Beery Vmi Performance in Autism Spectrum Disorder
Beery Vmi Performance in Autism Spectrum Disorder
Beery Vmi Performance in Autism Spectrum Disorder
Author manuscript
Child Neuropsychol. Author manuscript; available in PMC 2017 January 01.
Author
Ryan R. Green1, Erin D. Bigler*,1,2,3, Alyson Froehlich3, Molly B.D. Prigge3, Brittany G.
Travers4, Annahir N. Cariello3, Jeffrey S. Anderson5, Brandon A. Zielinski6, Andrew
Alexander4,7,8, Nicholas Lange9,10, and Janet E. Lainhart4,8
1
Department of Psychology, Brigham Young University, Provo, Utah
2
Neuroscience Center, Brigham Young University, Provo, Utah
Author
3
Department of Psychiatry, University of Utah, Salt Lake City, Utah
4
Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, WI, USA
5
Department of Radiology, University of Utah, Salt Lake City, Utah
6
Department of Pediatrics and Neurology, School of Medicine, University of Utah, Salt Lake City,
Utah
7
Department of Medical Physics, University of Wisconsin, Madison, Wisconsin
8
Department of Psychiatry, University of Wisconsin, Madison, Wisconsin
9
Departments of Psychiatry and Biostatistics, Harvard University, Boston, Massachusetts
10
Neurostatistics Laboratory, McLean Hospital, Belmont, Massachusetts
Author
Abstract
Few studies have examined the visual-motor integration (VMI) abilities of individuals with
Autism Spectrum Disorder (ASD). An all-male sample consisting of 56 ASD participants (ages 3–
23) and 36 typically developing participants (TD) (ages 4–26) completed the Beery-Buktenica
Developmental Test of Visual-Motor Integration (Beery VMI) as part of a larger
neuropsychological battery. Participants were also administered standardized measures of
intellectual functioning and the Social Responsiveness Scale (SRS), which assesses autism and
autism-like traits. The ASD group performed significantly lower on the Beery VMI and on all IQ
measures compared to the TD group. VMI performance was significantly correlated with FSIQ,
PIQ, and VIQ in the TD group only. However, when FSIQ was taken into account, no significant
Beery VMI differences between groups were observed. Only one TD participant scored 1.5
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standard deviations below the Beery VMI normative sample mean, whereas 21% of the ASD
sample did. As expected, the ASD group was rated as having significantly higher levels of social
impairment on the SRS compared to the TD group across all major domains. However, level of
functioning on the SRS was not associated with Berry VMI performance. These findings
demonstrate that a substantial number of individuals with ASD experience difficulties compared
to TD in performing VMI-related tasks and that VMI is likely affected by general cognitive
ability.
The fact that lowered Beery VMI performance occurred only within a subset of individuals with
Correspondence should be addressed to: Erin D. Bigler, Ph.D., Department of Psychology & Neuroscience Center, 1001 SWKT,
Brigham Young University, Provo, UT 84602, Phone: (801) 422-4287, Fax: (801) 422-0602, [email protected].
Green et al. Page 2
ASD and did not correlate with SRS would indicate that visuomotor deficits are not a core feature
of ASD, even though they present at a higher rate of impairment than observed in TD participants.
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Children with ASD have increased difficulty with visual-motor integration (VMI; Dowd,
McGinley, Taffe & Rinehart, 2012), including problems with handwriting (Fuentes,
Mostofsky & Bastian, 2010; Johnson et al., 2013; Kushki, Chau Anagnostou, 2011).
Combined with motor skills, visual control over motor function is requisite in tasks such as
copying (Braddick & Atkinson, 2013). The degree to which visuomotor impairments in
ASD are influenced by motor impairments is not known, but various deficits in motor
functioning such as stereotyped/repetitive behaviors, abnormal gait and posture, diminished
fine motor coordination, catching and balance as well as deficits in imitative movements
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such as facial expressions or waving goodbye have been well documented (Ament et al.,
2014; Dawson & Watling, 2000; Duffield et al., 2013; Chukoskie, Townsend, &
Westerfield, 2013; Hardan, Kilpatrick, Keshavan, & Minshew, 2003; Hilton, Zhang,
Whilte, Klohr, & Constantino, 2012; McPhillips, Finlay, Bejerot, & Hanley, 2014;
Mostofsky et al., 2009; Soper, Wolfson, & Canavan, 2007). Indeed, Libertus and collegues
(2014) have shown that fine motor and grasping skills at 6-months in infants at high risk for
autism are below matched infants without a family history of ASD.
of motor actions and a key aspect of behavioral neuroscience” (p. 1313). These authors go
onto state that a general agreement has been established that VMI processes are
accomplished by a cortical network involving posterior parietal and premotor areas of the
frontal lobe – the traditional sensory-motor systems of the brain. Integrating a sensory input
with a behavioral output is a more complex neurological process than performing either on
its own and requires intra- as well as inter-hemispheric transfer of information. Additionally,
recent developments in the understanding of the cerebellum and its relation to coordinating
cognitive tasks and motor function suggest cerebellar involvement in VMI (O’Halloran,
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Kinsella, & Storey, 2012; Rogers et al., 2013). Moreover, producing a written product also
necessitates complex cognitive processes such as planning, goal orientation, and sustaining
attention throughout the task (Jones & Christensen, 1999). VMI thus requires higher-order
assimilation of multidimensional sensory input (visual), behavioral output (motor), and a
variety of cognitive processing demands that coordinate guided eye-hand movements
(Bertone, Mottron, Jelenic, & Faubert, 2005; Takarae, Minshew, Luna, & Sweeney, 2007).
The above evidence suggests that VMI deficits are expected in individuals with ASD given
the multiple, complex neurological processes that must be integrated in order to perform a
VMI task and the fact that deficits have been observed in various neurocognitive processes
in ASD, yet published VMI studies in ASD have resulted in inconsistent findings.
An early study by Fulkerson and Freeman (1980) demonstrated reduced Beery VMI
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In contrast, Minshew and colleagues (1997) did not observe VMI deficits in an ASD
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sample that included children and adults (IQ > 80). However, consistent with the previously
mentioned potential for motor deficits in individuals with ASD, these authors did find
significant differences in performances on Grooved Pegboard and Trail Making A but not
in Finger Tapping. A follow-up study of children with ASD (IQ >80) compared to adults
with ASD by Williams, Goldstein, and Minshew (2006) also did not find the visuospatial
domain to significantly exemplify the ASD neuropsychological profile for either children or
adults. They did however demonstrate that deficits in grip strength and the Wechsler
Intelligence Scale for Children-III Coding (Wechsler, 1991), but not Finger Tapping or
Grooved Pegboard (see Lezak et al., 2012), were associated with the neuropsychological
profile of adults and children with ASD.
Visuomotor integration is likely a composite brain function that requires visual attention,
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visual feature detection and identification, anticipatory judgment, motor planning and motor
execution. The small functional imaging literature to date has generally not observed deficits
in visual perception and feature detection in autism. For example, in four separate studies
using an embedded figure task (Ring et al., 1999; Lee et al., 2007; Manjaly et al., 2007;
Malisza et al., 2011), autism participants exhibited normal or increased activation of visual
cortex and lateral occipital regions, and relatively normal activation of visual attentional
regions along the medial intraparietal sulcus. More complex tasks requiring mental rotation
have shown decreased activation in autism in anterior cingulate cortex, frontal eye fields, and
caudate nuclei (Silk et al., 2006).
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Although both gross and fine motor skills may be impaired in autism (Fournier, Hass, Naik,
Lodha, & Cauraugh, 2010), functional imaging of motor responses has been mixed. A
button pressing task demonstrated increased cerebellar activation for continuous pressing,
but decreased cerebellar activation when buttons were pressed in response to attentional
cues (Allen & Courchesne 2003). In another study examining appositional finger tapping,
autism subjects showed reduced activation of the ipsilateral cerebellum but greater
activation in the supplementary motor area (Mostofsky et al., 2009). Furthermore, Nebel
and colleagues (2014) have shown differences in frontal connectivity involving the
precentral gyrus in individuals with autism.
One of the most commonly used standardized measures of VMI is the Beery-Buktenica
Developmental Test of Visual-Motor Integration (Beery, 1989; Beery, 1996; Beery &
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Beery, 2004), typically referred to as the Beery VMI (Lezak et al., 2012). Although the
Beery VMI has a rich tradition in assessing children and adults with various developmental
disorders and acquired brain injuries (Bloch et al., 2011; Sutton et al., 2011), remarkably
few studies have examined Beery VMI findings in ASD. The current study sought to add to
the VMI literature in ASD by examining Beery VMI performance in a large ASD group
whose ages ranged from childhood through young adulthood.
The specific aims of the study were to provide a descriptive analysis of the relation between
VMI performance, IQ, and ASD in an attempt to clarify previous discrepant findings.
Although cross-sectional, we felt that is was important to assess a broad age-range of ASD
participants and typically developed controls, since it is well established that VMI
performance is, in part age-dependent. Furthermore, since visuomotor abilities positively
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correlate with IQ measures (Bolen, 2003; Baron et al., 2014), the only restriction on IQ was
a lower limit, which ensured some ability to comply with the demands of
neuropsychological testing. To explore ASD severity issues, we examined Beery VMI
findings in relation to scores on the Social Responsiveness Scale (SRS; Constantino, 2002),
where SRS is used to specify severity of ASD symptoms (see Constantino et al., 2003).
Although not using the SRS, MacDonald, Lord and Ulrich (2014) have shown that ASD
children with reduced motor skill had greater social communicative skill deficits. Since
motor activities required to perform VMI tasks are but a subset of overall motor
functioning, we wanted to explore if relations were present between SRS findings and
Beery VMI findings. Furthermore, we hypothesized that individuals with ASD would
perform more poorly on a VMI task compared to individuals in the typical development
(TD) group and that individuals with more severe forms of ASD would perform more
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There are major participant ascertainment issues for both those assessed with ASD as well
as TD controls (see Howe, Yatchmink, Viscidi, & Morrow, 2014; Tager-Flusberg, (2004);
Idring et al., 2012). For the current study we elected to examine a broad age-range (3–26)
of only male participants recruited to be part of a longitudinal study focused on brain
maturation from early childhood to early adulthood (see Lange et al., 2014; Zielinski et al.,
2014; Travers et al.. 2014). The advantages of such a design is that it mimics clinical
reality for a large age-span of individuals with ASD but the disadvantages are that because
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of the greater likelihood for lower levels of intellectual ability in the ASD sample, it
becomes impossible to truly match on that dimension. For neurodevelopmental disorders
where intellectual ability may directly relate to the disorder, some argue that minimal to no
front- end control should be imposed on the TD sample (see Dennis et al., 2009).
Therefore, for the current study ASD participants with a much broader range of intellectual
ability were recruited than was the case for the TD sample. Accordingly, analyses initially
statistically controlled for age and intellectual differences between the ASD and TD
samples.
Method
Subjects and Assessment
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Participant groups—All participants were male, 3–26 years of age, thus precluding
analysis of potential sex differences. Fifty-six participants comprised the ASD group and
36 participants comprised the TD group.
Disorder Not Otherwise Specified. History, physical exam, fragile-X gene testing, and
karyotype performed on all subjects excluded medical and genetic causes of autism.
Measures
Visual-motor integration—VMI was measured using the Beery-Buktenica
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Developmental Test of Visual-Motor Integration (Beery VMI) (Beery, 1989; Beery, 1996;
Beery & Beery, 2004). Given the longitudinal nature of the parent project, the 3rd, 4th, and
5th editions of the Beery VMI were used during the various stages of data collection. The
stimuli in the various editions did not change. The Beery VMI is comprised of drawings of
geometric forms that increase in difficulty. The forms are copied with paper and pencil and
scored based on objective scoring criteria outlined in the test manuals according to how
accurately they were copied when compared to the original. The Beery VMI has been
demonstrated to have good reliability and validity as reported in the manual. Raw scores
were converted to age-appropriate standard scores based on the standardization sample
reported for the corresponding version of Beery VMI used. No significant group differences
were observed between the three versions for either the ASD or TD sample.
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IQ—Various measures of intellectual functioning were utilized given the age range of
participants in the study and because of changes in IQ test instruments over the 10 years of
recruiting subjects for the parent project. For the present investigation, FSIQ, VIQ, and PIQ
were measured using the Wechsler Intelligence Scale for Children–Third Edition (WISC–III;
Wechsler, 1991), Wechsler Intelligence Scale for Children–Fourth Edition (WISC–IV;
Wechsler, 2003), Wechsler Adult Intelligence Scale– Third Edition (WAIS-III; Wechsler,
1997), or Differential Ability Scales (DAS; Elliott, 1990). A VIQ minus PIQ comparison
was made between ASD and TD participants because some have suggested that IQ profile
analyses may be predictive of phenotypic differences in development (Margolis et al.,
2013). For example, lower VIQ may reflect greater language impairment, whereas lower
PIQ may reflect greater perceptual-motor impairment (Charman et al., 2011). It should be
noted that the most up-to-date, age-specific norms were used.
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Statistical Analyses
Independent samples t tests were conducted to derive descriptive statistics using group
means. Pearson correlations were computed along with analysis of covariance (ANCOVA)
to better understand the relation between Beery VMI performance and IQ variables. Pearson
correlations of Beery VMI and SRS were also computed.
conservatively defined as falling 1.5 standard deviations below the mean of a normative
sample (Lezak et al., 2012; Strauss et al., 2006). A frequency count was used to determine
how many participants in each group performed at or below these two levels of impairment
based on normative data derived from the Beery VMI manuals.
Results
Sample Characteristics
During sample characteristics analyses, pairwise deletion was used to maximize power in
the overall sample. No significant differences between ASD and TD groups were observed
in age or handedness. As expected, and indicated in Table 1, significant differences were
observed between groups in VMI, FSIQ, PIQ, and VIQ. No significant differences were
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Pearson correlations for VMI performance and IQ are summarized in Table 2 while Table 3
summarizes the frequencies of the IQ tests used in the study. All IQ variables in both ASD
and TD groups were correlated with one another as expected. Interestingly, 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, and the VIQ correlation trended toward significance (p = 0.06).
Twelve ASD participants but no TD participants exhibited FSIQ standard scores below 80.
Analyses were repeated (see Table 4) with these 12 ASD participants removed and included
only the participants with matching FSIQ scores within ±5 points (ASD n = 22, TD n = 22).
This FSIQ-restricted analysis resulted in a non-significant difference between groups on
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Beery VMI performance (VMI restricted FSIQ d = 0.54). The difference between the non-
restricted and restricted FSIQ effect sizes was 0.22. Additionally, no significant differences
were observed in the group of participants with restricted FSIQ scores in FSIQ, PIQ, VIQ,
and VIQ - PIQ whereas in the original, non-FSIQ-restricted analysis all IQ variables but the
VIQ - PIQ variable were significantly different.
Pearson correlations were then performed on the subset of 12ASD participants with FSIQ
below 80 and the subset of ASD participants with a FSIQ above 79 (see Figures 1 and 2 for
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broad graphic representation of all data and Figures 3 through 6 for specific representations
of age, Beery VMI, and FSIQ relationships). Interestingly, significant correlations were
observed between Beery VMI, FSIQ, and PIQ but not VIQ for those with a FSIQ below 80
but no significant correlations between Beery VMI and IQ variables were observed for those
with a FSIQ above 79 (see Table 5). Although the ages in the two groups were considerably
different, the age-specific normative data used in the study limit any potential age-related
confounds. To further test this, partial correlations controlling for age were undertaken, with
no meaningful changes observed. As indicated above, Figures 1–6 and Table 5 illustrate the
relationships between data. Of specific interest is that in the ASD group with FSIQ <80,
relatively strong correlations were observed in VMI performance such that the higher the
FSIQ the higher the VMI scores. In contrast, no such correlation was observed in the ASD
group with FSIQ >79 suggesting that FSIQ is a predictor of VMI performance only in the
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lower functioning group. Similarly, age in the ASD group with FSIQ <80 appears to be
associated with FSIQ such that the older the individual the higher the FSIQ score; where
this relationship was not observed in the ASD group with FSIQ > 79. It should be noted,
however, that the sample size in the FSIQ group was somewhat small and thus this trend
may be overturned if a larger sample was observed. Interestingly, it can be seen in Figures 1
and 2 that in the ASD group with FSIQ <80 there is no relationship between age and VMI
score whereas in the ASD group with FSIQ >79 there appears to be a trend such that the
older the individual was the lower they tended to score on the VMI tasks.
ANCOVA reported here excludes the interaction term. When FSIQ was statistically
controlled, the main effect for group Beery VMI performance was non-significant [F(1, 86)
= 2.34, p = .13, η 2 = .027].
p
Partial correlations between SRS domains and Beery VMI were performed. All SRS
domains were significantly correlated with each other in both groups with the exception of
the correlation between Awareness and Motivation in the TD group. None of the SRS
domains were significantly correlated with Beery VMI performance in either group (see
Table 7). However, correlations between Beery VMI and the Cognition and the
Discussion
The objectives of the current study were to examine and describe the visuomotor
performance in an all-male ASD sample with ages that ranged from childhood to early
adulthood and to better understand how these findings related to IQ and level of
functioning. At a group level, the ASD sample exhibited an overall attenuation in VMI
performance associated with reduced FSIQ, VIQ, and PIQ when compared to age-matched
TD controls. Our sample purposefully included a large range of intellectual abilities which
reflected the broad range of cognitive phenotypes observed in autism (Dissanayake et al.,
2009). A large effect size difference in Beery VMI performance suggested decreased VMI
in the ASD subjects; however, this appeared to be driven by a subgroup of ASD participants
with overall lower intellectual ability. Only one TD participant had a Beery VMI score < 1.5
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S.D. below the normative sample mean, whereas twelve (21%) individuals in the ASD
sample did. The differences in VMI performance appeared to be driven by a subset of ASD
participants with lower FSIQ such that when those with FSIQ scores < 80 were removed
from the analysis, the effect size was decreased by d = 0.22 and a significant difference
between ASD and TD Beery VMI performance was no longer observed. Additional support
for the notion that FSIQ contributes considerably to Beery VMI performance was seen
when significant differences were no longer observed in the entire sample after statistically
controlling for FSIQ. It should be noted that four different IQ measures were used in the
current study.
However, the DAS was the most frequently used IQ test administered in both groups (i.e.,
46 of 54 in the ASD group, and 29 of 35 in the TD group). Therefore, it is unlikely that
differences in visual-spatial emphasis between IQ measures considerably impacted the
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results.
The relation between IQ as a marker of general cognitive ability and Beery VMI
performance in ASD is complex. There is a substantial literature that shows ASD
individuals perform more poorly than controls on a wide variety of neuropsychological
measures (see Duffield et al., 2013; Geschwind, 2009; Gidley-Larson & Mostofsky, 2008;
Gilbert, Meuwese, Towgood, Frith, & Burgess, 2009; Keary et al., 2009; Minshew,
Goldstein, & Siegel, 1997; Polsek, Jagatic, Cepanec, Hof, & Simic, 2011; Takarae, Luna,
Sweeney, 2008; Southwick et al., 2011). All areas of cognitive functioning including VMI
derived metrics, are likely related, under the umbrella of what has been referred to
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as ”general intelligence” or “g” (Deary, 2012.). The design of this investigation was not
intended to explore how performance on VMI measures related to “g” other than reporting
VMI-IQ correlations. How motor abilities, and in particular VMI abilities may be separated
from general cognitive ability needs to be addressed in future studies. Since those with
lower intellectual ability performed worse on VMI measures whether their visuomotor
impairment was truly a reduction in perceptual-motor functioning or simply a byproduct of
lowered “g” could not be answered. How to separate VMI performance from some aspect of
“g” awaits further investigation. When the entirety of the current sample was considered,
FSIQ correlated positively with Beery VMI in both the ASD and TD groups yet was only
significant within the TD group. This suggests a divergence between ASD and TD in the
interrelation of cognitive and perceptual-motor abilities, likely reflecting a difference in
cerebral organization. However, when correlations between Beery VMI and IQ variables
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were performed in the subset of 12 ASD participants with FSIQ scores below 80, significant
correlations were observed between Beery VMI, FSIQ, and PIQ, while no significant
correlations were observed in Beery VMI and IQ variables in the remaining 42 ASD
participants who exhibited FSIQ scores at or above 80. This finding suggests a further
complexity in the phenotypic relationship in ASD individuals who exhibit lower levels of
overall cognitive abilities and those with higher levels of overall cognitive functioning.
Interestingly, within ASD participants age was related to VMI performance such that older
age was associated with lower VMI scores. Recently, we have shown that cortical volume
and thickness have different developmental trajectories between those with typical
development and ASD (Lange et al., 2014; Zielinski et al. 2014). Factors related to cellular
pruning and issues of neural connectivity are major discussion points involving the origins
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of ASD (see Thomas, Davis, Karmiloff-Smith, Knowland & Charman 2015). Indeed,
Courchesne, Campbell and Solso (2011) have shown some age-related accelerated brain
volume loss in autism after adolescence, but how such factors may influence VMI
performance has not been examined.
To further add to the complexity, the relation of Beery VMI performance to core ASD
symptoms based on SRS findings was not significant. That is, increased levels of social
impairment as reflected in SRS scores was not an indicator of worse Beery VMI scores. Of
course, VMI is but a subset of a larger repertoire of motor skills which may relate to severity
of social impairment (MacDonald, Lord, & Ulrich, 2014). For example, Reiersen,
Constantino and Todd (2008) found that the combination of ASD and motor problems
associated with comorbid attention-deficit hyperactivity disorder was associated with higher
SRS findings. The notion that motor impairment and by extension VMI may affect social
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functioning may be appreciated in Given the above discussion on intellectual findings with
Beery VMI yet no relation with level of social impairment, it appears that the lowered
visuomotor ability in ASD occurs primarily as a function of lower FSIQ below 80. Thus, the
lower Beery VMI scores observed when the entire ASD group was compared to the TD
participants, was driven by those with FSIQ <80. As with the study by Wilson and
colleagues (2014), once intellectual abilities are controlled in individuals characterized as
Reinvall et al. (2013) found deficits in ASD in Visuomotor Precision and Design Copying
on the Finnish version of the NEPSY-II with similar findings by Mayes and Calhoun in their
2003 and 2007 studies using the DTVMI. As shown in the present study, VMI performance
was attenuated at the group level. However, more than three-fourths of the ASD participants
in the current ASD cohort did not exhibit VMI performance deficits (i.e., performance
within 1.5 S.D. of the normative sample) which is consistent with Minshew and colleagues’
(1997) observations in their ASD sample.
Differences in network functioning and neural organization have been associated with ASD
(Nielsen et al., 2013; Zielinski et al., 2012) and specifically within motor circuits relevant to
motor integration (Müller, Kleinhans, Kemmotsu, Pierce & Courchesne, 2003; Turner,
Frost, Linsenbardt, McIlroy, Müller (2006); therefore, it was not unexpected that differences
in between group and within group patterns in IQ-Beery VMI performance would be
present. Future studies linking VMI performance with neuroimaging variables and network
analyses could potentially reveal other differences between those with ASD and TD. For
example, several studies have demonstrated neuroimaging abnormalities in ASD involving
the structural and functional relations of several brain regions likely critical for VMI
performance. These include the corpus callosum (Alexander et al., 2007; Prigge et al.,
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2013), frontal-parietal dysconnectivity (Just, Keller, Malave, Kana, & Varma, 2012),
atypical white matter microstructure development (Cheng et al., 2010; Wolff et al., 2012),
cerebellar connectivity (Mostofsky et al., 2009), medial prefrontal cortical abnormalities
(Gilbert, Meuwese, Towgood, Frith, & Burgess, 2009) and a distributed specificity of
cortical structural abnormalities including many of these implicated brain regions (Zielinski
et al., 2012; Zielinski et al., 2014). Investigating these regions with multimodal
neuroimaging methods may yield additional insights into why VMI ability appears to be
attenuated in at
least a subset of individuals with ASD and whether this may reflect differences in white
matter microstructure and/or abnormalities within motor and perceptual networks.
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There are limitations to the current investigation. For example, the sample did not include
females and so generalizability is limited. Additionally, although the role of visuomotor
impairment in lower functioning ASD as a function of FSIQ and social ratings was
explored in a subset of ASD participants, the relationship between these variables needs to
be more clearly understood. How to investigate the heterogeneity of cognitive phenotypes
in ASD and deal with intellectual disparities between TD and ASD samples represents a
major experimental design and statistical debate.
In summary, the findings of the current study suggest that VMI performance is attenuated
in ASD at the group level compared to controls. However, this group difference was driven
by a minority subset within the ASD group such that 79% of the participants with ASD had
Beery VMI performance that was comparable to controls. The current study also suggests
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that visuomotor impairment found in ASD is not associated with overall level of autism
symptom severity measured with the SRS. Given that some level of visuomotor impairment
was present in more than 20% of our sample, there is a need for further research to explore
the clinical significance and neurobiological underpinnings of visuomotor impairment in
ASD. Moreover, future research may clarify whether these measures can be useful in ASD
subset phenotyping and selection for therapeutic intervention.
References
Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR, … Lainhart JE. Diffusion tensor
imaging of the corpus callosum in autism. NeuroImage. 2007; 34:61–73. DOI: 10.1016/
j.neuroimage.2006.08.032 [PubMed: 17023185]
Allen G, Courchesne E. Differential effects of developmental cerebellar abnormality on cognitive and
Author
motor functions in the cerebellum: an fMRI study of autism. American Journal of Psychiatry.
2003; 160(2):262–273. [PubMed: 12562572]
Ament K, Mejia A, Buhlman R, Erklin S, Caffo B, Mostofsky S, Wodka E. Evidence for specificity
of motor impairments in catching and balance in children with autism. Journal of Autism and
Developmental Disorders. 2014 Electronic Publication.
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4.
Washington, DC: Author; 1994.
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5. Arlington,
VA: American Psychiatric Publishing; 2013.
Baron IS, Weiss BA, Baker R, Khoury A, Remsburg I, Thermolice JW, Litman FR, Ahronovich MD.
Subtle adverse effects of late preterm birth: a cautionary note. Neuropsychology. 28(1):11–18. DOI:
10.1037/neu0000018 [PubMed: 24040924]
Beery, KE. Developmental test of visual motor integration: Administration, scoring, and teaching
manual. 3. Cleveland, OH: Modern Curriculum Press; 1989. rev
Author
Beery, KE. The Beery-Buktenica developmental test of visual motor integration: Administration,
scoring, and teaching manual. 4. Cleveland, OH: Modern Curriculum Press; 1996.
Beery, KE.; Beery, NA. The Beery-Buktenica developmental test of visual motor integration:
Administration, scoring, and teaching manual. 5. Cleveland, OH: Modern Curriculum Press; 2004.
Bertone A, Mottron L, Jelenic P, Faubert J. Enhanced and diminished visuo-spatial information
processing in autism depends on stimulus complexity. Brain: A Journal of Neurology. 2005;
128(10):2430–2441. DOI: 10.1093/brain/awh561 [PubMed: 15958508]
Bigler ED, Tate DF, Neeley ES, Wolfson LJ, Miller MJ, Rice SA, Lainhart JE. Temporal lobe,
autism, and macrocephaly. American Journal of Neuroradiology. 2003; 24:2066–2076. [PubMed:
Author
14625235]
Bloch MH, Sukhodolsky DG, Dombrowski PA, Panza KE, Craiglow BG, Landeros-Weisenberger A,
… Schultz RT. Poor fine-motor and visuospatial skills predict persistence of pediatric-onset
obsessive-compulsive disorder into adulthood. Journal of Child Psychology and Psychiatry.
2011; 52(9):974–983. DOI: 10.1111/j.1469-7610.2010.02366.x [PubMed: 21244423]
Bolen LM. Constructing local age norms based on ability for the Bender-Gestalt test. Perceptual and
Motor Skills. 2003; 97(2):467–76. [PubMed: 14620234]
Braddick O, Atkinson J. Visual control of manual actions: Brain mechanisms in typical development
and developmental disorders. Developmental Medicine & Child Neurology. 2013; 55:13–18.
DOI: 10.1111/dmcn.12300 [PubMed: 24237273]
Charman T, Pickles A, Simonoff E, Chandler S, Loucas T, Baird G. IQ in children with autism
spectrum disorders: Data from the Special Needs and Autism Project (SNAP). Psychological
Medicine. 2011; 41(03):619–627. DOI: 10.1017/S0033291710000991 [PubMed: 21272389]
Cheng Y, Chou KH, Chen IY, Fan YT, Decety J, Lin CP. Atypical development of white matter
microstructure in adolescents with autism spectrum disorders. NeuroImage. 2010; 50(3):873–882.
Author
[PubMed: 20074650]
Constantino, J. The Social Responsiveness Scale. Los Angeles, CA: Western Psychological Services;
2002.
Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, … Reich W. Validation
of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale
with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders.
2003; 33(4):427–433. [PubMed: 12959421]
Chukoskie L, Townsend J, Westerfield M. Motor skill in autism spectrum disorders: A subcortical
view. International Review of Neurobiology. 2013; doi: 10.1016/B978-0-12-418700-9.00007-1
Courchesne E, Campbell K, Solso S. Brain growth across the life span in autism: age-specific changes
in anatomical pathology. Brain Research. 2011; 1380:138– 145. DOI: 10.1016/j.brainres.
2010.09.101 [PubMed: 20920490]
Dawson G, Watling R. Interventions to facilitate auditory, visual, and motor integration in autism: A
review of the evidence. Journal of Autism and Developmental Disorders. 2000; 30(5):415–421.
DOI: 10.1023/a:1005547422749 [PubMed: 11098877]
Author
underpin motor dysfunction in autism? A kinematic study of young children with autism. Journal
of Autism and Developmental Disorders. 2012; 42(8):1539–48. DOI: 10.1007/s10803-011-1385-8
[PubMed: 22105140]
Elliott, CD. Differential ability scales. San Antonio, TX: The Psychological Corporation; 1990.
Emck C, Bosscher R, Beek P, Doreleijers T. Gross motor performance and self-perceived motor
competence in children with emotional, behavioural, and pervasive developmental disorders: a
review. Developmental Medicine & Child Neurology. 2009 Jul; 51(7):501–17. DOI:
10.1111/j. 1469-8749.2009.03337.x [PubMed: 19538424]
Fournier KA, Hass CJ, Naik SK, Lodha N, Cauraugh JH. Motor coordination in autism spectrum
disorders: a synthesis and meta-analysis. Journal of Autism and Developmental Disorders. 2010;
Author
disorders. Journal of the American Academy of Child and Adolescent Psychiatry. 2014; 53(6): 698–
700. DOI: 10.1016/j.jaac.2014.04.003 [PubMed: 24839890]
Idring S, Rai D, Dal H, Dalman C, Sturm H, Zander E, … Magnusson C. Autism spectrum disorders in
the Stockholm youth cohort: Design, prevalence and validity. Public Library of Science One.
2012; doi: 10.1371/journal.pone.0041280
Johnson BP, Phillips JG, Papadopoulos N, Fielding J, Tonge B, Rinehart NJ. Understanding
macrographia in children with autism spectrum disorders. Research in Developmental Disabilities.
34(9):2917–2926. DOI: 10.1016/j.ridd.2013.06.003 [PubMed: 23816627]
Jones D, Christensen C. Relationship between automaticity in handwriting and students’ ability to
generate written text. Journal of Educational Psychology. 1999; 91(1):44–49.
Just MA, Keller TA, Malave VL, Kana RK, Varma S. Autism as a neural systems disorder: A theory
of frontal-posterior underconnectivity. Neuroscience and Biobehavioral Reviews. 2012;
36(4):1292– 1313. DOI: 10.1016/j.neubiorev.2012.02.007 [PubMed: 22353426]
Keary CJ, Minshew NJ, Bansal R, Goradia D, Fedorov S, Keshavan MS, Hardan AY. Corpus callosum
volume and neurocognition in autism. Journal of Autism and Developmental Disorders. 2009;
Author
Lee PS, Foss-Feig J, Henderson JG, Kenworthy LE, Gilotty L, Gaillard WD, Vaidya CJ. Atypical
neural substrates of Embedded Figures Task performance in children with autism spectrum
Author
and adolescents: review of associated health benefits. Sports Medicine. 2010; 40(12):1019–35.
DOI: 10.2165/11536850-000000000-00000 [PubMed: 21058749]
MacDonald M, Lord C, Ulrich DA. Motor skills and calibrated autism severity in young children
with autism spectrum disorder. Adapted Physical Activity Quarterly. 2014; 31(2):95–105. DOI:
10.1123/apaq.2013-0068 [PubMed: 24762385]
Malisza KL, Clancy C, Shiloff D, Foreman D, Holden J, Jones C, Paulson K, … Chudley AE.
Functional evaluation of hidden figures object analysis in children with autistic disorder. Journal
of Autism and Developmental Disorders. 2011; 41(1):13–22. [PubMed: 20411412]
Manjaly ZM, Bruning N, Neufang S, Stephan KE, Brieber S, Marshall JC, Kamp-Becker I,
Remshmidt H, Herpertz-Dahlmann B, Konrad K, Fink GR. Neurophysiological correlates of
relatively enhanced local visual search in autistic adolescents. Neuroimage. 2007; 35(1):283–291.
[PubMed: 17240169]
Margolis A, Bansal R, Hao X, Algermissen M, Erickson C, Klahr KW, Peterson BS. Using IQ
discrepancy scores to examine the neural correlates of specific cognitive abilities. The Journal of
Neuroscience. 2013; 33(35):14135–14145. [PubMed: 23986248]
Author
Mayes S, Calhoun S. Ability profiles in children with autism: Influence of age and IQ. Autism. 2003a;
7(1):65–80. [PubMed: 12638765]
Mayes S, Calhoun S. Learning, attention, writing, and processing speed in typical children and
children with ADHD, autism, anxiety, depression, and oppositional-defiant disorder. Child
Neuropsychology (Neuropsychology, Development and Cognition: Section C). 2007; 13(6):469–
493.
Meilleur AA, Berthiaume C, Bertone A, Mottron L. Autism-specific covariation in perceptual
performances: “g” or “p” factor? PLoS One. 2014 Aug 12.9(8):e103781. eCollection 2014. doi:
10.1371/journal.pone.0103781 [PubMed: 25117450]
McPhillips M, Finlay J, Bejerot S, Hanley M. Motor deficits in children with autism spectrum
disorder: A cross-syndrome study. Autism Research. 2014; 7(6):664–676. [PubMed: 25258309]
Minshew NJ, Goldstein G, Siegel DJ. Neuropsychologic functioning in autism: Profile of a
complex information processing disorder. Journal of the International Neuropsychological
Society. 1997; 3(4):303–316. [PubMed: 9260440]
Author
Minshew NJ, Hobson JA. Sensory sensitivities and performance on sensory perceptual tasks in high-
functioning individuals with autism. Journal of Autism and Developmental Disorders. 2008; 38(8):
1485–1498. DOI: 10.1007/s10803-007-0528-4 [PubMed: 18302014]
Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, Pekar JJ. Decreased connectivity
and cerebellar activity in autism during motor task performance. Brain. 2009; 132(9):2413–2425.
DOI: 10.1093/brain/awp088 [PubMed: 19389870]
Müller RA, Kleinhans N, Kemmotsu N, Pierce K, Courchesne E. Abnormal variability and distribution
of functional maps in autism: An FMRI study of visuomotor learning. American Journal of
Author
Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia.
1971; 9:97–113. DOI: 10.1016/0028-3932(71)90067-4 [PubMed: 5146491]
O’Riordan M, Passetti F. Discrimination in autism within different sensory modalities. Journal of
Autism and Developmental Disorders. 2006; 36(5):665–675. DOI: 10.1007/s10803-006-0106-1
[PubMed: 16639532]
Osterrieth PA. Le test de copie d’une figure complexe (The Complex Figure Copy Test). Archives de
Psychologie. 1944; 30:206–356.
Polsek D, Jagatic T, Cepanec M, Hof P, Simic G. Recent developments in neuropathology of autism
spectrum disorders. Translational Neuroscience. 2011; 2:256–264. [PubMed: 22180840]
Prigge MB, Lange N, Bigler ED, Merkley TL, Neeley ES, Abildskov TJ, … Lainhart JE. Corpus
Callosum Area in Children and Adults with Autism. Research in Autism Spectrum Disorders.
2013; 7(2):221–234. DOI: 10.1016/j.rasd.2012.09.007 [PubMed: 23130086]
Reiersen AM, Constantino JN, Todd RD. Co-occurrence of motor problems and autistic symptoms in
attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and
Author
Soper, HV.; Wolfson, S.; Canavan, F. Neuropsychology of autism spectrum disorders. In: Horton, A.;
Wedding, D., editors. The neuropsychology handbook. 3. New York, NY: Springer Publishing
Author
Takarae Y, Luna B, Minshew NJ, Sweeney JA. Patterns of visual sensory and sensorimotor
abnormalities in autism vary in relation to history of early language delay. Journal of the
International Neuropsychological Society. 2008; 14(6):980–989. DOI: 10.1017/
s1355617708081277 [PubMed: 18954478]
Takarae Y, Minshew NJ, Luna B, Sweeney JA. Atypical involvement of frontostriatal systems during
sensorimotor control in autism. Psychiatry Research: Neuroimaging. 2007; 156(2):117–127. DOI:
10.1016/j.pscychresns.2007.03.008 [PubMed: 17913474]
Thomas MS, Davis R, Karmiloff-Smith A, Knowland VC, Charman T. The over-prunning hypothesis
of autism. Developmental Science. 2015; In press. doi: 10.1111/desc.12303
Travers BG, Bigler ED, Tromp do PM, Adluru N, Froehlich AL, Ennis C, … Lainhart JE.
Longitudinal processing speed impairments in males with autism and the effects of white matter
microstructure. Neuropsychologia. 53:137–145. Epub 2013 Nov 21. DOI:
10.1016/j.neuropsychologia.
2013.11.008 [PubMed: 24269298]
Tseng M, Cermak S. The influence of ergonomic factors and perceptual-motor abilities on handwriting
Author
Wilson CE, Happé F, Wheelwright SJ, Ecker C, Lombardo MV, Johnston P, … Murphy DG. The
neuropsychology of male adults with high-functioning autism or asperger syndrome. Autism
Research. 2014; 7(5):568–81. DOI: 10.1002/aur.1394 [PubMed: 24903974]
Wolff JJ, Gu H, Gerig G, Elison JT, Styner M, Gouttard S, … Piven J. Differences in White Matter
Fiber Tract Development Present From 6 to 24 Months in Infants With Autism. The American
Journal of Psychiatry. 2012; 169(6):589–600. DOI: 10.1176/appi.ajp.2011.11091447 [PubMed:
22362397]
Wolynski B, Schott BH, Kanowski M, Hoffmann MB. Visuo-motor integration in humans: Cortical
patterns of response lateralisation and functional connectivity. Neuropsychologia. 2009; 47(5):
1313–1322. DOI: 10.1016/j.neuropsychologia.2009.01.027 [PubMed: 19428395]
Zielinski BA, Anderson JS, Froehlich AL, Prigge MB, Nielsen JA, Cooperrider J, … Lainhart JE.
scMRI reveals large-scale brain network abnormalities in autism. PLoS One. 2012; 7(11)doi:
Author
10.1371/journal.pone.0049172
Zielinski BA, Prigge MB, Nielsen JA, Froehlich AL, Abildskov TJ, Anderson JS, … Lainhart JE.
Longitudinal changes in cortical thickness in autism and typical development. Brain. 2014;
137:1799–1812. Epub 2014 Apr 22. DOI: 10.1093/brain/awu083 [PubMed: 24755274]
Zwaigenbaum L, Bryson SE, Szatmari P, Brian J, Smith IM, Roberts W, Vaillancourt T, Roncadin
C. Sex differences in children with autism spectrum disorder identified within a high-risk
infant cohort. The Journal of Autism and Developmental Disorders. 2012; 42(12):2585–2596.
DOI: 10.1007/s10803-012-1515-y [PubMed: 22453928]
Author
Author
Author
Figure 1.
Scatterplot Matrix of ASD Participants with FSIQ Standard Score below 80
Author
Author
Figure 2.
Scatterplot Matrix of ASD Participants with FSIQ Standard Score above 79
Author
Author
Figure 3.
Scatterplot of ASD Participants with FSIQ Standard Score below 80 by Age
Author
Author
Figure 4.
Scatterplot of ASD Participants with FSIQ Standard Score above 79 by Age
Author
Author
Figure 5.
Scatterplot of ASD Participants with FSIQ Standard Score below 80 by Beery VMI
Standard Score
Author
Author
Figure 6.
Scatterplot of ASD Participants with FSIQ Standard Score above 79 by Beery VMI Standard
Score
Author
Author
Green et
ASD TD
Age (years) 56 10.57 4.76 3–24 36 11.90 5.10 4–26 1.28 .20 0.27
Handedness 56 60.18 57.72 −100–100 36 70.00 39.60 −80–100 1.07 .29 0.20
Beery VMI 56 92.61 17.85 60–141 36 105.17 14.95 75–143 3.59* .001 0.76
Child Neuropsychol. Author manuscript; available in PMC 2017 January
FSIQ 54 94.20 20.81 49–137 35 116.69 14.95 85–153 5.53* .001 1.24
PIQ 53 97.77 20.19 50–133 35 115.03 15.08 88–152 4.58* .001 0.97
VIQ 48 93.73 23.20 51–145 35 114.74 15.50 81–151 4.94* .001 1.06
VIQ-PIQ 48 −6.25 20.05 −52–26 35 −0.29 11.20 −29–20 1.72 .90 0.37
ASD = Autism Spectrum Disorder. TD = Typically Developing. Handedness = Edinburgh Handedness Inventory based on a scale from −100 (left-handed) to 100 (right-handed). FSIQ = Full Scale IQ. PIQ
= Performance IQ. VIQ = Verbal IQ.
*
p < 0.001.
Page
Table
Correlation Matrix of Beery VMI and IQ Using Listwise Deletion
Green et
ASD (n = 48) TD (n = 35)
Beery VMI = Beery-Buktenica Developmental Test of Visual-Motor Integration. ASD = Autism Spectrum Disorder. TD = Typically Developing.
*
p < 0.003.
Page
Green et al. Page 27
Table 3
Frequencies of IQ Tests
Author
ASD TD
Test n n
DAS 46 29
WISC-III 2 1
WISC-IV 1 0
WAIS-III 5 5
ASD = Autism Spectrum Disorder. TD = Typically Developing. DAS = Differential Ability Scales. WISC-III = Wechsler Intelligence Scale for
Children–Third Edition. WISC-IV = Wechsler Intelligence Scale for Children–Fourth Edition. WAIS-III = Wechsler Adult Intelligence Scale–
Third Edition. WASI = Wechsler Abbreviated Scale of Intelligence.
Author
Author
Author
Green et
ASD (n = 22) TD (n = 22)
Age (years) 11.55 4.52 6–23 12.42 4.63 4–26 0.63 0.53 0.19
Handedness 65.65 52.94 −100–100 74.13 33.67 −60–100 0.63 0.53 0.19
Beery VMI 95.18 14.20 62–121 102.59 13.34 75–129 1.78 0.08 0.54
Child Neuropsychol. Author manuscript; available in PMC 2017 January
FSIQ 110.23 16.00 80–137 110.72 13.77 85–142 0.11 0.91 0.03
PIQ 105.64 21.77 81–133 107.45 12.93 88–146 0.52 0.61 0.10
VIQ 111.86 16.03 65–145 109.50 14.22 81–133 0.34 0.74 0.25
VIQ-PIQ −6.23 20.99 −51–22 −2.04 12.13 −29–18 0.81 0.42 0.24
ASD = Autism Spectrum Disorder. TD = Typically Developing. Handedness = Edinburgh Handedness Inventory based on a scale from −100 (left-handed) to 100 (right-handed). FSIQ = Full Scale IQ. PIQ
= Performance IQ. VIQ = Verbal IQ.
Page
Table
Correlation Matrix of Beery VMI and IQ for ASD Participants with FSIQ < 80 and >79
Green et
ASD: FSIQ < 80 (n = 12) ASD: FSIQ > 79 (n = 41)
Beery VMI = Beery-Buktenica Developmental Test of Visual-Motor Integration. ASD = Autism Spectrum Disorder.
*
p <.05,
**
p = <.01.
Page
Table
SRS Characteristics
Green et
ASD (n = 50) TD (n = 30)
Cognition 79.54 13.52 43–103 41.30 5.13 36–54 17.97* 0.001 3.74
Child Neuropsychol. Author manuscript; available in PMC 2017 January
Communication 80.14 10.93 53–107 41.40 4.84 36–56 21.76* 0.001 4.58
Motivation 73.26 17.24 42–106 43.43 6.98 37–63 10.84* 0.001 2.27
Mannerisms 84.68 13.37 55–117 42.53 3.64 40–51 21.03* 0.001 4.30
Total 83.20 12.91 51–109 40.97 4.81 34–53 20.85* 0.001 4.33
Page
Table
Pearson Correlation Matrix of Beery VMI and SRS Domains
Green et
ASD (n = 55) TD (n = 33)
Variable Awa Cog Com Mot Man Tot Awa Cog Com Mot Man Tot
VMI .10 .00 .17 .18 .06 .13 .22 .33 .36 .00 −.02 .27
Awa – .67** .76** .50** .62** .80** – .45* .43* .35 .45* .67**
Child Neuropsychol. Author manuscript; available in PMC 2017 January
VMI = Beery-Buktenica Developmental Test of Visual-Motor Integration. ASD = Autism Spectrum Disorder. TD = Typically Developing. Awa = Aware, Cog = Cognition, Com = Communication, Mot =
Motivation, Man = Mannerisms, Tot = Total.
*
p <.05,
**
p <.01.
Page
Table
Comparisons of High and Low ASD Scorers on SRS Total and SRS Cognition
Green et
High SRS Total (n = 29) Low SRS Total (n = 22)
Mean SD Mean SD t p d
96.05 15.37 91.69 20.15 0.84 0.4 0.24
Mean SD Mean SD t p d
95.32 16.4 91.89 19.96 0.67 0.51 0.19
Page