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www.elsevier.com/locate/b&c
a,b,*
, G. Dawson
a,b,c,d
, S. Webb
b,c,d
, M. Murias
b,c,d
Abstract
Imitation ability has consistently been shown to be impaired in individuals with autism. A dysfunctional execution/observation
matching system has been proposed to account for this impairment. The EEG mu rhythm is believed to reect an underlying execution/observation matching system. This study investigated evidence of dierential mu rhythm attenuation during the observation, execution, and imitation of movements and examined its relation to behaviorally assessed imitation abilities. Fourteen high-functioning
adults with autism spectrum disorder (ASD) and 15 IQ- and age-matched typical adults participated. On the behavioral imitation task,
adults with ASD demonstrated signicantly poorer performance compared to typical adults in all domains of imitation ability. On the
EEG task, both groups demonstrated signicant attenuation of the mu rhythm when executing an action. However, when observing
movement, the individuals with ASD showed signicantly reduced attenuation of the mu wave. Behaviorally assessed imitation skills
were correlated with degree of mu wave attenuation during observation of movement. These ndings suggest that there is execution/
observation matching system dysfunction in individuals with autism and that this matching system is related to degree of impairment
in imitation abilities.
2007 Elsevier Inc. All rights reserved.
Keywords: Autism; Imitation; EEG; Mu rhythm; Mirror neurons
1. Introduction
Imitative decits in individuals with autism have consistently been observed (Williams, Whiten, & Singh, 2004). In
fact, several researchers have suggested that imitation deficits are one of the core impairments of autism spectrum
disorders (ASD; Dawson & Adams, 1984; Dawson &
Lewy, 1989; Rogers & Pennington, 1991; Williams,
Whiten, Suddendorf, & Perrett, 2001). Imitation impairments in autism were rst reported by DeMyer and col*
Corresponding author. Address: Box 357920, Center on Human
Development and Disability, University of Washington, Seattle WA
98195, USA. Fax: +1 206 543 5771.
E-mail address: rab2@u.washington.edu (R. Bernier).
0278-2626/$ - see front matter 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.bandc.2007.03.004
Jones & Prior, 1985; Ohta, 1987; Smith & Bryson, 1998).
Such impairments persist into adolescence and adulthood
although there are fewer studies that have examined this
age group (Avikainen, Wohlschlager, Liuhanen, Hanninen,
& Hari, 2003; Hobson & Lee, 1999; Rogers, Bennetto,
McEvoy, & Pennington, 1996). Hobson and Lee (1999)
found that teens with autism were able to imitate goal
directed actions but failed to imitate the style in which
the examiner performed the task with greater frequency
than the control group. Further, during the imitative acts,
the subjects with autism made considerable reversal errors,
errors in which the imitator replicates the gestures but in
the perspective of how the gesture was observed. Similarly,
Avikainen et al. (2003) examined imitation in adults
through a task in which participants imitated the experimenters actions using either the same hand or opposite
hand. They found that while typical adults used the mirror
image of the experimenters actions to increase response
speed and accuracy, the individuals with Asperger syndrome and high functioning autism failed to capitalize on
the mirror image.
It has been proposed that a decit in self other mapping
is the most parsimonious explanation for the imitation
impairments found in ASD (Williams et al., 2004). The
self-other mapping decit hypothesis, which posits that a
biological dysfunction of cross modal processes prevents
the individual with autism from forming and coordinating
representations of the self and others, was earlier presented
by Meltzo and Gopnik (1993) and Rogers and Pennington (1991). Evidence from infant imitation work suggests
that cross modal processes necessitate an execution/observation matching system (Meltzo & Decety, 2003; Meltzo
& Moore, 1997). That is, in order for an infant to imitate
faces, the infant must cross modally map an observed facial
expression with his or her own motor execution of that
expression. But the infant cannot see his or her face and
so must have a supramodal internal representation that
enables a match between the observed and executed
expression.
1.1. Mu activity and the execution/observation system
The rst neurophysiological evidence of an execution/
observation matching system in humans comes from
EEG work conducted in the 1950s which focused on the
mu rhythm band oscillations. The EEG mu rhythm band
falls between 8 and 13 Hz and is recorded from scalp electrodes over the sensorimotor cortex. Attenuation of resting
EEG mu rhythm reects desynchronization of the underlying cell assemblies, which suggests an increased load on
those cells (Pfurtscheller, Neuper, Andrew, & Edlinger,
1997). Attenuation of the resting EEG mu rhythm was
observed in adult subjects in response to the execution of
actions, both passive or reex movements (Chatrian, Petersen, & Lazarte, 1959). Attenuation was also observed in
adults who were watching others movements (boxing) on
lm (Gastaut & Bert, 1954). More recently, the nding of
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230
Table 1
Participant descriptive characteristics
Group
Ethnicity
Handedness
Age (years)
Min.
Max.
M (SD)
FSIQ
VIQ
PIQ
ASD
Typical
14
15
13 White, 1 Other
13 White, 2 Other
12 Right, 2 Left
11 Right, 4 Left
19.4
18.6
37.5
43.7
23.6 (4.9)
26.7 (8.7)
114.0 (14.2)
108.9 (15.6)
117 (14.1)
110.1 (14.7)
107.6 (15.4)
105.4 (18.2)
impedances were below 50 kX. EEG signals were analog ltered (0.1 Hz high-pass, 100 Hz elliptical low-pass) amplied, and digitized at a 250 Hz. The participant sat
approximately 75 cm from a video monitor that delivered
the stimuli. The video stimuli were presented on the monitor at a size of 17.5 cm by 26.25 cm and subtended a visual
angle of 13.3 by 19.8. All 128 channels were recorded continuously and stimulus onset and cessation and event
markers were registered with the physiological record for
o-line segmentation of the data. The vertex electrode
was used as a reference, and the data were later re-referenced to an average reference. Data were post processed
using software provided by Electrical Geodesics, Inc.
2.3.2. EEG imitation paradigm
Following the paradigm developed by Muthukumaraswamy and Johnson (2004) the experiment consisted of
four conditions: resting, observe, execute, and imitate. All
stimuli were presented on videotape to ensure standardization of administration of the hand movements. In the resting condition, the participant was asked to sit quietly with
hands in lap. In the observe condition participants viewed
an adult gripping a manipulandum (Muthukumaraswamy
et al., 2004) with thumb and index nger as shown in
Fig. 1.
In the observe condition, participants sat with hands in
lap and observed the action. In the execute condition, participants were verbally instructed to grip the manipulandum identical to that shown in the videotape in the same
manner as shown in the videotape. The video monitor
showed only the manipulandum at this time and no movement. The manipulandum was placed on the table 50 cm
directly in front of the participant. In the imitate condition,
the participant was instructed to imitate the experimenter
gripping the manipulandum as shown on the videotape.
Each trial lasted approximately 3 s and there was a 7-s inter
trial interval between each trial. Twenty trials in each condition were presented with condition order randomized.
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232
Table 2
Results for mature imitation task
Summary scale
Mean (SD)
Typical group
Autism group
Total score
Face summary score
Hand summary score
Single task summary
Sequenced task summary
Style total
Number of errors
185.2
57.7
45.9
28.8
74.9
9.7
12.4
155.1
46.1
35.1
24.3
56.9
4.9
19.9
(13.1)
(4.3)
(7.8)
(2.4)
(8.8)
(1.9)
(5.2)
(19.4)
(7.7)
(12.4)
(3.5)
(14.7)
(2.9)
(10.1)
t-test
Sig. p<
4.92
5.076
2.832
4.047
4.037
5.299
2.544
.001
.001
.01
.001
.001
.001
.05
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Table 3
Mu wave power values for each autism participant (in lV2)
Subject No.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
Execute
.303940
.155272
.203481
.255224
.846268
.549620
.183697
.424599
.571214
.706779
.532764
.123849
.211769
.175790
(.125)
(.064)
(.081)
(.070)
(.478)
(.222)
(.031)
(.205)
(.372)
(.365)
(.175)
(.027)
(.040)
(.069)
Observe
Imitate
Resting
.685585 (.302)
.143876 (.040)
.127112 (.074)
.302710 (.093)
2.36863 (1.72)
.880590 (.434)
.248708 (.060)
.666416 (.308)
.842045 (.464)
2.00470 (.957)
1.01521 (.388)
.133719 (.056)
.358013 (.134)
.150766 (.091)
.336325 (.132)
.165551 (.058)
.158918 (.050)
.175809 (.092)
1.22539 (.895)
.508607 (.221)
.303731 (.103)
.359777 (.110)
.301757 (.149)
.572928 (.167)
.515492 (.190)
.106281 (.038)
.203514 (.058)
.226580 (.071)
1.08213 (.438)
.407575 (.146)
.214257 (.072)
.783554 (.350)
3.45046 (1.75)
.853169 (.750)
1.62923 (.417)
.546059 (.137)
2.12702 (.423)
3.09828 (.587)
3.65624 (1.32)
.152444 (.086)
.285538 (.138)
.117707 (.058)
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235
Another possibility is that disruption of the visual processing system or a disruption to other input systems may
disrupt the circuitry in the execution/observation matching
system. While rst order motion processing appears to be
intact in individuals with autism (Dakin & Frith, 2005),
there is evidence to suggest that there is a disruption in
the processing of biological motion and specically processing in the superior temporal sulcus (Boddaert et al.,
2004; Pelphrey, Morris, & McCarthy, 2005; Waiter et al.,
2004). Further research is necessary to clarify the role that
the processing of biological motion plays in the execution/
observation matching system, imitation, and the social deficits in autism. The most parsimonious explanation is that
disruptions to multiple circuits acting in concert result in
the pattern of social impairments seen in autism.
However, the execution/observation system cannot be
entirely dysfunctional, as individuals with autism are able
to imitate, albeit more poorly than individuals with typical
development. Likewise, there is much variability in theory
of mind abilities, empathy, and other social cognition deficits in individuals with autism. Therefore, it could be
degrees of dysfunction of this system, acting in concert with
degrees of disruptions in other neural systems, such as the
superior temporal sulcus, the limbic system, the cerebellum,
and the ventromedial prefrontal cortex, that potentially
lead to the range and variety of decits observed in autism.
In summary, the execution/observation matching system is believed to serve as the underlying neural circuitry
for imitation. This system allows the observer to translate
observed actions into an understanding of the action
through the activation of the observers motor system. Disruptions in the circuitry that translates visual input into
motor understanding can signicantly impact social interaction. In light of the fact that decits in social cognition
are a core feature of autism, it is logical to examine this circuitry as one of the many sources of impairment in autism.
This study provides further evidence of a disruption in the
execution/observation system in autism and the relation
between this circuitry and imitation skills.
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