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Published in final edited form as:

J Pediatr Neuropsychol. 2019 September ; 5(3): 77–84. doi:10.1007/s40817-019-00069-z.

Beery VMI and Brain Volumetric Relations in Autism Spectrum

Disorder
Ryan R. Green1, Erin D. Bigler1,2,3,4, Alyson Froehlich3, Molly B. D. Prigge5, Brandon A.
Zielinski4,5, Brittany G. Travers6,7, Jeffrey S. Anderson8, Andrew Alexander6,9,10, Nicholas
Lange11,12, Janet E. Lainhart6,10
1Department of Psychology, Brigham Young University, 1001 SWKT, Provo, UT 84602, USA
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2Neuroscience Center, Brigham Young University, Provo, UT, USA

3Department of Psychiatry, University of Utah, Salt Lake City, UT, USA
4Department of Neurology, University of Utah, Salt Lake City, UT, USA
5Department of Pediatrics, University of Utah, Salt Lake City, UT, USA
6Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin-Madison, Madison,
WI, USA
7Occupational Therapy Program, University of Wisconsin-Madison, Madison, WI 53705, USA
8Department of Radiology, University of Utah, Salt Lake City, UT, USA
9Department of Medical Physics, University of Wisconsin-Madison, Madison, WI, USA
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10Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA

11Departments of Psychiatry and Biostatistics, Harvard University, Boston, MA, USA
12Neurostatistics Laboratory, McLean Hospital, Belmont, MA, USA

Abstract
Although diminished proficiency on tasks that require visual-motor integration (VMI) has been
reported in individuals with autism spectrum disorder (ASD), very few studies have examined the
association between VMI performance and neuroanatomical regions of interest (ROI) involved in
motor and perceptual functioning. To address these issues, the current study included an all-male
sample of 41 ASD (ages 3–23 years) and 27 typically developing (TD) participants (ages 5–26
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years) who completed the Beery-Buktenica Developmental Test of Visual-Motor Integration

(Beery VMI) as part of a comprehensive neuropsychological battery. All participants underwent
3.0 T magnetic resonance imaging (MRI) with image quantification (FreeSurfer software v5.3).
The groups were statistically matched on age, handedness, and intracranial volume (ICV). ASD
participants performed significantly lower on VMI and IQ measures compared with the TD group.
VMI performance was significantly correlated with FSIQ and PIQ in the TD group only. No pre-
defined neuroanatomical ROIs were significantly different between groups. Significant
correlations were observed in the TD group between VMI and total precentral gyrus gray matter

Erin D. Bigler erin_bigler@byu.edu.

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volume (r = .51, p = .006) and total frontal lobe gray matter volume (r = .46, p = .017). There were
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no significant ROI correlations with Beery VMI performance in ASD participants. At the group
level, despite ASD participants exhibiting reduced visuomotor abilities, no systematic relation
with motor or sensory-perceptual ROIs was observed. In the TD group, results were consistent
with the putative role of the precentral gyrus in motor control along with frontal involvement in
planning, organization, and execution monitoring, all essential for VMI performance. Given that
similar associations between VMI and ROIs were not observed in those with ASD,
neurodevelopment in ASD group participants may not follow homogenous patterns making
correlations in these brain regions unlikely to be observed.

Keywords
Autism; Typical development visual-motor integration; MRI; Volumetrics
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Introduction
In Kanner’s 1943 Autistic disturbances of Affective Contact publication, he observed that
“several of the children were somewhat clumsy in gait and gross motor performances…”
(p.248). Since that initial observation, a number of studies have confirmed that motor skill
acquisition and development in autism spectrum disorder (ASD) may be attenuated, at least
in some compared with typically developing (TD) children, where significant differences
have been noted on neuropsychological tests of motor control, dexterity, and speed,
including visuomotor tasks (Braddick and Atkinson 2013; Cook 2016; Elabbagh and
Johnson 2016; Van Damme et al. 2015; Leisman et al. 2015; Green et al. 2015; Travers et al.
2015 and 2016; Sharer et al. 2015, 2016, Wang et al. 2015).
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One of the most commonly used clinical measures of visuomotor functioning in the
assessment of child development is the Beery-Buktenica Developmental Test of Visual-
Motor Integration (Beery VMI; Beery 1996; Beery and Beery 2004). In a previous study that
examined Beery VMI in an ASD compared with TD sample, we found overall lower Beery
VMI performance in individuals with ASD but did not explore neuroanatomical correlates.
Neuroanatomically, the integrity of cortical (frontal and parietal lobes) and subcortical
(white matter, basal ganglia, thalamus, brainstem) motor areas along those involved in
somatosensory and visual processing (parietal and occipital lobes, respectively) would be
considered key regions of interest (ROI) to explore in relation to VMI performance. Indeed,
these ROIs constituted the a priori regions that were examined in the current study.
Furthermore, within the lobular and cerebellar ROIs, white and gray matter volumes were
calculated, as white matter volume has implications for brain connectivity and cortical gray
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matter as reflecting cellular integrity. If volumetric differences were observed in any of these
ROIs between ASD and TD research participants, such findings may provide additional
understanding as to the neurobiology of autism, and specifically to the motor impairments
that may be associated with autism.

A variety of quantitative magnetic resonance imaging (MRI) techniques are suitable for
extracting volumetric ROIs, with the most commonly used method being FreeSurfer (see:

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FreeSurfer https://surfer.nmr.mgh.harvard.edu/ ). These tools have been particularly useful in

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understanding the potential neuroanatomical basis of motor impairment in other disorders

where motor involvement is commonplace, including children born pre-term (Sripada et al.
2015), fetal alcohol spectrum disorders (FASD; Wozniak et al. 2016), and attention-deficit/
hyperactivity disorder (ADHD; Castellanos and Aoki 2016), as well as ASD (Lo et al. 2016;
Sharer et al. 2015, 2016). Specific to FreeSurfer-based volumetric studies, Sripada and
colleagues (Sripada et al. 2015) used the FreeSurfer method for ROI neuroimage
quantification in a cohort of adults with a history of very low birth weight (VLBW) and
compared Beery VMI performance with neuroanatomical regions involved in motor and
perceptual control. These researchers found that, compared with term-born controls, the
VLBW group performed more poorly on tasks of VMI and that these neurocognitive
measures were significantly related to several neuroanatomical ROIs important for
perceptual processing and motor functioning.
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In the current study, we used FreeSurfer volumetric findings to explore neuroanatomical ROI
correlates of VMI performance in a legacy sample of ASD participants compared with TD
controls, as part of a longitudinal neuroimaging project of autism. To control for multiple
comparisons, only the a priori, the ROIs mentioned above were selected because of their
assumed role in motor and perceptual control in visuomotor functioning and potential
relations in ASD (see Stigler et al. 2011). This study had three primary aims: (1) to examine
group differences in VMI performance between ASD and TD participants, (2) to examine
whether volumetric differences in neuroanatomical ROIs were present between the two
groups in known regions that participate in motor control, and (3) to examine
neuroanatomical relations between ROIs and VMI performance in both groups. Following
previous literature published on individuals with ASD compared with TD controls, we
predicted differences in VMI performance between groups and that as a group, ASD
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participants would display attenuated VMI and IQ performance compared with the TD
group. We further predicted that the two groups would differ in MRI-based volumetric ROIs
and how those neuroanatomical regions related to VMI performance, lending insight into the
brain-behavior relations of visuomotor ability in ASD.

Method
Subjects and Assessment
Ascertainment—Although full details regarding participants have been previously
published (Alexander et al. 2007; Bigler et al. 2003), a brief description will be given here.
ASD and TD participants were recruited over a 10-year period (1997–2007) as part of an
NIH-funded longitudinal neuroimaging study of autism. The data for this investigation was
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designated based on the reference norms of the Beery VMI from initial participant data
collection and closeness of MRI scan date (within 6 months) to Beery VMI administration.
As previously described (see Green et al. 2015), this investigation was undertaken with the
written consent of each subject or legal guardian, with full approval of the University of
Utah and Brigham Young University Institutional Review Boards.

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Participant Groups—Participants were male from the ages of 3–26 years, with basic
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demographic information provided in Table 1. Analyses of potential sex differences were not
possible with these data, as all participants were males. Forty-one ASD participants and 27
TD participants comprised the groups.

Autism Sample—Autism was rigorously assessed in all participants using the Autism
Diagnostic Interview-Revised (ADI-R; Lord et al. 1994) and the Autism Diagnostic
Observation Schedule-Generic (ADOS-G; Lord et al. 2000). Medical and genetic causes of
autism were excluded as determined by history, physical exam, fragile-X gene testing, and
karyotype. Similarly, the TDC group was examined with comparable methods involving
direct interview and questionnaires and had no history of learning, developmental, cognitive,
neurological, or neuropsychiatric problems.

Control Sample—All control participants were also male and matched on age with ASD
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participants. As stated above, no developmental, neurological, or clinical histories of major

psychiatric disorder were observed in any of the control participants. All control participants
completed an assessment with the ADOS-G to rule out ASD.

Measures
IQ Four measures of intellectual functioning were used in the study because age differences
and changes in IQ test instruments over the 10 years of recruiting subjects. For the present
investigation, FSIQ, VIQ, and PIQ were measured using the Wechsler Intelligence Scale for
Children-Third Edition (WISC-III; Wechsler 1991), Wechsler Adult Intelligence Scale-Third
Edition (WAIS-III; Wechsler 1997), Wechsler Abbreviated Scale of Intelligence (WASI;
Wechsler 1999), or Differential Ability Scales (DAS; Elliott 1990).
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Handedness—The Edinburgh Handedness Inventory (Oldfield 1971) was used to assess

handedness. A score of +100 signifies complete right handedness and a score of − 100
indicates complete left handedness. A score of 0 would suggest mixed handedness or
ambidexterity.

Visual-Motor Integration—The Beery-Buktenica Developmental Test of Visual-Motor

Integration (Beery VMI; Beery 1989; Beery 1996; Beery and Beery 2004) was used to
assess VMI. The Beery VMI is comprised of drawings of geometric designs that increase in
difficulty and which did not change over the course of the parent project. The geometric
designs are observed and copied with paper and pencil. Objective scoring criteria are based
on the accuracy with which the designs were copied, with higher scores reflecting better
visual-motor ability. The Beery VMI has good reliability and validity. Raw scores were
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converted to standard scores based on participant age.

Neuroimaging—Volumetric studies were based on magnetic resonance images acquired

on a Siemens Trio 3.0-T scanner at the University of Utah. A 12-channel RF head coil was
used to obtain 3D T1-weighted image volumes with 1-mm isotropic resolution using an MP-
RAGE sequence (TI = 900 msec, TR = 2300 msec, TE = 2.91 msec, flip angle = 9°, sagittal,
field of view = 25.6 cm, matrix = 256 × 256 × 160).

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Volumetric Image Analysis—All analyses were performed with FreeSurfer, version 5.3
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(http://surfer.nmr.mgh.harvard.edu/), following the methods detailed by Bigler et al. (2010),

using the Destrieux et al. (2010) parcellation method for cortical structures (https://
surfer.nmr.mgh.harvard.edu/fswiki/CorticalParcellation) and the standard FreeSurfer output
for subcortical ROIs. Volume calculations for the following ROIs were obtained: frontal lobe
gray matter (GM), frontal lobe white matter (WM), precentral gyrus GM, parietal lobe GM,
parietal lobe WM, occipital lobe GM, occipital lobe WM, cerebellum GM, cerebellum WM,
basal ganglia, thalamus, brain stem, and corpus callosum. Intracranial volume (ICV) was
used as a matching variable.

Statistical Analysis
One-way analyses of variance (ANOVA) was performed to determine whether between-
group differences existed in sample characteristics and neuroanatomical ROIs. Pearson
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correlations were computed to determine associations between VMI performance and IQ

variables and between VMI performance and neuroanatomical ROIs. Differences in
correlations between ROIs and VMI performance between groups were compared. Group-
matching variables were not used as covariates, given they did not significantly differ. Group
differences in IQ variables were assessed but not used as covariates, as per the
recommendation of Dennis et al. (2009), when examining neurocognitive outcome where IQ
disparities are assumed to be present between the TD and target group under investigation.

Results
Sample Characteristics
No significant differences between ASD and TD groups were observed in matching
variables including age, handedness, or intracranial volume (see Table 1).
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VMI and IQ Relationships

As reported in Table 1, Beery VMI performance and all IQ variables were significantly
lower in the ASD group compared with the TD group. Some IQ variables did not pass the
tests of homogeneity of variance (Levene’s test). However, the results remained the same
after applying a robust Welch’s t test (Shieh and Jan 2015).

Pearson correlations for VMI performance and IQ variables are summarized in Table 2. All
IQ variables in both ASD and TD groups were correlated with one another as expected.
However, none of the IQ variables were significantly correlated with Beery VMI
performance in the ASD group, whereas FSIQ and PIQ were significantly correlated with
VMI performance in the TD group.
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VMI and Neuroanatomical ROI

ANOVA was performed to determine whether significant differences were observed between
ASD and TD groups on neuroanatomical ROI. Assumptions of homogeneity of variances
were met. Interestingly, no ROI significantly differed between groups (see Table 3).

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Pearson correlations were conducted to assess the relation between VMI performance and
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neuroanatomical ROIs. In the TD group, significant correlations between VMI performance

and neurological ROIs were found in total precentral gyrus volume (r = .51, p = .006) and
total frontal lobe gray matter volume (r = .46, p = .02). No significant correlations were
found between VMI and ROIs in the ASD group. Contrary to our hypothesis, no correlations
between ROIs and VMI performance were significantly different between groups.

Discussion
The aims of the current study were to examine VMI performance between ASD and control
participants between the ages of three and twenty-six who were statistically matched on age,
handedness, and intracranial volume; examine whether volumetric differences in
neuroanatomical ROIs were observable between the groups; and examine whether
correlations were observable between neuroanatomical ROIs and VMI performance in both
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groups. As a group, the ASD sample performed more poorly on the Beery VMI compared
with the TD group. However, only the TD group’s VMI scores were positively correlated
with FSIQ and PIQ. Contrary to one of our stated hypothesis, there were no differences
found between the groups in MRI-based volumetric measures of neuroanatomical ROIs.
Consistent with one of our hypotheses, VMI performance in the TD group was associated
with total precentral gyrus volume and total frontal lobe gray matter volume. In contrast,
VMI performance did not relate to any of the investigated volumetric measures in the ASD
group. As will be explained below, the lack of anatomical relations of VMI with known
motor regions suggests difference in motor network integrity between ASD and TD
individuals.

In acquired focal brain injury, parietal damage may be particularly disruptive to visuomotor
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functioning (Mutha et al. 2011). However, in the current investigation, parietal volumes did
not differ between the ASD and TD participants. Accordingly, at a gross volumetric level, no
major structural differences in parietal volume were found that distinguished ASD from TD
controls.

ASD is a complex neurodevelopmental disorder associated with neurocognitive and

neurobehavioral anomalies. Contemporary theories conceptualize part of the pathobiology of
ASD in terms of disrupted neural networks and connectivity associated with the social,
language, sensory-motor, and cognitive features of the disorder (Caeyenberghs et al. 2016;
Duffield et al. 2013; Geschwind 2009; Gidley-Larson and Mostofsky 2008; Gilbert et al.
2009; Keary et al. 2009; Minshew et al. 1997; Southwick et al. 2011). Although this study
examined only whether there were volumetric anatomical differences in known motor areas,
the findings may suggest network dysfunction as the basis for reduced VMI efficiency in
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ASD. Motor network dysfunction in ASD has been implicated by other studies (see Müller
et al. 2003; Travers et al. 2015, 2016; Turner et al. 2006) and in this investigation is likely
the reason why there were significant and positive relations with some of the motor ROIs in
the TD controls but not the ASD group. Three motor ROIs in the TD group with known
involvement in motor control (i.e., precentral gyrus) or with planning, organization, and
execution monitoring (i.e., frontal lobe) of motor function positively related to VMI
performance, whereas none of the correlations were significant in the ASD group. This

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suggests a size-function disparity between a ROI and neuropsychological task between the
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ASD and TD controls (see Bigler 2015). Since the areas that correlated in the TD group are
required to effectively complete VMI-related tasks, the lack of correlation in the ASD
participant group suggests that those regions likely were organized differently. Thus, based
on the current findings, it does not appear that there are any coarse abnormalities in basic
motor system ROIs in ASD, but underlying motor networks likely differ. As such, better
clarification of motor system impairments will likely be derived from white matter and
network-based models that assess motor systems with different neuroimaging techniques
(see Catani and Bambini 2014; Just et al. 2012; Kawahara et al. 2016; Travers et al. 2015.
2016) that may also explore other relations of motor development with language and
cognitive functioning in ASD (Hannant 2018; Lim et al. 2015). It may also be the case, as
demonstrated by Travers et al. (2016) that subtle white matter pathology at the level of the
brainstem may relate to motor anomalies in ASD. As such, analyses at the cortical and
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subcortical levels would yield no major findings, as was the case with the current
investigation. Additionally, from a connectivity standpoint, network abnormalities in ASD
have implicated disrupted interhemispheric connectivity (Alexander et al. 2007; Prigge et al.
2013), frontal-parietal dysconnectivity (Just et al. 2012), atypical white matter
microstructure development (Cheng et al. 2010; Wolff et al. 2012), and cerebellar
connectivity (Mostofsky et al. 2009) as well as distributed network of cortical structural
abnormalities (Zielinski et al. 2012), all of which could also affect the integration of motor
control and VMI performance. Most recently, using an MRI-based resting-state functional
connectivity mapping approach, Oldehinkel et al. (2019) demonstrated alterations both
within- and between-network connectivity involving the cerebellum, visual, and sensory-
motor networks, which they argued underlying the often-observed impairments in
multisensory and visuomotor functioning in ASD. Similarly, King et al. (2018), also using
MRI-based functional connectivity methods, demonstrated significantly decreased
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synchrony across brain regions in individuals with autism compared with TD controls,
primarily in connections between the default mode and limbic networks with somatomotor
networks. These observations highlight how connectivity involving visuomotor functioning
relates to networks associated with emotional and cognitive control. The current findings
point out the limits of modular approaches to understanding regional specificity in ASD. As
improvement in connectomic research and ASD progress (see Sathyanesan et al. 2019;
Mevel and Fransson 2016), an improved understanding of which brain areas contribute to
VMI performance and impairment will likely emerge.

Investigating these regions with DTI and functional MRI methods may yield additional
insights into why VMI ability appears to be diminished in at least a subset of individuals
with ASD and whether this may reflect differences in white matter microstructure and/or
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abnormalities within motor and perceptual networks. Additionally, using a multimodality

approach to image and network analyses associated with visuomotor control will provide
methods for exploring how social deficits in autism relate to visuomotor impairment (see
Nebel et al. 2016). Such studies await to be conducted.

There are limitations to the current investigation. For example, the sample did not include
females and therefore, generalizability is limited. Additionally, this study represents a cross
sectional investigation of neuroanatomical ROIs and VMI performance across a large age

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range. To more fully understand the relations between these variables, longitudinal
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examinations need to be undertaken. Furthermore, as already indicated, the current study did
not investigate white matter integrity measures (e.g., DTI) to understand the functional
connectivity between putative ROIs involved in VMI performance. Additional studies in this
area will likely help elucidate the relationships between these variables.

Another limitation of the current study, as reflected in the descriptive participant overview in
Table 1, is the average intellectual functioning of the ASD sample, indicating at a group
level, these ASD participants would be considered “high functioning (see Mottron 2004)”,
yet had, in general, lower scores on intellectual assessment. Accordingly, these findings may
not generalize toward ASD individuals with lower levels of intellectual ability, or levels
more in line with the TD group, which had significantly higher verbal, performance, and
full-scale IQ scores than the ASD sample. Whether the TD findings would remain in a
matched IQ group with ASD participants is not known and should be investigated.
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In summary, the findings of the current study suggest that VMI and IQ performance is
attenuated in ASD at the group level compared with controls. However, no group differences
were observed in neuroanatomical ROIs between groups, whereas positive correlations were
observed in the TD group, but not the ASD group, between visuomotor performance and
total precentral gyrus and frontal lobe gray matter volumes. These findings suggest that,
although no mean differences in anatomical ROIs were observed between the groups, there
are likely network differences that relate to VMI performance.

Acknowledgments
This work was supported by the NICHD U19 HD35476 (University of Utah), the NICHD/NIDCD Collaborative
Programs of Excellence in Autism (CPEA), the NIH Mental Retardation/Developmental Disabilities Research
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Center (MRDDRC-Waisman Center), NIMH 62015 (ALA), and NIDA15879 (ALA). The technical assistance of
Tracy J. Abildskov is gratefully acknowledged.

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Table 1

Sample characteristics using pairwise deletion

ASD TD F P d
Green et al.

n Mean SD Range n Mean SD Range

Age (years) 41 10.87 4.90 3–23 27 12.41 4.94 5–26 1.599 .21 .31
Handedness 41 60.42 57.78 − 100–100 27 68.56 44.21 − 80–100 0.385 .54 .16
ICV 41 1,601,121 149,810 See below 27 1,572,721 224,375 See below 0.393 .53 .15
Beery VMI 41 92.59 19.329 60–141 27 105.96 14.450 75–143 9.44 .003 .78
FSIQ 40 95.35 22.246 58–137 27 119.67 15.387 95–153 24.34 .001 1.27
VIQ 36 96.28 23.813 51–145 27 115.15 15.593 91 –151 12.81 .001 .94
PIQ 41 98.46 20.529 64–133 27 117.44 15.802 88–152 16.58 .001 1.04

ASD, autism spectrum disorder; TD, typically developing; handedness, Edinburgh Handedness Inventory based on a scale from − 100 (left-handed) to 100 (right-handed); ICV, intracranial volume;
intracranial volume range ASD 1,240,747.10–1,942,259.20; TD 1,000,272.80–1,940,526.00; FSIQ, full-scale IQ; PIQ, performance IQ (non-verbal IQ), VIQ, verbal IQ

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Table 2

Correlation matrix of Beery VMI and IQ with listwise deletion

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ASD (n = 36) TD (n = 27)

Variable FSIQ PIQ VIQ FSIQ PIQ VIQ

Beery VMI .20 .27 .04 .55* .56* 0.32

FSIQ - .89* .89* - .91* .85*

PIQ - - .62* - - .72*

Beery VMI Beery-Buktenica Developmental Test of Visual-Motor Integration, ASD autism spectrum disorder, TD typically developing,
*
p < 0.003
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Table 3

Volumes of neuroanatomical regions of interest (mm3)

ASD (n = 41) TD (n = 27)

Green et al.

ROI Mean SD Mean SD F p

Frontal lobe GM 254,581.29 28,822.798 257,089.11 25,076.392 0.14 .71
Parietal lobe GM 158,009.61 21,436.207 151,246.63 13,810.765 2.11 .15
Occipital lobe GM 59,344.85 7126.595 56,793.96 5458.168 2.49 .12
Frontal lobe WM 174,339.39 23,617.228 181,362.67 24,470.650 1.34 .24
Parietal lobe WM 107,643.10 14,297.206 108,841.44 14,865.077 0.11 .74
Occipital lobe WM 42,359.78 7282.371 43,752.67 6274.968 0.66 .42
Precentral gyrus GM 32,491.22 3987.538 32,625.48 3835.801 0.02 .89
Cerebellum WM 27,519.02 4398.803 28,013.15 4105.596 0.22 .64
Cerebellum GM 124,784.93 13,050.738 126,380.67 15,103.726 0.22 .65
Basal ganglia 25,302.10 3229.263 25,400.04 3082.642 0.02 .90
Brain stem 21,843.66 2989.289 22,548.74 2900.359 0.93 .34
Thalamus 16,850.61 2077.980 16,865.96 2078.480 <.01 .98
Corpus callosum 3000.00 532.687 3208.74 554.027 2.4 .12

ASD, autism spectrum disorder; TD, typically developing; ROI, neuroanatomical region of interest; GM, gray matter; WM, white matter

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