DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY

ORIGINAL ARTICLE

Minor neurological dysfunction in children with autism spectrum

disorder
MARIANNE DE JONG 1 | MARJA PUNT 1 | ERIK DE GROOT 2 | RUUD B MINDERAA 3 | MIJNA HADDERS-ALGRA 4
1 Symfora Group, Department of Child and Adolescent Psychiatry Fornhese, Amersfoort. 2 Dimence, Centre for Mental Health Care, Deventer. 3 Department of Child and
Adolescent Psychiatry, University Medical Centre Groningen, Groningen. 4 Department of Paediatrics, Developmental Neurology, University Medical Centre Groningen, Groningen,
the Netherlands.
Correspondence to Dr Marianne de Jong at Regentesselaan 10, 3762 DS Soest E-mail: marjapunt@planet.nl

PUBLICATION DATA

AIM The aim of this study was to improve the understanding of brain function in children with

Accepted for publication 24th February 2011.

Published online 13th May 2011.

METHOD We studied MNDs in 122 children (93 males, 29 females; mean age 8y 1mo, SD 2y 6mo)

ABBREVIATIONS

ASD Autism spectrum disorder

MAC-ICD-9
Multi-Axial Classification Scheme for
Psychiatric Disorders in Childhood and
Adolescence, version 9
MND Minor neurological dysfunction

autism spectrum disorder (ASD) in relation to minor neurological dysfunctions (MNDs).

who, among a total cohort of 705 children (513 males, 192 females; mean age 9y, SD 2y 0.5mo)
referred to a regional outpatient non-academic psychiatric centre in the Netherlands, were
diagnosed with ASD after an extensive multidisciplinary psychiatric assessment. Children with
clear neurological abnormalities (e.g. cerebral palsy or spina bifida) were excluded from the study.
MNDs were assessed in all 705 children using the Touwen examination method. Special attention
was paid to the severity and type of MND. Data of the children with ASD were compared with
neurological morbidity data of children with other psychiatric disorders and with children in the
general population, who were born at Groningen University Hospital between 1975 and 1978.
RESULTS Seventy-four percent of the children with ASD showed complex MNDs compared with
52% of the children with other psychiatric disorders and 6% of the reference group (v2=18.0,
p<0.001; v2=937.5, p<0.001 respectively). Specific dysfunctions frequently encountered in ASD
were dysfunctional posture and muscle tone, fine manipulative disability, dyscoordination, and
excessive associated movements.
CONCLUSION These findings suggest a contribution of dysfunctional supraspinal networks involving multiple parts of the brain in the pathogenesis of ASD. This is consistent with findings from
neuroimaging studies, and highlights the importance of neurological examinations in paediatric
psychiatric assessments.

Autism spectrum disorder (ASD) is an early childhood-onset

neurodevelopmental disorder characterized by delay and deviations in the development of social, communicative, and cognitive skills, and is associated with a very wide range of
syndrome expression. The term ASD encompasses children
with the full autism syndrome as well as variants, such as
Asperger syndrome, and pervasive developmental disorders
not otherwise specified.
Children with ASD are often described as clumsy13 or as
having motor deficits.46 In addition, psychiatric classification
systems cite stereotypes in motor behaviour (e.g. hand-flicking
or -twisting) as criteria for classifying ASD.7,8 However, little
is known about the neurological background of the clumsiness. Some studies report that children with ASD frequently
exhibit soft neurological signs,9 but only rarely are details of
these signs reported. Others report motor deficits but do not
refer to the neurological background of these deficits.46
Neuroimaging studies of ASD shed some light on the
neural substrate of ASD. Abnormalities are described in the

following neural systems:1012 (1) the cerebellum loss of

Purkinje cells and anomalies in the shape of the cerebellum
and vermix;13,14 (2) the cerebral cortex hyperplasia of grey
and white matter of the frontal, temporal, and parietal lobes,15
and abnormalities in the corpus callosum and ventricular systems;16,17 (3) the basal ganglia increased volume of caudate
nucleus and putamen;18 (4) the hippocampus reduction in
size and atrophy;19 and (5) the thalamus increased volume.20
These findings are inconsistent, which may in part be attributable to the heterogeneity of the disturbance itself and in part
to incompatible reference groups and technical limitations.11,21
Two recent theories on the origin of the neurological dysfunctions in ASD are the growth dysregulation hypothesis10
and the theory of abnormal neural connectivity in individuals
with ASD.22,23 The aforementioned findings and theories
suggest that dysfunctional neural circuitries underlie the
symptomatology of ASD. Surprisingly, little research has
focused on clinical neurological dysfunctions as an expression

The Authors. Developmental Medicine & Child Neurology 2011 Mac Keith Press

DOI: 10.1111/j.1469-8749.2011.03971.x 641

of dysfunctional neural circuitries. Nevertheless, understanding the neurological make-up of children may provide an
insight into the aetiology and pathogenesis of ASD and the
abilities and impairments of children with ASD, and may have
consequences for treatment. Therefore, in assessing children
with psychiatric problems such as ASD, examination of the
childs neurological condition may be important. One instrument with a satisfactory reliability for assessing a childs neurological condition24 is the examination according to
Touwen,25 a standardized and age-specific examination that
focuses on the presence of minor neurological dysfunctions
(MNDs).
The present study was conducted within the framework of
our larger study (n=705) on neurobehavioural relationships in
children with psychiatric morbidity26,27 and focuses on the
prevalence and type of MNDs in children with ASD. The
findings are compared with data on neurological dysfunction
obtained in children in a reference group who are representative of the general population. We tested the following
hypotheses: (1) the prevalence of complex MNDs in children
with ASD is higher than in children from the reference population. This assumption is based on the neuroimaging data
and the aforementioned theories that indicate that structural
deficits may underlie ASD; (2) specifically, the prevalence of
coordination problems and fine manipulative disabilities is
higher in children with ASD than in children from the reference population. This assumption is based on neuroimaging
data, which most frequently report abnormalities in cerebellar
and cerebral circuitries in children with ASD.

METHOD
Participants
The study group consisted of 122 children (93 males, 29
females; mean age 8y 1mo, SD 2y 6mo) who were diagnosed
with ASD according to the criteria for ASD of the Multi-Axial
Classification Scheme for Psychiatric Disorders in Childhood
and Adolescence, version 9 (MAC-ICD-9).8 The diagnosis of
ASD included full autism syndrome as well as variants, such as
Asperger syndrome, and pervasive developmental disorders
not otherwise specified. Participants in this study comprised
122 children diagnosed with ASD out of 705 children (513
males, 192 females; mean age 9y, SD 2y 0.5mo) who in the
period 1985 to 1999 had been referred to Fornhese, a regional outpatient non-academic diagnosis and treatment centre
for children with psychiatric problems. Each of the 705 children had undergone an extensive multidisciplinary child psychiatric assessment consisting of history taking, including
developmental history and parental report, family diagnostics,
and child psychiatric and neurological examination; previous
relevant diagnostic data and school information had also been
gathered. If required, the diagnostic programme was extended
to include other examinations such as a psychodiagnostic
assessment, an occupational therapeutic assessment, and a
supplementary medical examination. The final diagnosis and
classification were established by consensus in our team
conference on the basis of all collected information. The
diagnosis of ASD indicated that this was the childs primary
642 Developmental Medicine & Child Neurology 2011, 53: 641646

What this paper adds

This papers shows that the prevalence of complex MND in children with ASD
is higher than in children in the general population.
The data suggest a contribution of dysfunctional supraspinal networks
involving multiple parts of the brain in the pathogenesis of ASD.
The findings show that neurological examination is important in paediatric
psychiatric assessment.

psychiatric disorder and did not preclude the presence of additional behavioural symptoms.26 The prevalence of neurological dysfunctions in the 583 children with other psychiatric
disorders is also reported. Other psychiatric disorders included
emotional disorders (n=218; 31%), adjustment disorders
(n=90; 13%), conduct disorders (n=80; 11%), neurotic
disorders (n=56; 8%), attention-deficit disorders (n=57; 8%),
dyslexia (n=44; 6%), and special symptoms or syndromes
(n=30; 4%).
Reference data for MNDs in the general population were
based on data from a subgroup of 570 children of the Groningen Perinatal Project, a birth cohort born in Groningen University Hospital during the period 1975 to 1978.28,29 For these
children, information on neurological status at birth and at the
age of 9 years was available. Data on neonatal neurological
morbidity in the general population (Berghs G, Spanjaards E.
De normale zwangerschap: Bevalling en beleid. PhD thesis,
University of Nijmegen, Netherlands, 1988) permitted us to
extrapolate the prevalence of MNDs at the age of 9 years in
the general population.29,30
Table I presents the most important demographic characteristics of the children with ASD, the children with other psychiatric disorders, and the reference group. Cognitive testing
revealed that the Full-scale IQ of the large majority of children
was average. Only 6.6% of the children with ASD had an
intellectual disability (Full-scale IQ <70). This reflects the
situation in the Netherlands, where children with serious deficits in cognitive function and or communication are referred
to facilities providing services for people with intellectual
disability.

Procedure
As part of the extensive multidisciplinary child psychiatric
assessment, every child underwent a neurological examination
according to Touwen25 that was supplemented with aspects
important for the judgement of the neuropsychiatric condition
of the child, for example aspects of language development,
attention, tics, quality of contact, and physical anomalies. This
extended examination was always conducted in the same testing room by two of the authors (MdJ and MP), blinded to the
childs final diagnosis, and could be accomplished in about
1 hour.
The examination according to Touwen is a standardized,
detailed, and age-specific examination that pays special attention to the presence of MNDs. Signs of dysfunction are taken
into account only if they occur in functional domains. The
presence of a single sign of dysfunction, such as a positive
Babinski reflex without other signs, does not lead to a diagnosis of MND. The domains are organized according to the
functional neurobehavioural subsystems of the nervous system

Table I: Demographic characteristics and mean Full-scale IQ of the group

with autism spectrum disorder (ASD), the group with other psychiatric
disorders, and the reference group
Other
psychiatric
disordersb
(n=583), n (%)

Reference
group,c
n (%)

93 (76)
29 (24)
8.1 (2.6)

420 (72)
163 (28)
9.2 (1.8)

254 (45)
316 (55)
9

44 (36)
68 (56)
1 (1)
9 (7)
92.5 (18.1)

370 (63)
204 (35)
5 (1)
4 (1)
97.5 (15.9)

534 (94)
36 (6)
0
0
NA

ASD groupa
(n=122), n (%)
Sex
Males
Females
Age, mean (SD)
Education
Mainstream primary
Special primary
Secondary
Other none
Full-scale IQ, mean (SD)
a

Classification of ASD according to the Multi-Axial Classification

Scheme for Psychiatric Disorders in Childhood and Adolescence,
version 9 (MAC-ICD-9) classification system. bOther psychiatric
disorders: classification on the MAC-ICD-9 classification system.
c
Reference group described by Hadders-Algra et al.28 NA, not available.

that are used in clinical practice.28 On the basis of the examination, children were classified as neurologically typical, having a simple MND or a complex MND, or as neurologically
atypical. Children with clear neurological abnormalities (e.g.
cerebral palsy or spina bifida) were excluded from the study.
Children were classified as neurologically typical if no domain
of dysfunction was present, as having a simple MND if one or
two domains were scored as deviant, and as having a complex
MND in the case of three or more dysfunctional domains (for
details see Peters et al.24). Simple MND can be regarded as
the expression of a normal but non-optimally developed brain,
is only weakly related to pre- and perinatal adversities, and is
associated with a mild risk of learning and behavioural problems. In contrast, complex MND is strongly related to preand perinatal adversities and is associated with a high risk of
learning and behavioural problems.28,29

Data analysis
v2 tests were used to compare the prevalence of MNDs and
the prevalence of the specific domains of dysfunction between
the group with ASD and the group with other psychiatric
disorders. The prevalence of MNDs and of the specific

domains of dysfunction in the group with ASD were compared with that of the reference group by performing v2 goodness-of-fit tests. Results were considered statistically
significant at p<0.05.

RESULTS
Prevalence of simple MND and complex MND
Children with ASD often showed complex MNDs (74%; see
Table II). The prevalence of simple MNDs was 21%. The
prevalence of MNDs in children with other psychiatric disorders was somewhat but not significantly lower (Table II).
MNDs occurred substantially more often in the children with
ASD than in the reference group of 9-year-olds (p<0.001).
Prevalence of specific domains of dysfunction
The prevalence of the dysfunctional domains in children with
ASD, the children with other psychiatric disorders, and the
reference group is shown in Table III. The most frequently
occurring dysfunctional domains in children with ASD were
posture and muscle tone and fine manipulative abilities. Mild
abnormalities in coordination were present in about 60% and
an excess of associated movements in 40 to 45%. Deviances
were also found in the domains of cranial nerve function,
involuntary movements, reflexes, and sensory function, but
less frequently. Children with ASD more often exhibited dysfunctions in the domains of posture and muscle tone, reflexes,
coordination, and sensory function than did children with
other psychiatric disorders. All types of dysfunction occurred
significantly more often in the children with ASD than in the
reference group.
DISCUSSION
The present study demonstrated that about 95% of children
with ASD showed MNDs, particularly complex MNDs. They
particularly exhibited dysfunctional posture and muscle tone
regulation, fine manipulative disabilities, dyscoordination, and
an excess of associated movements. Other types of neurological dysfunction were also more prevalent in children with
ASD than in the general population, but less prominently so.
Strengths and limitations of our study
To the best of our knowledge, this study is the first to assess
systematically the presence of MNDs in a large cohort of

Table II: Prevalence of minor neurological dysfunction (MND) in children with autism spectrum disorder (ASD), children with other psychiatric disorders,
and the reference group

Neurological
classification
Normal
Simple MND
Complex MND
Total

ASD,a n (%)

Other psychiatric
disorders,b
n (%)

Comparison of the
ASD group and the group with
other psychiatric disorders (v2)

Reference
groupc (%)

Comparison of the
ASD group and the reference
group (goodness of fit)

6 (5)
24 (21)
83 (74)
113 (100)d

82 (14)
192 (34)
300 (52)
574 (100)d

v2=18.0; df=2; p<0.001

79
15
6
100

v2=937.5; df=2; p<0.001

Classification of ASD according to the Multi-Axial Classification Scheme for Psychiatric Disorders in Childhood and Adolescence, version 9
(MAC-ICD-9) classification system. bOther psychiatric disorders: classification on the MAC-ICD-9 classification system. cReference group described
by Hadders-Algra et al.28. dTotal number is lower than in Table I because for some children one or more MND domains of dysfunction could not
be determined because they could not perform the required tests. Maximum number missing is nine.

Autism and Minor Neurological Dysfunction Marianne de Jong et al. 643

Table III: Prevalence of the specific types of minor neurological dysfunction (MND) in children with autism spectrum disorder (ASD) compared with children
with other psychiatric disorders and the reference group

Type of MND
Mild dysfunction in posture
and muscle tone regulation
Mildly abnormal reflexes
Mild dyskinesia
Mild coordination problems
Mild fine manipulative disability
Excess of associated movements
Mild sensory dysfunction
Mild cranial nerve dysfunction

ASDa
(n=122),b
n (%)

Other psychiatric
disorders
(n=583),c n (%)

Comparison of the
ASD group with the
group of other
psychiatric disorders (v2)

106 (87)

340 (58)

v2=35.4, df=1, p<0.001

11.7

v2=667.5, df=1, p<0.001

26 (23)
29 (25)
65 (58)
84 (75)
47 (45)
17 (15)
41 (39)

69 (12)
126 (22)
164 (29)
405 (70)
245 (42)
34 (6)
178 (31)

v2=9.4; df=1; p=0.002

v2=0.81; df=1; p=0.37
v2=35.8; df=1; p<0.001
v2=1.3; df=1; p=0.26
v2=0.23; df=1; p=0.63
v2=12.2; df=1; p<0.001
v2=2.52; df=1; p=0.11

10.7
13.0
4.3
7.0
<0.5
NAe
<0.5

v2=17.1; df=1; p<0.001

v2=15.6; df=1; p<0.001
v2=785.9; df=1; p<0.001
v2=795.5; df=1; p<0.001
v2=4134.8; df=1; p<0.001

v2=3105.8; df=1; p<0.001

Reference
groupd (%)

Comparison of the ASD

group and the reference
group (goodness of fit)

Classification of autism spectrum disorder according to the Multi-Axial Classification Scheme for Psychiatric Disorders in Childhood and
Adolescence, version 9 (MAC-ICD-9) classification system. bThe number differs for each cell because for some children the MND-domains could
not be determined because they could not perform the required tests. Maximum number missing is 17 (domain 6). cOther psychiatric disorders:
classification on the MAC-ICD-9 classification system. dReference group described by Hadders-Algra et al.28 eRarely occurring, but no details
available. NA, not available.

children with psychiatric morbidity who were referred to a

third-level clinical child psychiatric centre. More specifically,
the strengths of our study are that: (1) it applied a standardized, reliable, and internationally used age-specific neurological examination for the assessment of MNDs; (2) the study
population consisted of children referred to a regional centre
of child psychiatry because our group lacks the selection of
referrals to a university hospital, the results presumably are
representative for the average paediatric psychiatric population; (3) an extensive multidisciplinary child psychiatric assessment, including psychiatric interviews, was conducted for all
participants; and (4) the majority of children in the study
group had normal Full-scale intelligence, indicating that, even
in children in whom ASD is not complicated by an intellectual
disability or medical condition, neurological morbidity, as
defined by MNDs, is highly prevalent. However, the typical
intelligence of our study group also means that it is not possible to generalize our results to all children with ASD because
autism is often associated with intellectual disability.
The classification of ASD was not based on a single standardized psychiatric assessment, such as questionnaires, but on
extensively documented individual files from careful multidisciplinary psychiatric assessments. This might be considered a
limitation of this study in terms of reliability. However, we
previously reported that the clinical diagnosis in our cohort
was reliable in terms of symptom diagnostics.26
The use of the MAC-ICD-9 instead of a more recently
developed classification system such as the Diagnostic and Statistical Manual of Mental Disorders, 4th edn. (DSM-IV)31 for
the classification of clinical syndromes might be regarded as
another limitation. However, we believed that continuing to
use the MAC-ICD-9 classification system, rather than changing the classification system mid-course, would be more reliable in terms of achieving homogeneity of data over the long
period of data collection.26 In addition, the description of the
primary diagnosis of ASD in MAC-ICD-9 and DSM-IV is
almost identical. The systems differ in the way that they deal
644 Developmental Medicine & Child Neurology 2011, 53: 641646

with the subtypes of ASD, but for the current study this difference is not relevant.
In addition, the fact that the data were collected over a long
period of time and that some children were diagnosed about
25 years ago may be considered a limitation of the study. Since
then, the prevalence of the diagnosis of ASD has increased
from 0.1 to 0.6% as a result of a broadening of the concept, an
expansion of diagnostic criteria, the development of services,
and an improved awareness of the condition.32 This may
imply that the children included in our study have relatively
serious forms of ASD.
Finally, the fact that we used a historical reference group
may be considered a limitation the data for the general population were collected about 10 years earlier than those of the
children with psychiatric morbidity. Recently, it has been suggested that over the last decade the prevalence of MND has
been changing.33,34 For instance, the prevalence of choreiform
dyskinesia has decreased and that of coordination problems
and simple MND has increased. The prevalence of complex
MND, however, has been stable over time.33 This means that
our findings on complex MND, fine manipulative disability,
dysfunctional posture and muscle tone, and excessive associated movements presumably are valid, notwithstanding the
use of the historical reference group. Kikkert et al.35 recently
reported higher rates of MND (37% simple MND and 13%
complex MND) in children born at term. The higher prevalences in this study may be attributed to the studys selection
criteria, as a major part of the study group were selected on
the basis of formula feeding.

Findings and clinical implications

Other studies have reported on clumsiness,13 motor deficits,46 and neurological soft signs9 in children with ASD, but
this is the first study to report on the severity and type of
MND in children with ASD. Our study revealed that about
three-quarters of the children with ASD showed complex
MND, which points to distinct brain dysfunction and the

involvement of various parts of the brain in the disorder. Our

neurological findings are consistent with the heterogeneity
reported in the imaging data and with the theories of growth
dysregulation and abnormal connectivity. The frequently
occurring types of neurological dysfunction suggest which
parts of the brain may be involved. They suggest dysfunctions
in cortical structures (dysfunctions in fine manipulative abilities), in cerebellarbrainstem circuitries (dysfunctional regulation of posture and muscle tone and coordination), and more
global dysfunction (excess of associated movements, which
may point to immature or inadequate pathways and or a large
effort during performance). The children with other psychiatric disorders also showed a high prevalence of complex MND,
indicating that distinct brain dysfunction predisposes the children to a variety of psychiatric disorders. The finding of a high
prevalence of fine manipulative dysfunction in children with
other psychiatric disorders suggests that cortical dysfunction
in particular is associated with psychiatric morbidity. In contrast, coordination problems, sensory dysfunction, and dysfunctional posture and muscle tone regulation were more
strongly associated with ASD than with other psychiatric morbidity. This suggests a stronger contribution of dysfunction of
subcortical structures to ASD than to other child psychiatric
disorders.
The results of our study highlight the importance of a neurological examination as a part of a paediatric psychiatric

assessment, because it furnishes information about the type

and severity of brain dysfunction without invasive or expensive
procedures. The early detection of an MND and the type of
dysfunction can provide direction to treatment of maladaptive
behaviour, taking into account the limitations in the childs
brain function,33 and can provide insight into the consequences for daily life of each individual child. For instance, in
our centre, a childs neurological condition serves as one of
the indicators for referral to physical and occupational
therapy.

CONCLUSION
The majority of children with ASD show complex MND.
This finding underlines the idea that ASD is not due to dysfunction of a single specific structure in the brain, but that it is
based on dysfunctional supraspinal networks in which multiple
parts of the brain play a role. Children with ASD are often
described as clumsy. We propose abandoning the term
clumsy and using descriptions based on neurological dysfunction instead.
ACKNOWLEDGEMENT
The Open Ankh Foundation, Soesterberg, the Netherlands, provided
financial support for this study.

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