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Research in Autism Spectrum Disorders


Journal homepage: http://ees.elsevier.com/RASD/default.asp

Internal model deficits impair joint action in children and adolescents


with autism spectrum disorders
Astrid M.B. Stoit a, Hein T. van Schie b,*, Madelon Riem c,1, Ruud G.J. Meulenbroek c,
Roger D. Newman-Norlund c,2, Dorine I.E. Slaats-Willemse d,
Harold Bekkering c, Jan K. Buitelaar d,e
a
Karakter Child and Adolescent Psychiatry, P.O. Box 40244, 8004 DE, Zwolle, The Netherlands
b
Radboud University Nijmegen, Behavioural Science Institute, P.O. Box 9104, 6500 HE, Nijmegen, The Netherlands
c
Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, P.O. Box 9104, 6500 HE, Nijmegen, The Netherlands
d
Karakter Child and Adolescent Psychiatry, University Centre, Reinier Postlaan 12, 6525 GC, Nijmegen, The Netherlands
e
Radboud University Nijmegen Medical Centre, Donders Institute for Brain, Cognition and Behaviour, P.O. Box 9101, 6500 HB, Nijmegen, The Netherlands

A R T I C L E I N F O A B S T R A C T

Article history: Qualitative differences in social interaction and communication are diagnostic hallmarks
Received 18 November 2010 in autism spectrum disorders (ASD). The present study investigated the hypothesis that
Received in revised form 1 December 2010 impaired social interaction in ASD reflects a deficit to internally model the behavior of a co-
Accepted 25 February 2011 actor. Children and adolescents with ASD and matched controls performed a computerized
bar-balancing task in a solo condition (S), and together with another individual in two joint
Keywords: action conditions (J2 and J4) in which they used either two or four hands to control the bar
Autism lift. Consistent with predictions derived from the ‘internal modelling hypothesis’, results
Joint action
from the J2 task indicated that ASD dyads were impaired in predicting the occurrence of
Internal models
their partner’s response and failed to coordinate their actions in time. Furthermore, results
Agency
Self-other differentiation
from the J4 task showed that ASD participants used an adaptive strategy to disambiguate
their responses from their partner’s by regulating opposite sides of the bar during lifting.
These findings provide empirical support of theories positing the existence of an internal
modelling deficit in ASD. In addition, our findings suggest that impaired social reciprocal
behavior and joint cooperative play exhibited by individuals with ASD may reflect
behavioral adaptations to evade conflicting or ambiguous information in social settings.
ß 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Social interactions make up an important part of our daily activities. We anticipate the behavior of others when driving in
traffic, safely exchanging mugs filled with hot liquid, or deciding whether someone is in the mood for a lengthy conversation.
Sensitivity to social cues and our ability to understand and adapt to the behavior of others appears to come naturally and
intuitively. However, for individuals with ASD this is not the case. Already from a young age on, children with ASD manifest a
lack of social reciprocity that may be characterized by deficiencies in joint attention (Osterling, Dawson, & Munson, 2002),
difficulty with imitation and self-other discrimination (Rogers & Pennington, 1991), and impairments in false-belief tests
requiring Theory of Mind (Baron-Cohen, Leslie, & Frith, 1985; Peterson, Wellman, & Liu, 2005).

* Corresponding author. Tel.: +31 024 36 12575; fax: +31 024 36 12677.
E-mail address: h.vanschie@psych.ru.nl (H.T. van Schie).
1
Present address: The Institute of Education and Child Studies, University of Leiden, Wassenaarseweg 52, 2333 AK, Leiden, The Netherlands.
2
Present address: University of South Carolina, Department of Exercise Science, Discovery 1, 202D, 915 Greene Street, Columbia, SC 29201, USA.

1750-9467/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.rasd.2011.02.016

Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders (2011), doi:10.1016/
j.rasd.2011.02.016
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2 A.M.B. Stoit et al. / Research in Autism Spectrum Disorders xxx (2011) xxx–xxx

The cognitive deficits associated with ASD are diverse and range from social to executive, motor and attentional
disabilities (Sigman, Spence, & Wang, 2006; van Engeland & Buitelaar, 2008; Williams, Whiten, Suddendorf, & Perrett, 2001).
Accordingly, a long list of hypotheses, theoretical explanations, and functional mechanisms has been proposed to explain
different aspects of the autistic spectrum disorders. One particular mechanism that is believed to be elementary in reciprocal
interactions with others is the availability of an internal (action) model that allows individuals to simulate the actions of
others in their own sensory-motor systems in order to support understanding and predicting others’ actions over time
(Blakemore & Decety, 2001). Although internal models may indeed be important for representing the behavior of others,
their primary function is to support the efficiency of individual motor planning and the execution of actions. For action
production two basic categories of internal models have been proposed: forward and inverse models (review in Kawato
(1999)). Forward models predict the sensory consequences of upcoming actions in advance of their execution (e.g. the
anticipation of touch when grasping a cup) to which actual action effects may be compared. Inverse models, on the other
hand, allow sensory information of objects (e.g. the spatial position of a cup) to pre-activate motor commands that might be
appropriate for these objects (e.g. grasping). Both types of internal models are considered important for increasing the speed
of movement execution and the ability to correct errors fluently in response to movement errors detected at sensory and
motor levels.
The idea that ASD children may suffer from an impairment to monitor and anticipate the consequences of their action
intentions is not new (Pacherie, 1997; Russell, 1996; Russell & Jarrold, 1998, 1999). In support of this idea, Schmitz,
Martineau, Barthelemy, and Assaiante (2003) and Martineau, Schmitz, Assaiante, Blanc, and Barthelemy (2004) recently
found that autistic children, but not control children, failed to anticipate self-initiated carrying load and that their postural
adjustments for carrying primarily reflected feedback information instead of feedforward prediction (however, for
conflicting evidence see Larson, Bastian, Donchin, Shadmehr, and Mostofsky (2008)). As indicated above, in addition to
supporting individual action production, internal models may be very useful for monitoring and anticipating the actions of
others, i.e. they may support action understanding and allow efficient social interactions, as recent studies from Cattaneo
et al. (2007) and Fabbri-Destro, Cattaneo, Boria, and Rizzolatti (2009) seem to suggest. The study by Cattaneo et al. (2007)
revealed deficits in anticipatory action chaining in autistic children, reflected by delayed activation of mouth opening
muscles during the reaching and grasping of food for eating. Importantly, a similar delay in anticipatory motor activation was
found during the observation of other’s grasping and eating actions which suggests that the limits in temporal integration
that are found during action performance may directly influence the representation of others’ actions during observation.
Although the above studies provide an interesting and convincing case for defective internal modelling in ASD, several other
recent studies have failed to find convincing support for this hypothesis (e.g. see Blakemore et al., 2006; David et al., 2008;
Sebanz, Knoblich, Stumpf, & Prinz, 2005) raising some doubts about the extent and nature of the internal modelling
impairment in children with ASD.
Important to this discussion is that the exact neural mechanisms that support internal models for action are still under
investigation and different types of inverse and forward processing have been proposed (see Gazzola & Keysers, 2009; Miall,
2003). One particularly interesting neurophysiological mechanism that has been hypothesized to support both inverse and
forward models during action execution and the observation of actions is the mirror neuron system (MNS). More specifically,
Iacoboni (2005a) proposed that recurrent connections from frontal and parietal parts of the MNS, respectively, the inferior
frontal gyrus and the inferior parietal lobule, provide a forward model for action by converting plans for motor output back
into a visual prediction in the superior temporal sulcus. This visual prediction can then be compared with the actual visual
consequences of the movement once it is generated. At the same time, the MNS is widely known for its inverse modelling
properties, that is, the tendency to activate motor representations during the observation of goal-directed actions via a
process that is referred to as motor resonance (e.g. Rizzolatti, Fogassi, & Gallese, 2001).
Consistent with the suggestion that a defective MNS may underlie ASD impairments in action performance, action
observation and social interaction, several studies have reported deficiencies in MNS operation in autistic individuals.
Hadjikhani, Joseph, Snyder, and Tager-Flusberg (2006) found smaller volumes of grey matter in MNS areas in a group of high-
functioning individuals diagnosed with ASD and the amount of cortical volume negatively related with the severity of social
problems. Dapretto et al. (2006) found that control subjects, but not individuals with ASD showed mirror neuron activation
in the right inferior frontal gyrus when asked to imitate and observe facial expressions and that the severity of social
problems in this group was related to the level of activation in the inferior frontal gyrus. EEG evidence for a deficit in motor
resonance was reported by Oberman et al. (2005) who found that high-functioning individuals with ASD do not show the
typical mu-suppression during observation of hand movements. Nishitani, Avikainen, and Hari (2004) furthermore showed
that when persons with Asperger’s syndrome imitate lip movements, the temporal progression of MEG activation in MNS
areas is delayed as compared to healthy subjects, which may well reflect a deficit in functional connectivity between the
brain regions forming the MNS (cf. Villalobos, Mizuno, Dahl, Kemmotsu, & Muller, 2005).3
Interestingly, recent fMRI studies suggest that, in addition to its well known role in imitation (Iacoboni, 2005b), the MNS
does contribute to cooperation between individuals, e.g. in conditions where complementary actions are required such as

3
Note however that, notwithstanding the positive evidence for MNS dysfunction in ASD, there is still considerable controversy and doubt about the
validity of the theoretical proposal that dysfunction of the human MNS lies at the basis of ASD (Iacoboni & Dapretto, 2006), and whether it provides a unitary
explanation for all ASD characteristics (see Dinstein, Thomas, Behrmann, and Heeger (2008) for an excellent discussion).

Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders (2011), doi:10.1016/
j.rasd.2011.02.016
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when handing over objects (Newman-Norlund, van Schie, van Zuijlen, & Bekkering, 2007) or coordinating a joint lifting action
(Newman-Norlund, Bosga, Meulenbroek, & Bekkering, 2008). Although the precise contribution of MNS to joint action is still
under debate (see e.g. Kokal, Gazzola, & Keysers, 2009), it is certain that coordinating actions with a co-actor puts a large strain
on internal modelling. As such one should expect clear deficits in joint action performance in individuals with ASD.
In addition to supporting efficient execution, observation, and coordination of actions between individuals, internal
models may contribute to the experience of agency, i.e. ‘the sense that I am the one who is causing or generating an action’
(Gallagher, 2000). The feeling of agency may occur when the sensory consequences of an initiated action match its
anticipated effects as predicted by an internal forward model (Decety & Sommerville, 2003; Jeannerod & Pacherie, 2004).
Vice versa, agency will attenuate if the (spatial or temporal) congruency between an intended action and its anticipated
effect is disturbed. As a consequence, action effects may no longer be perceived to be self-generated but instead attributed to
an external cause, e.g. another person. Recent fMRI studies investigating the neural basis of agency have consistently found
activation in Theory of Mind (ToM) areas such as the region around the temporal parietal junction (TPJ) and medial
prefrontal cortex (MPFC) (Decety & Grèzes, 2006; Farrer & Frith, 2002; Farrer et al., 2003; Leube et al., 2003; Spengler, von
Cramon, & Brass, 2009). Spengler et al. (2009) for instance observed a positive correlation between BOLD signal in the TPJ and
the discrepancy between predicted and actual sensory effects. In the same study, BOLD signal was enhanced in the MPFC to
the extent to which participants attributed the cause of a sensory event to another person instead of to oneself. Conversely,
activation in both the insula and the precuneus has been found to increase as a function of self-relevance and the experience
of agency (e.g. Farrer & Frith, 2002; Farrer et al., 2003; Ruby & Decety, 2001; Vogeley et al., 2001). Together these findings
suggest that the attribution of agency to others instead of to oneself is associated with activation in areas supporting ToM,
whereas attributing agency to oneself as opposed to others is associated with enhanced activation in a network of areas
associated with first person experience and self-reflection (Modinos, Ormel, & Aleman, 2009; Uddin, Iacoboni, Lange, &
Keenan, 2007).
In the current study we investigated impairments in internal modelling in ASD by comparing a group of children and
adolescents with autism spectrum disorder with a group of matched normal controls on two joint action tasks that posed
different challenges in terms of action coordination and agency uncertainty (cf. Newman-Norlund et al., 2008). We used a
slightly adapted version of the paradigm employed by Newman-Norlund et al. (2008) who investigated the neural basis of
joint action in healthy individuals using a virtual joint bar-balancing task. In this study, three conditions, one solo, and two
joint action conditions, were administered. In the solo condition (S) each subject, on his or her own, used a pair of joysticks to
lift a virtual horizontal bar with their left and right hands while balancing a freely rolling virtual ball. The joint conditions
involved a nonisomorphic (J2) and an isomorphic condition (J4) in which participants lifted up the bar as a dyad either with
each subject holding one end of the bar (nonisomorphic) or having control over both sides of the bar, during lifting
(isomorphic) (see Fig. 1). Both joint action conditions, in comparison with the solo performance condition, were found to
generate stronger activation in the MNS (inferior frontal gyrus and inferior parietal lobe), a finding which is compatible with
increased use of internal models during joint task performance. Furthermore, both joint action conditions were accompanied
by enhanced activation in the area encompassing the TPJ and the precuneus, suggesting increased differentiation in agency
attributed to self (precuneus) and other (TPJ).
Based on the hypothesis that children and adolescents with ASD have problems in predicting the actions of others, we
expected them to show impairments in anticipating the movement onset of their co-actor, as reflected in inter-individual
reaction time differences in the J2 condition that placed stringent demands on the temporal coupling of actions. That is,
because in the J2 condition, subjects can only control their side of the bar, successful lifting requires that subjects take into
account the lift onset time of their partner and wait for each other in order not to drop the ball. As a consequence we
predicted that the ASD group, in addition to imperfections in lift onset synchronization, would show larger bar-rotation
[()TD$FIG]
errors in this condition and would drop the ball at a considerable lower height (earlier interval) during the lift.

Fig. 1. Experimental setup and bar-balancing screen. (A) The left panel shows a schematic of the experimental setup. Both subjects could control the lift and
orientation of a virtual bar on the screen, either alone (solo condition), together using all four hands (Joint 4 condition) or together using one hand each (Joint
2 condition). Subject 1, located on the left, controlled joysticks L1 and R1 with his respective left and right hand, and subject 2, located on the right,
controlled joysticks L2 and R2. (B) The right panel represents the bar-balancing task. The green virtual bar is located at the bottom of the screen (no joystick
displacement) with the pink ball on top. The target area is located at the top of the screen and is demarcated by the two horizontal lines. The subjects’ task
was to lift the bar into the target area and hold it there for 2 s without dropping the ball.

Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders (2011), doi:10.1016/
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In the J4 condition, where each individual was in control of both sides of the bar, we expected that the ASD group would
show problems with self-other differentiation and agency detection because in this condition bar movements reflect the
combined input from both participants. More specifically we predicted that ASD dyads would be inclined to reduce agency
ambiguity by dividing control over the two respective ends of the bar, as this would enhance the contingency between self-
initiated actions and their perceptual consequences. More specifically we anticipated that ASD participants would show a
preference for controlling the ipsilateral side of the stimulus bar (i.e. the side located proximal to their own body), in
accordance with joint action studies that have shown a preference for responding to stimuli with an ipsilateral direction or
position (Hommel, Colzato, & van den Wildenberg, 2009; Sebanz, Knoblich, & Prinz, 2003). A consequence of this strategy
would furthermore be that ASD dyads would not make optimal use of all four hands for stabilizing the bar, and as a
consequence would have more difficulty keeping the bar in the target area and completing the task successfully.

2. Methods

2.1. Participants

A total of 56 children and adolescents (14 females) between the age of 8 and 18 years (M = 11.6; SD = 3.2) with normal or
corrected to normal vision participated in the experiment. Twenty-eight children diagnosed with ASD were recruited from an
institution for child and adolescent psychiatry (Karakter, Zwolle, The Netherlands). A control group, matched on age, consisting
of 28 typically developing children was recruited from local primary and secondary schools in the vicinity of the institute. Dyads
were formed by pairing participants of the same group with a partner of approximately the same age (age difference maximally
one year). A t-test indicated no significant differences between the age of patient and control groups, t(54) = .46, ns.
Clinical ASD diagnosis according to DSM-IV criteria (American Psychiatric Association, 1994) was made by two experienced
professionals (a child psychiatrist and clinical psychologist) on the basis of a developmental interview, parent interview and
child psychiatric observation, and confirmed by the Autism Diagnostic Interview-Revised (ADI-R; Rutter, Le Couteur, & Lord,
2003) and/or Autism Diagnostic Observation Schedule-Generic (ADOS-G; Lord, Rutter, Dilavore, & Riso, 2001). Inter-rater
reliability was satisfactory, both for the ADOS (k = .78) as for the ADI-R (k = .73). Diagnoses included the broad autism spectrum.
Seven participants from the ASD group also had an ADHD diagnosis and were receiving medication to improve the symptoms
associated with ADHD. For one of the included participants it was not possible to obtain reliable ADI-R or ADOS-G data, due to
incompliance of the parents, but the experienced professionals had no doubts about the ASD diagnosis.
Exclusion criteria for both groups were IQ < 70 and neurological abnormality (epilepsy, motor disability). Intelligence of
the participants in the ASD group was tested psychometrically using subtests from the Dutch version of WISC-III (up to 16
years of age) or the Dutch version of the WAIS (16 years of age and older). We used 4 subtests (similarities, arithmetic,
picture-completion, and block design) for which it was shown to provide a reliable estimate of full scale IQ (Kaufman,
Kaufman, Balgopal, & McLean, 1996). A t-test indicated a statistical difference in IQ between the control group (M = 111.9,
SD = 11.0) and the ASD group (M = 100.3, SD = 12.6), t(54) = 3.61, p < .01.
Parents or primary caregivers of the control group were asked to complete a questionnaire inquiring about possible
behavioral problems (CBCL: the Dutch version of the Parent form of the Child Behavior Checklist, Achenbach, 1991) and
social impairments (VISK: the Dutch version of the Children’s Social Behavior Questionnaire, Luteijn, Minderaa, & Jackson,
2002) of their child. These questionnaires were administered to ensure that participants with behavioral or social problems
were not included in the control group. Scores in the clinical range on any of the subscales were interpreted as an indication
for behavioral or social problems.
Ethical permission for the study was granted by the regional medical ethics committee (CMO region Arnhem-Nijmegen).
Primary caregivers of all children and children from the age of 12 years gave their informed signed consent prior to
participation in the study. Children age 8–12 years gave their verbal consent. Participants were rewarded with a gift voucher.
The study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2000.

2.2. Apparatus and setup

An adapted version of the virtual bar-balancing task as exploited by Newman-Norlund et al. (2008) was used in the
current study. The task was programmed in Presentation 9.90 (Neurobehavioral Systems, USA). To make task performance
more appropriate for children, the squeeze pads that were used in the original study to control the vertical movement of the
bar on the computer screen were replaced by gamepads (Logitech Dual Action), each with two analog joysticks, one of which
could be controlled by the left thumb and the other by the participant’s right thumb.
The participants were seated comfortably on adjustable chairs side by side in front of a table on which a monitor (refresh
rate 75 Hz; 1024 by 768 pixels) was placed at eye level. The participants were able to control the bar by moving the left and
right analog joysticks forward in the sagittal plane. In the J4 condition, subjects’ respective left (L1 and L2) and right (R1 and
R2) joystick movements (see Fig. 1) were summed and multiplied by a gain factor of 3.5 to produce positional displacement
of the left and right side of the stimulus bar in pixels. The same gain factor was used for the solo and J2 conditions, in which
only two hands (either from the same or from different subjects) controlled the movement of the bar. Output of the gamepad
was sampled at a rate of 75 Hz and smoothed by a running-average of 10 samples. Lateral movements of the joysticks did not
affect the position of the bar.

Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
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2.3. Task and procedure

Before the experiment started, participants received instructions about the purpose of the task, i.e. to lift the bar into a
target area consisting of two horizontal lines in the upper part of the screen (see Fig. 1). It was explained that in order for a
trial to be successful the bar needed to be lifted to the target area, and held in the target area for 2 s continuously, without
dropping the ball. Participants received feedback when the bar was positioned correctly in the target area via the color of the
bar that would turn (from green to) white when the bar was positioned correctly in the target area. After the bar remained in
the target area for 2 s its color changed to purple indicating success and the trial would finish. Participants were not allowed
to talk during the task.
In the single condition (S), the participants lifted the bar on their own using the left and the right joysticks on the gamepad
to control the vertical position of the bar. Both participants always performed the solo condition first, one after the other.
Subsequently the joint conditions were run. The order of the two joint action conditions was counterbalanced between
dyads. In the J2 condition the participant sitting on the left side used his or her left hand (L1) to control the left end of the bar
and the participant on the right side used his or her right hand (R2) to control the right end of the bar. In the J4 condition
participants jointly lifted the bar with four hands, with the left hands of both subjects (L1 and L2) controlling the left end of
the bar and the right hands of both subjects (R1 and R2) controlling the right end.
All conditions (S, J2, and J4) consisted of 30 trials each, preceded by a minimum of three and a maximum of nine practice trials
to familiarize participants with the task requirements. At the start of each trial a visual countdown of 3 s was displayed in the
form of a digit presented in the center of the bar counting back from three to one. In cases where the joysticks were moved before
the countdown was finished, a message indicating the detection of a false start was presented on the screen and the trial was
restarted. After the countdown, a floating horizontal green bar with a pink ball on top appeared in the bottom of the screen (see
Fig. 1) after which participants would initiate their lifting movements. A trial would finish when subjects managed to keep the
bar inside the target area for 2 s, when the ball would drop, or when the maximum trial duration of 15 s was reached.

2.4. Data analysis

Reaction times were derived online in Presentation (Neurobehavioral Systems, USA) by an algorithm that measured if the
joy-stick rotation exceeded a baseline measurement that was taken before the countdown. The criterion for detection of a
movement was set at 30 pixels which approximated 18 of joy-stick rotation. Reaction times were calculated per trial for each
subject separately as the first movement of either the left or of the right joystick that exceeded the above criterion. Offline
analysis was done in Matlab 7 (The Mathworks, USA). Mean reaction times were calculated after excluding values shorter or
longer than 3 standard deviations from the mean, as well as reactions shorter than 100 ms and longer than 1000 ms. In
addition, absolute inter-individual RT differences between dyad members were calculated per trial and condition to
determine temporal synchronization between co-actors. Finally, we calculated the number of trials per condition in which
dyads managed to respond synchronously, i.e. within 100 ms from each other.
For each trial, the average rotation value per joystick (L1, R1, L2, and R2) was calculated to determine the average lift
distribution per dyad in the J4 condition. In order to control for possible transfer effects between joint action conditions only
the first joint action block of each dyad was analyzed. Differences in lift distribution percentages between outer and inner
hands were determined via the following equations:
!
X30
L1t R2t
Percentage outer hands ¼ þ
t¼1 L1t þ R1t L2t þ R2t

!
X
30
R1t L2t
Percentage inner hands ¼ þ
t¼1 L1t þ R1t L2t þ R2t

where t represents the trial number per condition, L1t and R1t , respectively, reflect the average left and right hand joystick
displacement per trial of subject 1, and L2t and R2t , respectively, the average left and right hand joystick displacement per
trial of subject 2. The resulting lift distribution percentages for outer hands and inner hands provide a measure of the relative
bias that dyads may have towards using their outer or inner hands for lifting the stimulus bar. An absence of bias would be
reflected in a 50% contribution of both inner and outer hands. Fig. 2 presents an example of a trial with biased lift distribution
where both subjects tend to use their outer hand more for lifting than their inner hands. In this example trial the outer hands
account for about 70% of the lifting whereas the contribution of the inner hands is only about 30%.
Bar rotation was assessed by calculating the absolute bar rotation angle in degrees relative to horizontal from the time of
movement onset until trial end. For trials in which the ball was dropped, the offset of the bar’s center was determined at the
moment that the ball was lost to specify the height of the ball drop. Furthermore, for each trial the total time was calculated during
which the stimulus bar was positioned correctly in the target area. Success-rate was determined by calculating the number of
successful trials as a percentage of the total number of trials administered. Average bar rotation, mean height of ball drop, average
time in target area, and the success-rate were determined per condition and per subject/dyad for statistical analyses.
Statistical tests were run separately for solo and joint conditions. Direct comparison between solo and joint conditions
was prohibited because the order of presentation to subjects was not counterbalanced. All dependent variables, except

Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders (2011), doi:10.1016/
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[()TD$FIG]
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60

Joystick angle (degrees)


50
L1
40

30 R1

20
R2
10
L2
0
0 1 2 3 4 5
Time (s)

Fig. 2. Example of a successful J4 trial with biased lift-distribution. This dyad shows a preference for lifting the stimulus bar with their outer hands (L1 and
R2) as opposed to their inner hands (R1 and L2). The contribution of outer and inner hands was calculated as a percentage score per trial.

success-rate, were analyzed using repeated measures ANOVA’s to test for within-subject effects of condition (J2 and J4) and
between-subject effects of group (ASD, control). Post hoc pair-wise comparisons between conditions were analyzed using
paired sample t-tests, and pair-wise comparisons between groups were tested with independent sample t-tests. Success-
rates were analyzed using Mann–Whitney tests for pair-wise comparisons between groups and sign tests were used for
comparisons between conditions. Alpha was set at .05.

3. Results and discussion

3.1. Solo task performance

In order not to mistake differences in joint action performance between ASD and control dyads with baseline differences in
their ability to do the lifting task, the performance of all participants in the solo task condition was first compared between the
two groups on a selection of dependent measures. No significant differences between the ASD and the control group were found
in their average reaction times, t(54) = 1.5, the height at which they dropped the ball, t(54) = .4, the time they held the bar in
the target area, t(54) = .7, and the success-rates of the two groups in their solo task performance, Mann–Whitney test, N = 56,
ns. However, individuals from the ASD group did show significantly larger variation in bar rotation as compared to the control
group in their solo task performance, t(54) = 2.6, p < .05 (see Table 1 for the solo task performance of both groups). Overall, these
results reveal strong similarity in solo task performance of individuals from the two groups as no coarse differences in behavior
were found. This suggests that the initial abilities of individuals from the autistic spectrum and controls for this specific task are
well matched and thus allow for comparing their joint action performance on the above measures.
Importantly, the similarity in lifting performance of individuals from the autistic and the control group should not be
taken to reflect that there are no specific motor deficits associated with ASD. In fact, problems with motor coordination are a
well known issue in ASD (Baranek, 1999; Spencer et al., 2000). Consistent with this fact, the present study revealed more
variation in bar rotation during lifting in participants with ASD as compared to controls. This increased variation in balancing
may have to do with impairments of the corpus callosum and decreased inter-hemispheric connectivity (Alexander et al.,
2007; Boger-Megiddo et al., 2006; Vidal et al., 2006), which are known to affect bimanual motor coordination in ASD
(Johansen-Berg, Della-Maggiore, Behrens, Smith, & Paus, 2007; Marion, Kilian, Naramor, & Brown, 2003).

3.2. Temporal coordination in joint action

3.2.1. Reaction times


We hypothesized that children and adolescents with ASD have problems building an internal model of the timing of the
actions of their co-actor. Consequently it was predicted that individuals from the ASD group would not adjust their RTs to

Table 1
Solo task performance data of participants from the ASD group and the control group.

Performance variable ASD group Control group

M SD M SD

Reaction time 352 104 398 132


Height of ball drop 237 128 291 176
Time in target area 574 575 691 653
Percentage success 14.4 18.3 22.2 22.2
Absolute bar rotation 18 4.4 14.4 4.0

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Fig. 3. Reaction times of the ASD and control group in the J2 and J4 joint action conditions, reaction times represent each individual’s average lifting onset.
Dyads from the control group waited for each other in the J2 condition which required synchronized lifting from both actors. Error bars reflect SEM.

accommodate the behavior of their partner, i.e. they would not wait for each other. A mixed-design ANOVA with condition
(J4 and J2) as within subject factor and group (ASD and control) as between subject factor, revealed no significant effect of
condition, F(1,54) = 2, ns, and no effect of group, F(1,54) = 2.8, ns on RTs. However, a significant group  condition interaction
was found, F(1,54) = 5.06, p < .05. This interaction effect is visible in Fig. 3. See Table 2 for the exact RTs. Post hoc comparisons
between conditions using paired sample t-tests indicated absence of a RT difference between the J4 and J2 conditions for the
ASD group, t(27) = .8, ns, whereas RTs of the control group were found to be delayed in the J2 condition as compared to the J4
condition, t(27) = 2.14, p < .05. Post hoc comparisons using independent sample t-tests showed no significant RT difference
between the two groups in the J4 condition, t(54) = .3, ns, but a clear difference between groups in the J2 condition, were the
control group’s RT was found prolonged relative to the ASD group, t(54) = 2.6, p < .05. These findings confirm the prediction
that children and adolescents with ASD have difficulty representing the timing of the lifting movements of their partners in
the J2 condition corroborating the hypothesis of impaired internal modelling in individuals with ASD.
The finding that dyads from the control group were slower to initiate their movements in the J2 condition than in the J4
condition is not an arbitrary finding considering that Kelso, Southard, and Goodman (1979) and Ohtsuki (1994) showed
unilateral movements are typically initiated faster than simultaneous bilateral actions that are carried out by two hands
(probably as a result of inter-hemispheric inhibition in the latter condition). This underscores the view that dyads from the
control group deliberately delayed their movement onset to synchronize with their partner to keep the ball from rolling of
the bar. However, in order to further corroborate this interpretation, for each dyad the absolute inter-individual RT difference
per trial (RTsync) was calculated and averaged across all trials in the J2 condition. Smaller values of RTsync indicate more
synchronous lifting reflecting enhanced coordination. An independent samples t-test comparing RTsync between the two
groups revealed no significant difference, t(27) = 1, ns. However, an additional analysis focusing on the number of closely
synchronized trials (RTsync < 100 ms) in the J2 condition, revealed a clear group difference reflecting more synchronized
trials for the controls (20%) than for dyads from the ASD group (10%), t(26) = 2.5, p < .05. This result clearly corroborates the
assumption that by delaying their RTs, controls were able to synchronize the onset of their movement with their partner.
Moreover, the smaller number of synchronized trials in the ASD group confirms the interpretation that subjects from the ASD
group did not accommodate their movements in accordance with the lifting onset of their partner.

3.2.2. Height of the ball-drop


As a consequence of the impaired temporal coordination by ASD dyads we predicted that they would drop the ball at a
much lower height in the J2 condition as compared with controls. A mixed-design ANOVA with condition (J4 and J2) as
within subject factor and group (ASD and control) as between subject factor revealed a main effect of condition,

Table 2
Joint task performance data of participants from the ASD group and the control group in the J2 and J4 conditions.

Performance variable ASD group Control group

J2 J4 J2 J4

M SD M SD M SD M SD

Reaction time 367 95 380 105 442 118 388 119


RTsynca 256 57 212 72 243 67 243 84
Height of ball drop 146 224 468 137 372 189 468 150
Time in target area 703 922 904 812 976 488 1385 579
Percentage success 23.7 33.7 28.7 26.1 29.0 15.6 42.7 23.7
Absolute bar rotation 22.2 7.4 20.2 7.0 17.1 5.2 15.9 5.3
a
RTsync reflects the absolute average difference in reaction time between the lifting onsets of both actors.

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F(1,26) = 48.3, p < .001, indicating that dyads in both groups lost the ball at a significantly lower height in the J2 condition
than in the J4 condition. No main effect of group, F(1,26) = 2.9, ns, but a significant group  condition interaction,
F(1,26) = 14.9, p < .01 was found indicating that dyads from the ASD group lost the ball at significantly lower elevation in the
J2 condition. Two post hoc independent t-test confirmed that ASD dyads lost the ball at a lower height in the J2 condition as
compared to dyads from the control group, t(26) = 2.9, p < .01. No difference in height of the ball-drop between the groups
was found in the J4 condition, t(26) = .2, ns (see Table 2). These results confirm the previous finding in RTs that dyads from the
ASD group did less well in coordinating the onset of their lifting movements resulting in ball-drops at an early stage of the
lifting action.
The above findings regarding movement onset synchronization and ball dropping indicate that children and adolescents
with ASD had particular difficulty in coordinating their actions with a co-actor in time. Internal models play an important
role in predicting the sensory consequences of self-generated actions over time (Wolpert, Miall, & Kawato, 1998) and much
evidence has been provided to suggest that the same models are also used for predicting the upcoming sensory effects of
other people’s actions (Gazzola & Keysers, 2009; Iacoboni, 2005a; Wolpert, Doya, & Kawato, 2003). As such, the present
results confirm the hypothesis that individuals with ASD are impaired in forming an internal model of a co-actors behavior,
which limits their ability to derive a reliable prediction at which time future actions of another individual are likely to take
place.
However an alternative explanation for the inability of participants with ASD to coordinate their actions in time with their
partner is that they paid less attention to or did not acknowledge the presence of the other person or their contribution to the
task. Studies of Sebanz et al. (2003) and Sebanz, Knoblich, and Prinz (2005) have shown that healthy individuals show a
strong (and automatic) tendency to form a co-representation of another person’s task even when no action coordination is
required. It may be that individuals with ASD are impaired at forming a task-representation or are simply not interested in
mentalizing about others, e.g. because of impairments in ToM. A study from Sebanz, Knoblich, Stumpf, et al. (2005)
addressing this specific question revealed similar effects of co-representation in groups of high-functioning adults with
autism and matched controls. This suggests that the reason why dyads with ASD did not coordinate their actions in the
current study is probably not because they did not represent the task of a co-actor, but more likely because of the specific
requirements of the J2 task to predict and coordinate movement onset with a co-actor in time. In line with this view, Liebal,
Colombi, Rogers, Warneken, and Tomasello (2008) recently found that children with ASD were impaired in tasks that require
inter-personal cooperation but showed no impairment in a task investigating one’s ability to understand other’s need for
help, and motivation to assist.

3.3. Agency in joint action

3.3.1. Lift distribution


In the present study, impairments in internal modelling for joint action in ASD were investigated in two joint action tasks,
J2 and J4, each of which posed a unique challenge to dyads. In the previous section (Section 3.2), focus was primarily directed
at temporal coordination of actions in ASD resulting from impairments in internal modelling. In the present section,
attention is directed at another functional deficit associated with impaired internal modelling, i.e. the experience of agency
and the difficulty in self/other discrimination in ASD.
The J4 task, among other things, was designed to generate difficulty in the detection of agency, i.e. the ability to
distinguish one’s own contribution of the bar movement on the screen from the contribution of a co-actor. That is, because
the lifting of the bar reflected the summed input of both actors, agency cannot be determined on the basis of sensory or motor
information alone, but requires integration of motor and sensory signals via internal modelling. Based on the hypothesis that
individuals with ASD suffer from a specific impairment in internal modelling it was predicted that they would experience
particular difficulty with this task (i.e. in associating their actions with their sensory effects). One solution to situations in
which agency is ambiguous is to try and separate action effects of either actor on a particular dimension (e.g. in time or
space). In the present study we asked whether or not participants with ASD would compensate for their inability to model
these action effects by developing a division of labor, or alternate spatial strategy, to enhance contingency between self-
generated actions and their sensory effects.
To examine lift distribution within each dyad, the relative contribution of each actor’s inner and outer hands during the
lifting was determined (see Section 2.4). The resulting lift percentages were transformed to the normally distributed variable
z by means of Fisher’s z transformation. To control for possible transfer effects between J2 and J4 only data was used from the
first joint action block that dyads completed. A mixed-design ANOVA with hands (outer and inner) as within subject factor
and group (ASD and control) as between subject factor revealed no significant effect of group, F(1,52) = 1.1, ns, a significant
effect of hands, F(1,52) = 13.0, p < .01, and a significant group  hands interaction F(1,52) = 7.1, p < .05. Post hoc comparisons
using paired sample t-tests showed a significant difference between the contribution of outer hands (70%) and inner hands
(30%) for dyads in the ASD group, t(26) = 3.3, p < .01, but no difference for the control group (54% and 46% for outer and inner
hands, respectively), t(26) = 1.4, ns (see Fig. 4).
These results indicate that dyads from the ASD group exerted significantly more control with their outer hands than with
their inner hands in the J4 condition, consistent with the prediction that they would follow a specific strategy to enhance
their experience of agency by distributing control over the bar. Furthermore, the direction of the distribution bias to the outer
hands is not likely to be a coincidental finding as previous studies (Hommel et al., 2009; Sebanz et al., 2003) have shown that

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100 Inner hands


Outer hands
80

Lift percentage
60

40

20

0
ASD Control

Fig. 4. Lift distribution percentages of inner and outer hands. Percentages reflect the relative contribution of each individual’s outer and inner hand (relative
to the dyad) to the bar lifts. Dyads from the ASD group had a strong tendency to distribute lift to their outer hands, a strategy which helped them
differentiate between self from other generated action effects. Error bars reflect SD.

subjects have a preference for stimuli presented at their side of a computer screen in a situation with two subjects sitting
aligned in front of a monitor. This effect is known as the social Simon effect, reflecting the original finding of Simon and
Rudell (1967) but framed in a social manner, that subjects are faster to respond to stimuli at locations that are congruent
with the location of their response, even if the stimulus location is irrelevant to the task. The finding that dyads with ASD
show a bias for controlling the bar using their outer hands confirms the presence of a social Simon effect in the present
experiment and replicates the findings from Sebanz, Knoblich, Stumpf, et al. (2005) who reported a social Simon effect in
high-functioning adults with autism. As indicated above, the finding of a social Simon effect in the present data confirms the
earlier suggestion that children and adolescents with ASD did acknowledge the presence (and relative location) of their co-
actor. However, more importantly, this finding confirms the hypothesis that dyads from the autistic group had particular
difficulty in differentiating their actions from a co-actor and attempted to circumvent this difficulty by distributing control
over the left and the right side of the bar between the two partners.

3.3.2. Success-rate
The strategy of dyads from the ASD group to maximize use of their outer hand during lifting in the J4 condition may have
consequences in terms of task performance. A study by Bosga and Meulenbroek (2007), using an earlier version of the bar
lifting paradigm in healthy adults, found lifting performance to be less efficient in a 2-actor/2-hands condition than in a 2-
actor/4-hands condition, comparable with the respective J2 and J4 conditions in the current study. Because the strategy of
ASD dyads to use mainly their outer hands renders the J4 task more similar to a J2 task, we would expect performance
measures, such as the time that is spent in the target area and the number of successful trials in this condition to more or less
resemble the J2 condition. For the control group, however we would expect an advantage of four (J4) over two (J2) hand
control.
Consistent with these predictions, Mann–Whitney tests comparing the J2 and J4 success-rates within the two groups
revealed a significant effect for the control group (sign test, N = 14, p < .05), reflecting higher success-rates in the J4 condition
than in the J2 condition (see Table 2). In contrast, no significant difference in success-rates between the J2 and the J4
conditions was found for dyads from the ASD group (sign test, N = 14, ns).

3.3.3. Time in target area


Similar to the analyses of success-rate we expected the ‘time in target area’ measures to be longer in the J4 condition than
in the J2 condition in dyads from the control group. Instead, for dyads from the ASD group we expected the ‘time in target
area’ measures in the J4 condition to be comparable to the J2 condition.
A mixed-design ANOVA with condition (J4 and J2) as within subject factor and group (ASD and control) as between
subject factor, revealed no significant effect of group, F(1,26) = 2.3, ns, but a significant effect of condition, F(1,26) = 7.7,
p < .05, reflecting more success in maintaining the bar in the target area in the J4 condition than in the J2 condition. The
interaction between condition and group was not significant, F(1,26) = .9, ns. However, separate analyses to determine the
reliability of the effect of condition in either group revealed an effect of condition in the control group, t(13) = 3.8, p < .01, but
no significant difference between conditions for the ASD group, t(13) = 1.05, ns. Table 2 reports the average time that dyads
managed to keep the bar in the target area correctly per group for each condition separately.
Both the success-rates and the time that dyads managed to keep the bar in the target area confirm the prediction that the
strategy of dyads from the ASD group to distribute control over the bar negatively affected the performance outcome of their
lifting actions. These results suggest that dyads from the ASD group sacrificed bimanual control over the bar in order to
enhance their sense of agency.

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3.3.4. Bar rotation


Our analysis of the solo condition (see Section 3.1) showed that children and adolescents with ASD exhibit stronger
average rotation of the bar. This finding limits our ability to draw conclusions regarding potential differences between ASD
dyads and control group dyads in the performance of joint action tasks. Within-group comparisons between conditions,
however, are still possible. With respect to bar orientation we expected a to find the same pattern of results we observed
with regards to success-rates, i.e. a reduction in rotation error in the J4 condition relative to the J2 condition for control dyads,
reflecting the increased control they gained over the bar by utilizing four hands. For the ASD group we expected no
differences in bar orientation due to the similarity in the distribution of lift between the J4 and J2 conditions.
A mixed-design ANOVA with condition (J4 and J2) as within subject factor and group (ASD and control) as between
subject factor, revealed a significant effect of group, F(1,26) = 4.6, p < .05, reflecting a stronger bar rotation error for dyads
from the ASD group than from the control group, replicating the earlier finding in solo task performance. However, neither
the effect of condition, F(1,26) = 2.8, ns, nor the group  condition interaction, F(1,26) < 1, ns, were significant. The absence of
a difference in bar orientation between conditions in the ASD group confirms the prediction that both tasks were conducted
in similar manner. However, the absence of a difference in bar orientation between conditions in the control group was
unexpected.

3.3.5. Positive effects of enhancing agency


Whereas the previous analyses (Sections 3.3.1–3.3.4) indicated negative effects associated with biasing lift distribution in
the J4 condition (i.e. smaller success-rate and earlier dropping of the ball), the hypothesis that changes in lift distribution
reflect an adaptive strategy suggests that there may also be performance benefits associated with this bias. Indeed, an
immediate positive effect of enhancing the sense of agency would be that participants would notice a tighter correlation
between actions (joystick displacement) and their accompanying sensory effects (lifting of one side of the bar), which should
positively affect their ability to control the lifting and angle of the bar. To test for such a positive effect a bivariate Pearson
correlation was calculated between the lift distribution and rotation angle of ASD dyads in the J4 condition. A significant
negative correlation was found, r = .56, p < .01, reflecting smaller bar orientation error in association with increased lift
distribution bias between co-actors. In the control group the same correlation did not reach significance, r = .24, ns. An
additional independent t-test (one-sided) between a subset of ASD dyads with high (>58%) and low (<58%) lift distribution
bias was significant, t(26) = 2.01, p < .05, reflecting smaller average bar orientation for the subgroup of ASD dyads with a
large lift distribution bias (M = 19.48) as compared to the subgroup with a small lift distribution bias (M = 23.98).
These results support the interpretation that the lift distribution between ASD dyads involves a deliberate strategy that is
helping them to circumvent problems in establishing agency and improving their ability to control the bar. That is, by biasing
the ratio between self generated effects (signal) and other generated effects (noise) ASD dyads may strategically compensate
for their impairments in internal modelling.
In the present study internal models are not only associated with supporting motor control but also believed to be
important for predicting the timing of a co-actor’s movement. Therefore, it was hypothesized that enhancing agency (by
means of distributing lift between actors) might also positively influence dyads’ ability to synchronize their response onsets.
That is, one would expect dyads with ASD who distribute lift to be better at coordinating the initiation of their movements,
i.e. have smaller inter-individual reaction time differences, as compared to dyads without a distribution bias. In order to test
this hypothesis a second bivariate Pearson’s correlation was calculated between ASD dyads’ (outer hand) lift distribution
percentages in the J4 condition and their absolute inter-individual reaction time differences in that same condition.
Consistent with our prediction we found a significant negative correlation, r = .48, p < .01, reflecting a relative reduction in
reaction time differences for dyads with a larger lift distribution bias. No such correlation was found for the control group,
r = .08, ns. An additional independent t-test (one-sided) between ASD dyads with high (>58%) and low (<58%) lift
distribution biases was significant, t(26) = 5.9, p < .001, indicating smaller inter-individual reaction time differences in ASD
dyads evincing a large lift distribution bias (M = 188 ms) as compared to ASD dyads evincing a small distribution bias
(M = 237 ms).
These findings support the view that the lift distribution bias observed in jointly acting ASD dyads reflects a true
functional adaptation to the task requirements of the J4 condition. Importantly, although this adaptation was found to
negatively affect ASD dyads’ performance as, e.g. reflected in success-rates, it did also positively affect their ability to balance
the bar and synchronize the onset of bar lifts. The finding that children and adolescents with ASD that participated in the
present study adopted a disambiguation strategy is particularly interesting because it (a) provides evidence for the existence
of an impaired sense of agency in this group and (b) reflects their natural tendency to make practical adjustments in order to
circumvent or make up for functional impairments.
An interesting and speculative suggestion that derives from this finding is that several of the social deficits associated
with ASD such as impairments in reciprocal play and social interaction may in fact reflect behavioral adaptations which have
been implemented for the explicit purpose of controlling or evading conflicting or ambiguous information. Consistent with
this view it has been suggested that highly repetitive and predictive behaviors such as hand flapping, and rocking back and
forth, which are stereotypical behaviors of children with ASD, are performed when children are overwhelmed by the
complexity and unpredictability of their surroundings, and seek to isolate themselves to regain a sense of agency over their
experience (Pares, Masri, van Wolferen, & Creed, 2005). In addition, the strategic isolation from conflicting information fits in
well with the classical condition of autism as described by Kanner involving a ‘‘seeming indifference to social interaction and

Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
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extreme self-focus [that is] exhibited by these children, who, as he observed, regarded contact with others as ‘interference’’’
(Kanner, 1943 as discussed by Uddin et al. (2008)).

4. Conclusion

The present study found clear differences in performance between the ASD group and matched controls in joint action
tasks that required close coordination between two actors. Children and adolescents with ASD were impaired in predicting
the occurrence of their partner’s response in the J2 task (joint lifting with two hands). They did not delay the timing of their
lift initiation to accommodate their partner and performed less well in synchronizing their response onsets, causing the ball
to drop quickly after movement onset. In addition, dyads from the ASD group were found to circumvent ambiguity in bar
lifting in the J4 task (joint lifting with four hands), by spatially re-distributing control of the bar to their outer hands. That is,
they sacrificed bimanual control over the bar in order to enhance their sense of agency. Participants who adopted this
strategy were more successful in controlling the stability of the bar and were better able to synchronize the onset of their bar
lifting movements with their partners. Findings from both tasks, i.e. impairments of ASD dyads in their ability to predict and
temporarily coordinate actions with a partner, and their adaptive strategy to reduce response ambiguity, fit well with the
hypothesis of impaired internal modelling in ASD. Furthermore, the strategy to separate action-effect contingencies between
partners in the J4 task suggest that reduced social reciprocal behavior and joint cooperative play exhibited by individuals
with ASD may reflect behavioral adaptations that are designed to evade conflicting or ambiguous information encountered
in social settings. Both impairments in internal modelling and behavioral adaptations to circumvent these impairments may
come about most clearly in tasks that require close coordinative action between co-actors and monitoring of self and other
generated behaviors. The current study stresses the importance of using social interactive paradigms to investigate the
origin and nature of autism related disorders.

Acknowledgements

This research was supported by the EU-Project ‘‘Joint Action Science and Technology’’ (IST-FP6-003747). We thank Pascal
de Water and Norbert Hermesdorf for their technical assistance.

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Please cite this article in press as: Stoit, A. M. B., et al. Internal model deficits impair joint action in children and
adolescents with autism spectrum disorders. Research in Autism Spectrum Disorders (2011), doi:10.1016/
j.rasd.2011.02.016

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