink et al., 2008).
Measures
Quality of spontaneous movements. The motor
repertoire was evaluated using the video-recording
made between 11 to 16 weeks post-term, following
Prechtl’s method for the assessment of the motor
repertoire between 3 and 5 months (Einspieler et
al., 2004). Age at assessment ranged from 11w to
15w (M = 13.3, SD = 1.1). At this age, the motor
 2009 The Authors

repertoire includes FMs and a variety of concurrent
movement and postural patterns. Scores were
assigned to the following five aspects:
1. Quality of FMs
2. Age-adequacy of concurrent movements
3. Presence and normality of concurrent movements
4. Presence and normality of postural patterns
5. Quality of concurrent movements
Scores for each aspect can range from 1 to 4. The
first and last aspects are scored qualitatively on the
basis of gestalt perception of the smoothness,
amplitude and speed of movement patterns
(Einspieler & Prechtl, 2005). The remaining scores
are semi-quantitative. Movement and postural pat-
terns expected to be present between 3 and
5 months are scored as present or absent and, when
present, as normal or abnormal. Normal concurrent
movements include kicking, manipulating clothing
and playing with the fingers. Abnormal concurrent
movements include circular arm movements, arch-
ing of the trunk, and sudden bursts of activity.
Normal postural patterns include ability to overcome
the asymmetric tonic neck reflex (ATN; one arm
extended, the other flexed, with head turned to the
extended arm), head held in the midline and varied
finger patterns, where fingers move independently of
each other. Abnormal postural patterns include
persistent ATN and invariant finger patterns (fingers
curled inwards to form a fist, or extended and
spread). Age-adequacy of concurrent movements is
scored on the basis of the number of movement and
postural patterns observed and the presence of
specific types of movement, in particular anti-gravity
movements, movements towards the midline and
fiddling. Presence and normality of concurrent
movements and postural patterns are scored on the
basis of the relative frequency of normal and
abnormal characteristics: 1 (abnormal > normal), 2
(abnormal = normal) and 4 (normal > abnormal).
Note that a predominance of normal characteristics
receives a heavier weighting. The scores for the five
aspects of the motor repertoire are summed to pro-
vide a Motor Optimality Score, range 5 to 20. Higher
scores indicate higher movement quality. The semi-
quantitative scores can be broken down into the
Table 2 Quality of spontaneous movements at 11 to 16 weeks post-term: scores for motor optimality and its components, and the
correlations between the components of motor optimality
M (SD; Range; N)
1. Motor Optimality Score 15.7
2. Quality of FMs 3.4
3. Age adequacy of concurrent movements 3.0
4. Presence, normality of postural patterns 2.6
5. Presence, normality of concurrent movements1 4.0
6. Quality of concurrent movements 2.6
1
Presence, normality of concurrent movements showed no variance at the 11–16 w measurement.
All correlations significant at **p = <.01.
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Infants’ spontaneous movements 923
specific movement patterns or characteristics they
reflect, allowing the analysis of associations with
both overall score and movement details on which it
is based. The scores for the different aspects of early
spontaneous movements and their inter-correlations
are presented in Table 2. The correlations ranged
from .38 to .63, showing that, although associated,
the scores provided unique information.
Two-thirds of the videos were scored by 2 or 3
observers. Cohen’s kappa for Quality of FMs, Quality
of Concurrent Movements and Age-adequacy of
Concurrent Movements was .91, .87 and .89
respectively. Agreement for Presence and Normality
of Concurrent Movement Patterns and Presence and
Normality of Postural Patterns was 89% and 90%
respectively.
Neurological status. Current neurological status
was assessed by an experienced paediatrician using
Touwen’s test (1979). Children without a neurological
handicap such as CP may have less serious neuro-
logical dysfunctions. The total score on Touwen’s test
indicates the degree of such minor neurological
dysfunction on the basis of assessment of posture and
muscle tone, reflexes, coordination and balance,
choreiform activity and fine manipulative ability
(Hadders-Algra, 2002). Recent investigations of the
psychometric quality of Touwen’s test have shown
moderate to good test–retest reliability, inter-observer
reliability and validity (Peters, Maathuis, Kouw,
Hamming, & Hadders-Algra, 2007; Heineman, Bos, &
Hadders-Algra, 2008).
Cognitive outcome. Intelligence was assessed using
four Verbal subscales (Similarities, Vocabulary,
Information, Arithmetic) and three Performance
subscales (Picture Arrangement, Block Design,
Object Assembly) from the WISC IIINL (Kort et al.,
2002). Verbal (VIQ), Performance (PIQ) and Total
(TIQ) IQ scores were calculated using Sattler’s (1992)
formula.
Behaviour problems outcome. Behaviour problems
were assessed using the Dutch version of the
Child Behaviour Checklist (CBCL) (Verhulst, van der
Ende, & Koot, 1996), a screening instrument with
Correlations
2 3 4 5 6
(3.6; 9–20; 65) 74** .83** .81** .79**
(1.0; 1–4; 65) – .63** .38** .42**
(1.1; 1–4; 65) – .50** .55**
(1.4; 1–4; 65) – .58**
(0; 4; 65) –
(1.0; 1–4; 65)

924 Phillipa R. Butcher et al.
well-established validity in distinguishing between
children with and without behaviour problems,
according to parental report. It yields scores on two
broadband scales, internalising and externalising,
with a separate subscale for attention problems. Raw
scores can be converted into T-scores (M = 50,
SD = 10) to provide continuous measures or classi-
fied according to cut-off scores as normal, borderline
and clinical.
Data analysis
Intelligence and internalising and externalising
scores were normally distributed. Since intelligence
and behaviour are multiply determined, hierarchical
multiple regression analysis was used to estimate
their associations with early movement quality. The
attention problems subscale scores were not nor-
mally distributed. They were therefore dichotomised
following the manual into normal (£ 92 percentile), or
borderline/clinical (>92 percentile). Logistic regres-
sion was used to estimate their association with
early movement quality. The educational level of
both parents, an established associate of intelligence
and behaviour, and the age of the child were entered
as first-level explanatory variables in all analyses.
Since attention problems may mediate associations
between motor skill and cognitive performance
(Wassenberg et al., 2005), the attention problems
subscale score was included as a first-level explan-
atory variable in the analysis of intelligence.
The Motor Optimality Score was entered as a sec-
ond level explanatory variable. Significant associa-
tions with intelligence and/or behaviour problems
were explored, with the components of the Motor
Optimality Score as second-level explanatory vari-
ables, entered using the stepwise entry procedure.
Significant associations with semi-quantitative
components were explored by repeating the analysis
with the relevant movement and postural patterns as
second-level variables.
Following Baron and Kenny (1986), multiple
regression was used to determine whether neuro-
logical status mediated any associations between
movement quality and intelligence. First, the asso-
ciation between neurological status and movement
characteristics associated with intelligence was
examined. Next, neurological status was included in
the analysis of the association between movement
characteristics and intelligence. Finally, the Sobel
test (Sobel, 1988) was carried out to determine if
including neurological status in the analysis reduced
the association between movement characteristics
and intelligence.
Results
Means and standard deviations of IQ, behaviour
problems and Touwen’s test scores are presented in
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Table 1b. Mean TIQ, VIQ and PIQ scores were sig-
nificantly lower than in the normative sample (94, 93
and 94), t(64) = –4.63, p = .000; t(64) = –4.54,
p = .000; t(64) = –3.62, p = .001 respectively. Mean
internalising and externalising scores were (nearly)
significantly higher than in the normative sample,
t(64) = 3.02, p = .004; t(64) = 1.70, p = .093 respec-
tively. Frequency of attention problems in the bor-
derline/clinical range was significantly higher,
v2 (1) = 16.187, p < .001.
Movement quality and intelligence
After controlling for the parents’ education and the
child’s age and attention problems, the Motor
Optimality Score contributed significantly to TIQ
(b = .27, p = .014), VIQ (b = .24, p = .035), and PIQ
(b = .23, p = .043). To determine whether the
associations were caused primarily by the five
children with mild CP, the analysis was repeated
without these children. Motor Optimality remained
significantly associated with both TIQ (b = .27,
p = .018) and VIQ (b = .28, p = .016). The associa-
tion with PIQ dropped below significance (b = .19,
p = .104).
To explore the basis for the association between
Motor Optimality and IQ, the analysis was repeated
with the components of Motor Optimality as second-
level explanatory variables, entered using the
stepwise entry procedure. After controlling for the
parents’ education and the child’s age and attention
problems, the relative frequency of normal versus
abnormal postural patterns contributed significantly
to TIQ (b = .31, p = .004), VIQ (b = .27, p = .016), PIQ
(b = .27, p = .018). No other components contributed
significantly to IQ (p’s ranged from .52 to .99). The
components of Motor Optimality were moderately
inter-correlated, raising the possibility of their being
dropped from the model on the basis of only small
differences in their unique contributions to TIQ. The
low semi-partial correlations between the excluded
variables and TIQ, range .039 to .044, showed that
this was not the case here. The associations between
postural patterns and TIQ, VIQ and PIQ decreased
slightly in significance (b = .29, p = .009; b = .28,
p = .016; b = .24, p = .045) when the analysis was
repeated without the children with CP.
To explore the association between postural pat-
terns and IQ, the analysis was repeated with the
number of normal postural patterns and the number
of abnormal postural patterns as second-level
explanatory variables, again entered using the
stepwise entry procedure. The number of normal
postural patterns contributed significantly to TIQ
(b = .35, p = .011), VIQ (b = .34, p = .015) and
almost significantly to PIQ (b = .27, p =.065). The
number of abnormal patterns was not associated
with IQ (TIQ p = .7; VIQ p = .691; PIQ p =.801). The
results of the regression analysis are presented in
Table 3a. The number of normal patterns remained
 2009 The Authors
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Infants’ spontaneous movements 925

Table 3 Summary of hierarchical multiple regression analyses (a)Associations between early movement quality and intelligence
scores (b) Associations between early movement quality and neurological status (c) Associations between early movement quality
and intelligence scores with neurological status as mediator

TIQ VIQ PIQ

Dependent variable B SE B b B SE B b B SE B b

(a)
Independent variable
Step 1
Parents’ education 2.56** .96 .29 3.27 1.08 .34 1.85 1.19 .18
Attention problems score –.52** .13 –.44 –.533** .15 –.40 –.52** .16 –.37
Age –3.03** 1.04 –.32 –2.03t 1.17 –.19 –4.03** 1.29 –.36
Step 2
Parents’ education 2.31* .92 .26 3.01** 1.10 .31 1.61 1.18 .15
Attention problems score –.44** .13 –.37 –.44** .14 –.34 –.44** .16 –.31
Age –2.24* 1.03 –.23 –1.07 1.12 –.10 –3.20* 1.32 –.28
Normal postural patterns 4.32* 1.65 .35 4.66* 1.89 .34 3.98t 2.12 .27
Abnormal postural patterns .38 .98 .05 .44 1.10 .05 .32 1.25 .04
Note. R2 = .29 for Step 1. Note. R2 = .25 for Step 1. Note. R2 = .23 for Step 1.
D R2 = .098 for Step 2 D R2 = .037 for Step 2 (p < .05) D R2 = .056 for
(p’s < .05) (N = 65) (p’s < .05) (N = 65) Step 2 (p < .1) (N = 65)

Touwen’s test score

Dependent variable B SE B b

(b)
Independent variable
Parents’ education .33 .32 .13
Attention problems score .10* .04 .29
Age .31 .35 .11
Normal postural patterns –.1.29** .48 –.34
Note. R2 = .35 (p < .05) (N = 61)

TIQ VIQ PIQ

Dependent variable B SE B b B SE B b B SE B b

(c)
Independent variable
Step 1
Parents’ education 2.17* 1.00 .24 3.25** 1.13 .32 1.58 1.17 .15
Attention problems score –.44*** .14 –.35 –.49** .16 –.36 –.44** .16 –.31
Age –2.16t 1.10 –.22 –.88 1.22 –.08 –3.23* 1.31 –.29
Normal postural patterns 4.40** 1.50 .33 4.57* 1.58 .33 3.67* 1.71 .25
Step 2
Parents’ education 2.33* .92 2.55 3.41** 1.13 .34 1.24 1.28 .11
Attention problems score –.39* .14 –.31 –.45** .16 –.33 –.32t .18 –.22
Age –2.01t 1.1 –.20 –.74 1.23 –.07 –3.27* 1.40 –.28
Normal postural patterns 3.76** 1.59 .28 3.94* 1.77 .27 3.58t 2.01 .22
Touwen’s test score –.49 .42 –.14 –.09 .47 –.02 –.90 .54 –.22
Note. R2 = .38 for Step 1. Note. R2 = .35 for Step 1. Note. R2 = .27 for Step 1.
(p < .05) D R2 = .016 for Step (p < .05) D R2 = .0 for Step 2 (p < .05) D R2 = .036 for Step
2 (p > .05) (N = 61) (p > .05) (N = 61) 2 (p > .05) (N = 61)

t = p < = .10, p = < .05; **p = < .01.

significantly associated with TIQ and VIQ when the
analysis was repeated without the children with CP
(b = .32, p = .027, b = .35, p = .017 respectively).
The association with PIQ fell below significance
(p = .167). The effect sizes, ranging from 3.0 to 4.9 IQ
points, can be considered large given a standard
deviation of 15 IQ points in the normative sample
and a range of 1 to 4 for number of normal postural
patterns.
To determine how well these results would gener-
alise to the broader population of preterm born
 2009 The Authors
Journal compilation  2009 Association for Child and Adolescent Mental Health.
children, we cross-validated the model for the total
group following Cohen, Cohen, West, and Aitken
(2003). The adjusted R2’s for TIQ, VIQ and PIQ were
.296, .247 and .183 respectively.
To determine if the associations between normal
postural patterns and IQ scores were mediated
by neurological status, a mediation analysis was
carried out. Number of normal patterns was signifi-
cantly associated with neurological status both with
(b = –.34, p = .009) and without (b = –.28, p = .05)
children with CP in the analysis. When normal
 14697610, 2009, 8, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2009.02066.x by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [24/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
926 Phillipa R. Butcher et al.

postural patterns and neurological status were Discussion

included in a single model, the contribution of
neurological status did not reach significance for any
Intelligence
measure of IQ (TIQ p = .249; VIQ p = .849; PIQ The present study found clear associations between
p = .101). The regression coefficients decreased in the quality of spontaneous movements in early
size with the inclusion of neurological status. Sobel infancy and intelligence 7 to 11 years later in a group
tests showed that the decrease was not significant of children born preterm. After controlling for the
(p = .285, p = .849 and p = .101 for TIQ, VIQ and parents’ education and the child’s age and attention
PIQ respectively). The results of the mediation problems, the number of normal postural patterns
analysis are presented in Table 3b and 3c. displayed between 11 and 16 weeks post-term con-
To illustrate the association between postural tributed significantly to Total and Verbal Intelligence
patterns and TIQ, three postural quality groups were scores, and almost significantly to Performance
formed on the basis of number of normal postural Intelligence scores. The adjusted R2, obtained by
patterns. TIQ scores were grouped into four 15-point cross-validation, then leads to the estimate that the
categories. The percentage of children from each combination parental education, age of the child,
postural quality group in each TIQ score category is CBCL attention problems score and number of nor-
shown in Figure 1. None of the infants displaying mal postural patterns explains 29.6% of the variance
fewer than two normal patterns at 11 to 16 weeks in TIQ in children born preterm.
post-term had TIQ scores above 100, while 62% of Importantly, although a minority of the children
the infants displaying more than two normal had neurological dysfunctions ranging in severity
patterns had IQ scores above 100. from minor neurological dysfunction to mild CP, a
mediation analysis showed that neurological status
did not mediate the association between early
Movement quality and behaviour problems
movement quality and intelligence. Consistent with
No significant associations were found between this, excluding the children with CP from the
Motor Optimality and CBCL externalising or inter- analysis did not affect the significance of the
nalising scores. Logistic regression showed that, associations, and the quality of FMs, a powerful
after controlling for the parents’ education and the predictor of neurological dysfunction, was not
child’s age, Motor Optimality made a near signifi- associated with intelligence. These findings then
cant, negative contribution to the classification suggest that associations between early movement
normal versus borderline/clinical on the attention quality on the one hand, and later intelligence and
problems subscale (B = –1.64, p = .071). The pre- neurological dysfunction on the other, emerge along
dictive value of the model did not reach significance different developmental pathways, which are
(p = .29). However, a Mann–Whitney U-test con- associated with different aspects of early movement
firmed the trend towards lower Motor Optimality quality.
scores in children classified borderline/clinical than
in children classified normal, U = 266.5, p = .07.
Behaviour problems
The association between Motor Optimality and
attention problems dropped below significance The quality of spontaneous movements between 11
(p = .32) when the analysis was repeated without and 16 weeks post-term was not associated with
the children with CP. internalising or externalising problems later in

TIQ < 85 (N = 14) TIQ 85 - 99 (N = 29) TIQ 100 - 114 (N = 21) TIQ ?
115 (N = 1)

100
Percent in IQ Category

75

50

25

0
< 2 normal postural 2 normal postural > 2 normal postural
patterns (N = 16) patterns (N = 23) patterns (N = 26)

Figure 1 Distribution of TIQ categories across the three postural quality groups
 2009 The Authors
Journal compilation  2009 Association for Child and Adolescent Mental Health.

childhood. However, poorer quality tended to be
followed more frequently by attention problems. In
a study of 4- to 9-year-old children, Hadders-Algra
and Groothuis (1999) found that poorer quality of
GMs in infancy, while not associated with CBCL
attention problems subscale score, was associated
with attention problems assessed by a questionnaire
derived from DSM IV diagnostic criteria. The asso-
ciations were stronger in the 4- to 5-year-olds, whose
medical histories placed them at higher risk than the
7- to 9-year-olds for developmental problems.
Together, the two studies suggest that an association
exists between movement quality at 2 to 3 months
post-term and behaviour problems in high risk
children. However, the association is weak and
seems to vary in strength with the age and medical
history of the child, and the instruments used to
assess GMs and behaviour problems.
Together with the results of previous research
(Bruggink et al., 2008; Cioni et al., 2000; Hadders-
Algra & Groothuis, 1999), the present results show
three important things. First, the quality of the
spontaneous movement repertoire at 11 to 16 weeks
post-term has prognostic value not only for motor
development but also for cognitive development, and
to a lesser extent, the development of behaviour
problems. Second, different aspects of the movement
repertoire are associated with outcome in the differ-
ent domains. FM quality – a global assessment – is
most strongly associated with later neurological
dysfunction, while specific postural patterns were
associated with intelligence and overall motor opti-
mality showed a trend to an association with atten-
tion problems. Third, the prognostic value is not
limited to children with extremely poor early motor
repertoires who go on to develop serious neurological
disabilities.
There are at least two interpretations of these
results. The first is that the quality of posture pro-
vides a broad measure of the quality of early central
nervous system (CNS) development. Cortical areas
increase their level of activity markedly during the
second and third months post-term, as do the
cerebellar cortex and the basal ganglia, areas which
are involved in networks with important motor,
cognitive and behavioural functions (Chugani,
Phelps, & Mazziotti, 1987). The different postural
patterns which emerge at this age may provide an
index of the quality of early CNS development in
different areas of the brain. One ‘normal’ posture,
ability to overcome the ATN posture, reflects the
suppression of an early reflex, suggesting normal
development of the cortical processes which allow its
inhibition. Another ‘normal’ posture, varied finger
movements, is likely associated with the ability to
move the fingers independently, which, unlike arm,
leg and whole body movements, requires cortico-
spinal input (Nolte, 1999). Its presence may there-
fore reflect the quality of cortical processing in
regions providing such cortico-spinal input. Murray
 2009 The Authors
Journal compilation  2009 Association for Child and Adolescent Mental Health.
14697610, 2009, 8, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2009.02066.x by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [24/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Infants’ spontaneous movements 927
et al. (2006) recently found an association between
age of standing without support in infancy and score
on a measure of categorisation in adulthood. They
similarly proposed that age of standing without
support may be an early measure of quality of pro-
cessing in the areas of the prefrontal cortex later
called on by the categorisation task.
A second interpretation is that the quality of
posture reflects the crucial role of motor activity in
the early development of perception and cognition.
Rapid brain development in the second and third
months post-term is accompanied by equally rapid
psychological development. Infants’ exploration of
their environment with eyes and hands becomes
more active and better coordinated. Independent
finger movements will facilitate exploration, sup-
plementing visual input with more precise tactile
and proprioceptive input. Their delayed emergence
may inhibit exploration in a period when develop-
ment is particularly sensitive to the input explora-
tion provides. Inability to overcome extreme
postures, such as the ATN, or to hold the head in
the midline, is also likely to interfere with explor-
atory activity. The extent to which expected postural
patterns are present between 11 and 16 weeks post-
term may provide a measure of the extent to which
spontaneous movements facilitate or inhibit infants’
interactions with the world around them during a
phase in which sensorimotor activity drives
perceptual and cognitive development (Wassenberg
et al., 2005).
The association between the quality of early pos-
ture and later intelligence is particularly interesting
against the background of current attempts to
understand the association between measures of
visual attention in infancy, for example habituation
and novelty recognition, and intelligence in later
childhood. This has been assumed to be some
shared underlying process, which is tapped by both
infant attention and childhood intelligence measures
(Sigman, Cohen, & Beckwith, 2000). Our findings
suggest that the predictive value of early measures
which are associated with later intelligence may be
based on what they reveal about the integrity of the
developing CNS, or in the quality of the foundation
they lay for future development, and not primarily on
shared underlying processes.
Limitations of the study
The results are based on data from a small group of
children from a single medical centre. This raises
the question as to how far they can be generalised to
the broader population of children born preterm. The
below average mean IQ scores and above average
frequencies of behaviour problems in the partici-
pants were highly similar to those found in other
follow-up studies of children born preterm (Bhutta et
al., 2002; Foulder-Hughes & Cooke, 2003). While
this increases our confidence that these results can
 14697610, 2009, 8, Downloaded from https://acamh.onlinelibrary.wiley.com/doi/10.1111/j.1469-7610.2009.02066.x by Universidad Nacional Autonoma De Mexico, Wiley Online Library on [24/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
928 Phillipa R. Butcher et al.

be generalised to the broader population of children
born preterm, further investigations are required to
determine their generalisability Further, in the
absence of a theoretical basis for determining the
order in which the components of the Motor Opti-
mality Score should be entered into the regression
equation, we used stepwise regression to explore
their individual contributions to the intelligence
score. This carries the risk of capitalising on chance
associations in this particular sample (Tabachnick &
Fidell, 2007), and highlights the need to replicate our
results in a new investigation.
Conclusions
This is the first study to our knowledge to investi-
gate the association between the quality of the
spontaneous motor repertoire in early infancy and
intelligence in later childhood, and the second to
investigate its association with behaviour problems.
The results suggest that the assessment of the
spontaneous motor repertoire can improve our
ability to predict in which high-risk infants cogni-
tion and/or behaviour are likely to be impaired.
However, further investigations of the associations
between early spontaneous movements and later
intelligence and behaviour problems in other
groups of high risk children are needed to test this
suggestion. Investigations should focus both on
children known to be at higher risk because of
pre- and perinatal medical complications, and on
children at risk for developmental disorders such
as dyslexia, autism and ADHD, which are fre-
quently accompanied by motor disorders. Finally,
these findings raise the important question of
whether the quality of the early spontaneous motor
repertoire also has prognostic value for children at
no increased medical risk. The most powerful
predictors of intelligence were postural patterns
which typically emerge between 11 and 16 weeks.
Neurological status did not mediate between early
postural quality and intelligence. This raises the
possibility that an association between the quality
of the early motor repertoire and intelligence in
later childhood may also be found in typically
developing children.
Correspondence to
Phillipa R. Butcher, Department of Psychology,
Australian National University, Canberra, ACT 0200,
Australia; Email: phillipa.butcher@anu.edu.au

Key points

• As a group, children born very preterm have lower intelligence scores, more behaviour problems, and
poorer neurological development than typically developing children.
• The quality of very preterms’ early spontaneous movements (11-16 weeks post-term) has well-established
predictive value for their later neurological development.
• We found that early movement quality also has predictive value for cognitive development, and to a lesser
extent, the development of attentional problems.
• The predictive value of early movement quality was not limited to children with extremely poor movement
repertoires who later develop serious neurological disabilities.
• Early assessment of spontaneous movements may improve our ability to identify very preterm infants
whose intellectual and attentional development is likely to be impaired.

Bos, A.F., Martijn, A., van Asperen, R.M., Hadders-

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Manuscript accepted 30 October 2008
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