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Neuroscience 307 (2015) 273–280

DIFFERENCES IN THE USE OF VISION AND PROPRIOCEPTION FOR


POSTURAL CONTROL IN AUTISM SPECTRUM DISORDER
S. L. MORRIS, * C. J. FOSTER R. PARSONS, development of social interaction and communication
M. FALKMER, T. FALKMER AND S. M. ROSALIE with restricted or repetitive interests and behaviors (Lai
Faculty of Health Sciences, Curtin University, GPO et al., 2014). ASD is commonly used as an comprehen-
Box U1987, Perth, Western Australia 6845, Australia sive umbrella term and includes among others the diag-
noses of Autistic disorder, Asperger syndrome (AS)
(American Psychiatric Association, 2000). The term
Abstract—Background: People with autism spectrum disor- high-functioning autism (HFA), usually refers to individu-
ders (ASDs) also have poorer fundamental motor skills. The
als within the spectrum with an IQ score within or above
development of postural control underlies both social and
motor skills. All three elements are facilitated by the active
the normative average range (Volker, 2012). ASD (previ-
use of visual information. This study compares how adults ously known as pervasive developmental disorder) is one
with ASD and typically developed adults (TDAs) respond of the most common childhood disorders with 1 in 68 chil-
to a postural illusion induced using neck vibration. Adults dren being diagnosed (Lord and Bishop, 2015). Despite
with ASD unlike the TDA, were not expected to correct the being predominantly a social disorder, at least 79% of
illusion using vision. Methods: The study used intermittent individuals with ASD are reported as having difficulties
(15off, 5on) posterior neck vibration during 200 s of quiet with fundamental motor skills (Ghaziuddin and Butler,
stance to induce a postural illusion. In TDAs and only in 1998; Pan et al., 2009; Fournier et al., 2010a). Funda-
the absence of vision this protocol induces a forward body mental motor skills are important in the development of
lean. Participants (12 ASD, 20 TDA) undertook four condi-
skills in play, interaction with others, communication and
tions combining vibration and visual occlusion. Results:
As predicted, TDA were only affected by the postural illusion
language (Gernsbacher et al., 2008; Blaesi and Wilson,
when vision was occluded (vibration condition: vision 2010; Clearfield, 2011). Therefore, the motor difficulty in
occluded (n = 1) p = 0.0001; vision available (n = 3) those with ASD may contribute to the significant social dif-
p > 0.2466). Adults with ASD were affected by the postural ficulty associated with this disorder (Bhat et al., 2011).
illusion regardless of the availability of vision (all conditions The ability to control posture is critical to the typical
p < 0.0007). Conclusions: Our findings indicated the adults development of fundamental motor skills (Miyahara,
with ASD did not use visual information to control standing 2013; Travers et al., 2013). If individuals with ASD expe-
posture. In light of existing evidence that vision-for- rience difficulties with postural control at key time points
perception is processed typically in ASD, our findings sup- during their development of fundamental motor skills,
port a specific deficit in vision-for-action. These findings
such difficulties may be a causative factor in the atypical
may explain why individuals with ASD experience difficul-
ties with both social and motor skills since both require
development of motor and social skills characteristic of
vision-for-action. Further research needs to investigate the ASD (Bhat et al., 2011). Studies have shown that children
division of these visual learning pathways in order to pro- and adolescents with ASD demonstrate differences in
vide more specific intervention opportunities in ASD. postural control with increased anteroposterior and medi-
Ó 2015 IBRO. Published by Elsevier Ltd. All rights reserved. olateral sway when standing still compared to their typi-
cally developing peers (Molloy et al., 2003; Fournier
et al., 2010b; Memari et al., 2013). Evidence suggests
that underdevelopment of postural control in the setting
Key words: postural control, autism spectrum disorder, of ASD continues into adulthood (Kohen-Raz et al.,
vision-for-action, vibration, sensory integration.
1992; Minshew et al., 2004; Travers et al., 2013); how-
ever, the mechanisms for the differences are not known.
Visual information usually dominates other forms of
INTRODUCTION sensory information in the control of posture (Peterka
Autism spectrum disorders (ASDs) are and Benolken, 1995; Nolan et al., 2005). Differences in
neurodevelopmental disorders present from early visual processing have been commonly reported in ASD
childhood which are characterized by atypical (Simmons, 2009). Studies comparing the effect of a visual
illusion of motion on the posture of young children with
and without ASD have shown that both younger children
*Corresponding author. Tel: +61-0892669226.
(Gepner et al., 1995) and older children (Gepner and
E-mail address: s.morris@curtin.edu.au (S. L. Morris).
Abbreviations: AS, Asperger syndrome; ASDs, autism spectrum Mestre, 2002) with ASD change their posture less in
disorders; HFA, high-functioning autism; TDAs, typically developed response to the perception of motion than typically
adults.

http://dx.doi.org/10.1016/j.neuroscience.2015.08.040
0306-4522/Ó 2015 IBRO. Published by Elsevier Ltd. All rights reserved.

273
274 S. L. Morris et al. / Neuroscience 307 (2015) 273–280

developing children. These findings suggest that children have focused on children and adolescents. Findings of
with ASD are less dependent on the perception of motion studies including adults with ASD are mixed. Evidence
to maintain a balanced posture. Interestingly, in the same both supports a deficit (Kohen-Raz et al., 1992;
study children with AS as opposed to children with autistic Minshew et al., 2004) and no deficit (Greffou et al.,
disorder were shown to be more reactive to the perception 2012; Travers et al., 2013) in the use of visual information
of motion than both children with autistic disorder and typ- for postural control in adults with ASD. Thus, it is unclear
ically developing children (Gepner and Mestre, 2002). whether the difficulties that children and adolescents with
This raises the possibility that children with the AS are ASD experience in postural control persist into adulthood,
more, rather than less, dependent on the perception of which has implications with respect to learning and perfor-
motion to maintain a balanced posture than typically mance of vocational skills.
developing children. Conversely, spatial and motion inte- Bove and colleagues (2009) recently pioneered a
gration tests that have compared the abilities of children method of examining the integration of visual and
with autism and typically developing children to verbally somatosensory information for posture control in quiet
respond to the perception of motion have shown no differ- standing. This method uses sequential periods of vibra-
ences (Del Viva et al., 2006). tion of posterior neck muscles interspersed with
Although visual information is the dominant source of vibration-free periods to produce a transient propriocep-
sensory information used in the control of posture, it is not tive illusion of movement of the head which is interrupted
the only source of information. Information from the as a backward lean of the truck due to constant vestibular
somatosensory and vestibular systems also contributes input (Bove et al., 2009). This illusion results in a ‘‘correc-
to the maintenance of an optimal body position (Peterka tive” transient forward movement of the center of pressure
and Benolken, 1995; Nolan et al., 2005). Thus, either pri- coinciding with periods of vibration. Posture is typically
mary deficits in somatosensory and/or vestibular informa- normalized once the illusion is removed. When partici-
tion (Weimer, 2001), or an inability to integrate visual pants were instructed to close their eyes across succes-
information with somatosensory and vestibular informa- sive periods of vibration, thereby denying themselves a
tion (Baranek, 2002; Cascio et al., 2012) could lead to visual reference for the position of the head, the forward
the difficulties in motor control experienced by individuals movement of the center of pressure was not only
with ASD. Evidence for both primary somatosensory and/ observed to increase but participants were unable to cor-
or vestibular deficits and deficits in integration is inconsis- rect their posture in the absence of vibration until vision
tent. It has been reported; however, that children with was restored (Bove et al., 2009). This result highlights
ASD have difficulties in standing on one leg with their the importance of visual information for typically develop-
vision occluded and this has been attributed to a proprio- ing individuals in setting the postural reference point and
ceptive deficit that caused an over-reliance on visual infor- returning to a neutral position after posture is perturbed
mation to balance (Weimer, 2001). It has also been (Bove et al., 2009). The method used by Bove et al.
reported that adolescents with ASD do not have a primary (2009) required the participants to open or close their
proprioceptive deficit (Fuentes et al., 2011) and in fact are eyes in response to a verbal command, which meant that
proprioceptive learners (Haswell et al., 2009). Con- the availability of visual information was controlled by the
versely, children with ASD have been shown to experi- participant and not the experimenter. This limitation can
ence greater postural sway than typically developing be overcome by using liquid crystal spectacles that allow
children when balance is perturbed by standing on an the precise control of the availability of vision across time
unstable surface (i.e., foam) both with and without the (Rosalie and Müller, 2013). These spectacles are particu-
availability of visual information. This greater sway has larly useful for controlling vision in individuals with ASD
been attributed to impaired integration of information from whose difficulties with communication and social interac-
the visual, somatosensory and vestibular systems (Molloy tion may make it problematic to follow a sequence of com-
et al., 2003). Though informative, in the foregoing study mands to open and close their eyes. By combining neck
postural sway was examined under conditions where muscle vibration with visual occlusion, it is therefore pos-
visual control of posture was directly inhibited through sible to have tight experimental control of both the
blindfolding the participants; whereas, somatosensory somatosensory and visual information available for postu-
control of posture was inhibited through manipulation of ral control in individuals with ASD.
the environment conditions. That is, balance was per- The purpose of this study was thus to determine
turbed via changes in the surface (platform versus foam). whether adults with ASD use and integrate visual and
To our knowledge researchers are yet to examine differ- somatosensory information to control posture during
ences in the integration of visual and somatosensory quiet standing differently from TDAs. Based on existing
information for the control of posture between individuals evidence (Weimer, 2001; Molloy et al., 2003; Fuentes
with and without ASD in a single study that directly and et al., 2011) it was hypothesized that: (i) proprioception
independently inhibits sensory input from both the visual is processed similarly in typically developed adult (TDA)
and somatosensory systems. Thus, evidence regarding and ASD such that when vision is occluded, both groups
differences between individuals with and without ASD in will respond to the postural illusion by leaning forward; (ii)
the integration of visual and somatosensory information vision is processed differently in TDA and ASD such that
for the control of posture on a stable surface is incom- TDA, but not adults with ASD, will normalize their posture
plete. Furthermore, previous studies of differences in pos- when vision is restored during the postural illusion; and
tural control between individuals with and without ASD (iii) integration of vision and proprioception is different in
S. L. Morris et al. / Neuroscience 307 (2015) 273–280 275

adults with ASD and TDA so the groups would respond plane data (i.e., forward and backward movement on the
differently in conditions when the availability of vision plate) was retained for further analysis (CFP). Leaning
was varied between periods of postural illusion and no forward would be indicated by an increase in the CFP
postural illusion compared to when the availability of and leaning backward would be indicated by a reduction
vision was constant across periods of postural illusion in CFP. The postural illusion was induced using a vibrator
and no postural illusion. (VB 115, Techno Concept, Cereste, France) fixed bilater-
ally to the dorsal neck muscles at C7 using an elastic
strap around the neck and shoulders in the same manner
EXPERIMENTAL PROCEDURES as Bove and colleagues (2009). Vision was manipulated
Participants using liquid crystal spectacles that could be changed from
translucent to opaque (PLATO, Model P1, Translucent
Twenty TDAs 19–35 years old (Mean 23.4 ± SD 5.1) and Technologies Inc., Toronto, ON, Canada) under the com-
twelve adults with a diagnosis of HFA or Asperger mand of the experimenter. Each of these systems was
syndrome (ASD) from 19–40 (Age: Mean 23.6 ± SD controlled via a custom-made computer program, which
7.9) with a Body Mass Index (BMI) between 20 and 42 allowed the accurate control of each of the trial conditions.
participated in this experimental study. Groups were The reasoning behind retaining only the sagittal plane
balanced for sex with two females in each group. The data for analysis was because the bilateral neck vibration
participants were recruited through advertising on social illusion targeted movement in the anterior posterior direc-
media. Inclusion criteria were that the participant was tion (i.e. forward lean). Postural lean in medio-lateral
aged over 18 years of age and had been diagnosed with direction due to bilateral neck vibration was not expected
HFA or AS. Exclusion criteria were an inability to and has not been reported.
communicate effectively, inability to understand
instructions, the presence of co-morbid neurological or
movement disorders other than developmental Procedure
coordination disorder or epilepsy, any therapeutic The visual occlusion and vibration apparatus was placed
intervention received within the last 2 weeks and on the participant and a period of familiarization
inability to stand with vision occluded for 2 min safely. provided. On commencing the experiment the
Formal diagnosis of ASD was ascertained from the participant was asked to stand (wearing shoes) with
participant as diagnosis by authorized and qualified both feet in the middle of the force plate in a
professionals in independent clinics, hence a re- comfortable standing position with arms hanging by the
evaluation of their diagnosis including excessive re- side of the body and foot position was marked by
testing in order to participate in the current study was drawing an outline of the entire foot on paper over the
considered as unethical (Falkmer et al., 2013). Partici- plate. A researcher was close by for support. Between
pants with ASD reported their diagnostic process as pedi- conditions the participant stepped off the plate. With
atrician only (3), pediatrician and clinical psychologist (3), each new condition the participant was directed to stand
clinical psychologist only (4) and three did not indicate. in the same position and as still as possible. Four trials
Four participants with ASD also reported comorbidities representing a combination of visual occlusion/vibration
which included dysgraphia (1), epilepsy (2), ADD or experimental conditions were undertaken in a
ADHD (2), restless leg syndrome and/or anxiety (1). Five randomized order. Each trial was 200 s long and
patients reported taking medication which included Ritalin consisted of 10 cycles of; 15 s of no vibration
(2), Sifrol (1), anti-anxiety medication not specified (1), (henceforth known as rest periods) followed by; 5 s of
epilepsy medication not specified (1) and/or medication vibration ((15 + 5)  10 = 200 s). The four visual
not specified (2). Each participant provided informed writ- occlusion conditions were: (1) vision available during
ten consent prior to participation. This study was com- both the rest and vibration periods (VAVA), (2) vision
pleted according to the guidelines of the Helsinki available during rest periods but vision occluded during
declaration and was approved by the Curtin University vibration (VAVO), (3) vision occluded in the rest period
Human Research Ethics Committee (Approval No: and available during vibration (VOVA) and (4) vision
PT250/2013). occluded throughout the full sequence (VOVO) of which
an example of a TDA trial is presented in Fig. 1. After
Experimental design and equipment each trial the participants dismounted the force plate
and a five-minute rest period was provided between trials.
The procedure used for this study followed closely the
methodology developed by Bove and colleagues (2009).
Statistical analysis
The participants’ task was to stand on a portable force
platform (AMTI, Watertown, MA, USA) at a set distance Data for two TD participants in the VAVA conditions were
of 1.5 m from a white wall and look at a black horizontal not collected due to hardware issues. All other data were
line running at a height of 165 cm from the floor. The complete. For each trial the mean CFP position was
sagittal plane of the participant was aligned with the y axis calculated for each of the 20 periods in the 200 s of
of the force plate. Force and moment data from the force standing. CFP is reported in millimeters. This created 10
plate were collected at 1000 Hz and decimated to a fre- CFP values representing the rest periods and 10 CFP
quency of 100 Hz. Post data collection the trajectory of values representing the vibration periods. CFP for each
the center of foot pressure was calculated and the sagittal of the 19 subsequent periods was normalized to the
276 S. L. Morris et al. / Neuroscience 307 (2015) 273–280

Fig. 1. Trace of a CFP in the sagittal plane from the typically developed adult during the VO-VO trial where vision was occluded during the entire
trial and vibration occurred in 5-s cycles preceded by 15 s rest over the 200 s of the trial.

CFP position inPthe first rest period of each trial significant interaction was observed between group and
((CFP = CFP ( CFP0–15)/15)) (now called CFP visual occlusion condition F(3, 2355) = 10.11,
position) so that each participant started each trial with p < 0.0001. Post-hoc pairwise comparisons revealed
a position of zero. A positive CFP then indicates a that the adults with ASD group had a significantly
leaning position forward from baseline and a negative greater change in CFP position compared to TDA when
CFP indicates a leaning position backward from baseline. vision was either fully or partially available (VAVA,
A linear mixed model with participant as a random t = 2.64, p < 0.01; VAVO t = 2.99, p < 0.01; VOVA
effect (intercept) was used to investigate the effect of t = 2.69 p < 0.01); whereas, there was no difference in
visual occlusion condition (VOVO, VAVA, VOVA, CFP position between groups when vision was occluded
VAVO), vibration (rest period [15 s]) or vibration period (VOVO, t = 0.63, p = 0.527) (Table 1) (Fig. 2).
[5 s]) and group (ASD or TDA) on CFP position. A
second linear mixed model analysis was undertaken
using the standard deviation of CFP position (CFP-SD) Mean CFP position – within-group differences in the
within each period (n = 10 rest and n = 10 vibration for use of vision
each participant) to determine if the variance within Within-group pairwise comparisons revealed no
periods was affected by the above-listed factors. For difference in the CFP position of adults with ASD
both analyses interactions at all levels (visual occlusion regardless of when vision was occluded across periods
condition*group, visual occlusion condition*vibration, of postural illusion (VAVA vs. VAVO, t = 1.74,
vibration group*visual occlusion condition) were p = 0.0822; VAVA vs. VOVA, t = 1.47, p = 0.1417;
investigated and significant interactions retained in the VAVO vs. VOVA, t = 0.27, p = 0.7881; VAVA vs.
analysis. Within-group differences were examined post VOVO, t = 0.39, p = 0.6973; VAVO vs. VOVO,
hoc using least squares means of fixed effects and least t = 2.13, p = 0.0335; VOVA vs. VOVO, t = 1.86,
squares mean differences of fixed effects. The SAS p = 0.0632) (Table 1) (Fig. 2). In contrast, a significant
version 9.2 software was used to perform these difference was observed in the CFP position of TDA
analyses (SAS Institute Inc., Cary, NC, USA 2008). when comparing if vision was available across periods
Following convention, a p-value <.05 was taken to of postural illusion (VAVA vs. VOVO, t = 6.12,
indicate a statistically significant difference in all tests. A p < 0.0001; VAVO vs. VOVO, t = 5.25, p < 0.0001;
more stringent p value of .01 was used for the pairwise
comparisons to reduce the chance of a type 1 error.
Table 1. Means and standard deviations in the displacement of the
Centre of Foot Pressure in the sagittal plane (CFP) for adults with
RESULTS autism spectrum (ASD) vs. typically developing (TDA) adults in each of
the four trial conditions (vibration period only): no occlusion (VAVA); no
Mean CFP position – between-group differences occlusion no vibration/occlusion during vibration (VAVO); occlusion no
vibration/no occlusion during vibration (VOVA); and occlusion (VOVO)
No statistically significant difference was observed
between TDA and adults with ASD in age (ASD 23.58 Condition TDA CFP (mm) ASD CFP (mm)
± 7.9 years; TDA 23.35 ± 5.05 years) or mass (ASD Mean SD Mean SD
92.62 ± 23.4 kg; TDA 79.58 ± 12.71 kg). Significant
VAVA 3.2 7.8 8.7 11.3
effects for CFP were observed for group (TDA vs.
VAVO 4.3 11.5 10.2 9.3
ASD), F(1, 2355) = 5.50, p < 0.05, postural illusion
VOVA 3.6 9.9 9.4 11.3
condition F(1, 2355) = 232.26, p < 0.0001, and visual VOVO 7.1 14.6 7.9 8.8
occlusion condition F(3, 2355) = 4.22, p < 0.01, and a
S. L. Morris et al. / Neuroscience 307 (2015) 273–280 277

Rest periods Vibration periods group or between the two groups (p > 0.01) during the
14 (15 seconds) (5 seconds) vibration period.
CFP position (mm)

12 During the rest periods TDA demonstrated


10
8 significantly smaller CFP-STD in the VAVA vs. VOVO
6 (t = 3.53, p = 0.0004) indicating that the loss of vision
4 in the rest period increased the within-period variability.
2
0
During the rest periods TDA also demonstrated
-2 significantly smaller CFP-STD in the VAVA vs. VAVO
-4
VAVA VAVO VOVA VOVO VAVA VAVO VOVA VOVO (t = 2.8, p = 0.0052).
Significant within-group differences for adults with
Fig. 2. Mean and 95% confidence interval of the average position of ASD were demonstrated only in the rest periods (not
the center of foot pressure (CFP) during no vibration periods (n = 9) vibration periods). For the ASD group there was a
and vibration periods (n = 10) relative to the initial CFP position at
the start of each trial (n = 1) for participants with ASD (circles)
significantly greater CFP-STD in the VAVA vs. VOVO
(n = 12) and TDA (triangles) (n = 20) across the four trial types conditions (t = 2.99, p = 0.0029) and the VOVA vs.
(vision available throughout trial VAVA; vision occluded throughout VOVO (t = 3.41, p = 0.0007) conditions.
trial VOVO; vision available only during the pre-vibration periods and
vision occluded during the vibration periods VAVO; and vision
occluded during the pre-vibration periods and vision available during
the vibration periods VOVA). DISCUSSION
The purpose of this experiment was to determine whether
VOVA vs. VOVO, t = 5.26, p < 0.0001), but not when adults with ASD use and integrate visual and
comparing when vision was available across periods of somatosensory information to control CFP in the same
postural illusion (VAVA vs. VAVO, t = 1.05, p = 0.2932; way as typically developing individuals. This was
VAVA vs. VOVA condition, t = 1.68, p = 0.0932; VAVO achieved by comparing the CFP responses of adults
vs. VOVA, t = 0.65, p = 0.5153) (Table 1) (Fig. 2). with ASD and TDAs to the illusion of neck extension
(due to posterior neck muscle vibration) when vision
was available and when vision was occluded. The
Mean CFP position – within group differences in the results showed that adults with ASD leaned forward in
effect of the postural illusion response to the postural illusion regardless of whether
Post-hoc pairwise comparisons revealed that TDA were vision was available or occluded. In contrast, TDAs only
only affected by the postural illusion when vision was leaned forward when vision was occluded. Therefore,
occluded throughout the postural illusion (VAVA TDA were able to use visual information to override
t = 0.32, p = 0.7496; VAVO t = 0.85, p = 0.3977; incongruous information provided by the somatosensory
VOVA t = 1.16, p = 0.2466, VOVO t = 3.37, system during the postural illusion and reset their
p < 0.0001); whereas the adults with ASD group were standing posture. Surprisingly, adults with ASD relied
significantly affected regardless of the availability of entirely on somatosensory information to determine
vision (VAVA t = 3.60, p < 0.0001; VAVO t = 4.44, posture and ignored the visual information even when
p < 0.0001; VOVA t = 4.31, p < 0.0001, VOVO the somatosensory information was clearly anomalous.
t = 3.41, p = 0.0007) (Table 1) (Fig. 2). This result suggests that adults with ASD do not use
vision to control posture but rather appear to be
‘‘selectively blind” to the optic flow information specifying
CFP-STD – between-group differences
self-motion. When adults with ASD were presented with
A significant 3-way interaction for visual occlusion aberrant somatosensory information which induced
condition*group*vibration indicated breaking the analysis them to shift their CFP position forward they were
into parts for ease of interpretation. Data were split into unable to use visual information to detect and correct
rest periods and vibration periods. their self-motion.
These results of the vibration study are consistent with
our first hypothesis that proprioception is processed
CFP-STD – within group differences in the use of
similarly in TDA and ASD since both typical adults and
vision
adults with ASD responded to the postural illusion by
Significant group*visual occlusion condition interactions leaning forward. They also support our second
were evident during both the vibration (F(3,1222) hypothesis, that vision is processed differently in ASD
p < 0.0001) and rest (F(3,1222) p < 0.0001) periods for because only the TDA group, not adults with ASD, used
CFP-SD. During vibration, the TDA demonstrated visual information to normalize their postural position.
significantly smaller CFP-STD in the conditions in VAVA Our findings support the hypothesis that TDAs
vs. VOVO (t = 5.66, p < 0.0001) and VAVA vs. VAVO preferentially use optic flow information regarding the
(t = 4.79, p < 0.0001); VOVA vs. VAVO (t = 4. 97, motion of the head over somatosensory information
p < 0.0001) and VOVA vs. VOVO (t = 5.87, regarding the position of the head in controlling posture
p 6 0.0001) indicating that the loss of vision during the (Bove et al., 2009). This is consistent with direct percep-
vibration period increased variability during that period tion theory which predicts that the perception of egocen-
(underlines indicate the vibration period). No significant tric motion, or self-motion with respect to the
difference was evident for the CFD-STD for the ASD environment, is facilitated by the visual perception of
278 S. L. Morris et al. / Neuroscience 307 (2015) 273–280

global changes in optic flow information (Gibson, 1966). In than visual input (Forssberg and Nashner, 1982;
contrast, we found that adults with ASD did not use optic Rodrigues et al., 2010). Therefore over reliance on
flow information to control postural position. Instead, somatosensory information for motor control is likely to
when we perturbed the posture of adults with ASD with result in greater postural error which will be most apparent
the postural illusion we found that they were not only visu- in tasks requiring greater postural accuracy. Individuals
ally blind to the fact that they were not leaning backward, with ASD exhibit difficulties in controlling posture during
but are also visually blind to the fact that they were lean- tasks that require accurate postural control such as sport-
ing forward. Thus, in adults with ASD, somatosensory ing activities (Forssberg and Nashner, 1982; Rodrigues
information regarding the position of the head clearly et al., 2010).
dominates over optic flow information regarding the Our findings have important clinical implications for
motion of the head. Analysis of the within-period variation the diagnosis and treatment of ASD. As well as
(CFP-STD) supported the finding for CFP mean position providing insight into factors that may contribute to the
in that larger variation was observed in the TDA during motor difficulties individuals with ASD experience, the
visual occlusion compared with vision available – sug- study also suggests possible avenues for developing
gesting a stabilization of posture. This stabilization was motor interventions. Visual processing is often referred
not evidence in the adults with ASD where variation was to as an area of strengths in individuals with ASD
similar with and without vision. In fact the adults with (Dakin and Frith, 2005; Mottron et al., 2006). As a conse-
ASD in our study may have experienced visual informa- quence, visual strategies have been successfully used to
tion as disturbing to postural control when vibration was promote skill acquisition in individuals with ASD (Tissot
absent. When standing without vibration, unlike the TDA and Evans, 2003). One of the visual techniques, video
the adults with ASD demonstrated a larger variation in modeling has been increasingly popular and recognized
postural position when vision was available compared as a promising strategy and has been used to teach indi-
with when vision was occluded. Kohen-Raz et al. (1992) viduals with ASD a range of skills including daily living
described a similar ‘‘paradoxical postural stress skills, social and academic skills and in order to enhance
response” in their study of autistic children and adoles- independence in individuals with ASD (Charlop-Christy
cents where they observed an unexpected better stability et al., 2000; Shipley-Benamou et al., 2002; D’Ateno
with vision occluded and standing on foam. If we consider et al., 2003; Ayres and Langone, 2005; Buggey, 2005;
people with ASD to be proprioceptive rather than visual Bellini and Akullian, 2007; Delano, 2007; McCoy and
learners as suggested by Haswell and colleagues Hermansen, 2007; Sansosti and Powell-Smith, 2008).
(2009), then it may not be surprising that they perform Although these techniques show promising results in
better on foam and without vision. The findings of our many areas of skill development for individuals with
study certainly suggest that the difficulties that children ASD (McCoy and Hermansen, 2007), the results from
with ASD have in using optic flow information to perceive the current study indicate that a more somatosensory
motion (Gepner et al., 1995; Gepner and Mestre, 2002) approach to intervention may need to be investigated in
extend into adulthood. regard to motor control. Finally, our study adds to current
Researchers have suggested that the motor deficits research which has shown that static visual information (i.
experienced by individuals with ASD are due to difficulty e., a visual cue that is not in motion) can guide an action
integrating visual and somatosensory information response (in this case postural adjustment) (Rosalie and
(Molloy et al., 2003). Our results are not consistent with Müller, 2013) which is consistent with a Gibsonian
this position which is a statement of our fourth hypothesis. account of visual perception (Gibson, 1979). Moreover,
Instead we found no difference in the postural response of our findings suggest that individuals with ASD process
adults with ASD across the three experimental conditions visual information for the control of action atypically. The
involving some visual occlusion (VOVA, VAVO, VOVO). dorsal visual stream is thought to dominate in the pro-
Therefore, the ability to integrate visual information with cessing of visual information for the control of action
somatosensory either before or during the postural illu- (vision-for-action) (Goodale et al., 1991). Previous
sion did not affect postural position compared to the situ- research has reported that individuals with ASD process
ation when only somatosensory information was visual information for perception typically (Del Viva
provided. As far as we understand this is the first study et al., 2006). The processing of visual information for per-
that attempted to test the integration vs. visual deficit ception (vision-for-perception) is thought to be a function
hypothesis directly. This finding reinforces our contention of the ventral visual stream (Goodale et al., 1991). In light
that the adults with ASD in our study selectively ignored of these findings it appears that individuals with ASD
the visual set point and used somatosensory information experience deficits in vision-for-action (dorsal stream)
to control posture regardless of whether the somatosen- but not vision-for-perception (ventral stream). It would
sory information was accurate or inaccurate. Further be valuable; however, to examine differences in the con-
research is necessary to confirm these findings including tribution of the dorsal and ventral visual streams to visual
exploring specific visual deficits in ASD in the absence of perception between individuals with ASD and typically
the requirement for integration. developing individuals in a single experiment.
Our findings may explain many of the motor deficits This study represents a small sample of adults with
experienced by individuals with ASD such as motor ASD and in order to reduce the burden on participants,
incoordination (Fournier et al., 2010b; Gowen and diagnosis was not re-evaluated during the study. The
Hamilton, 2013). Somatosensory input is less accurate differences between groups in outcomes in this study
S. L. Morris et al. / Neuroscience 307 (2015) 273–280 279

should be interpreted as the differences between adults Bhat AN, Landa RJ, Galloway JC (2011) Current perspectives on
with HFA and adults without HFA as the findings may motor functioning in infants, children, and adults with autism
spectrum disorders. Phys Ther 91:1116–1129.
not extend to all sub types of ASD. In addition the
Blaesi S, Wilson M (2010) The mirror reflects both ways: action
magnitudes of the difference in CFP movement between influences perception of others. Brain Cogn 72:306–309.
groups were small. It should be noted that this small Bove M, Fenoggio C, Tacchino A, Pelosin E, Schieppati M (2009)
average difference between groups represented the Interaction between vision and neck proprioception in the control
average across 10 successive periods of vibration. Bove of stance. Neuroscience 164:1601–1608.
and colleagues demonstrated that the size of response Buggey T (2005) Video self-modeling applications with students with
in all conditions of vibration increased across trials autism spectrum disorder in a small private school setting. Focus
Autism Other Dev Disab 20:52–63.
(Bove et al., 2009) so the average likely underestimates Cascio CJ, Foss-Feig JH, Burnette CP, Heacock JL, Cosby AA
the cumulative effect of vibration. The CFP position (2012) The rubber hand illusion in children with autism spectrum
reflects the control of the center of mass in the sagittal disorders: delayed influence of combined tactile and visual input
plane. The magnitude of the difference in CFP position on proprioception. Autism 16:406–419.
between groups in the vision available condition is the Charlop-Christy M, Le L, Freeman K (2000) A comparison of video
average error in estimation of center of mass position of modeling with in vivo modeling for teaching children with autism. J
Autism Dev Disord 30:537–552.
the participants with ASD. Small differences in estimating
Clearfield MW (2011) Learning to walk changes infants’ social
average postural position can translate to large differ- interactions. Infant Behav Dev 34:15–25.
ences in body movement during activity since postural Dakin S, Frith U (2005) Vagaries of visual perception in autism.
control underlies the development of motor skill. Neuron 48:497–507.
D’Ateno P, Mangiapanello K, Taylor BA (2003) Using video modeling
to teach complex play sequences to a preschooler with autism. J
CONCLUSION Positive Behav Interv 5:5–11.
Del Viva MM, Igliozzi R, Tancredi R, Brizzolara D (2006) Spatial and
This experimental study sought to extend the motion integration in children with autism. Vision Res
understanding our how individuals with ASD use and 46:1242–1252.
integrate visual and somatosensory information to Delano ME (2007) Video modeling interventions for individuals with
control posture during quiet standing. Through the use autism. Remedial Special Educ 28:33–42.
of visual occlusion in combination with a postural illusion Falkmer T, Anderson K, Falkmer M, Horlin C (2013) Diagnostic
procedures in autism spectrum disorders: a systematic literature
it was determined that adults with ASD rely more on
review. Eur Child Adolesc Psychiatry 22:329–340.
somatosensory information to control posture than TDAs Forssberg H, Nashner LM (1982) Ontogenetic development of
and are visually blind to changes in posture during quiet postural control in man: adaptation to altered support and visual
standing. These findings have furthered the conditions during stance. J Neurosci 2:545–552.
understanding of visual perception in the setting of ASD Fournier KA, Hass CJ, Naik SK, Lodha N, Cauraugh JH (2010a)
and have important implications in diagnosis and Motor coordination in autism spectrum disorders: a synthesis and
treatment. meta-analysis. J Autism Dev Disord 40:1227–1240.
Fournier KA, Kimberg CI, Radonovich KJ, Tillman MD, Chow JW,
Lewis MH, Bodfish JW, Hass CJ (2010b) Decreased static and
FINANCIAL DISCLOSURES dynamic postural control in children with autism spectrum
disorders. Gait Posture 32:6–9.
This study was funded by Curtin University. All authors Fuentes C, Mostofsky S, Bastian A (2011) No proprioceptive deficits
except Christopher Foster are employees of Curtin in autism despite movement-related sensory and execution
impairments. J Autism Dev Disord 41:1352–1361.
University. Christopher Foster was a student at Curtin
Gepner B, Mestre DR (2002) Brief report: postural reactivity to fast
University. The authors have nothing else to declare in visual motion differentiates autistic from children with Asperger
terms of conflict of interest or financial interests. syndrome. J Autism Dev Disord 32:231–238.
Gepner B, Mestre D, Masson G, de Schonen S (1995) Postural
Acknowledgments—The authors would like to acknowledge the effects of motion in young autistic children. NeuroReport
inputs of Paul Davey in developing the software and integrating 6:1211–1214.
Gernsbacher MA, Sauer EA, Geye HM, Schweigert EK, Hill
the hardware for the study. We would also like to acknowledge
Goldsmith H (2008) Infant and toddler oral- and manual-motor
the Curtin Autism Research Group for continued inputs and
skills predict later speech fluency in autism. J Child Psychol
support of our research.
Psychiatry 49:43–50.
Ghaziuddin M, Butler E (1998) Clumsiness in autism and Asperger
syndrome: a further report. J Intellect Disab Res 42(Pt 1):43–48.
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(Accepted 18 August 2015)


(Available online 24 August 2015)

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