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P. F. Ferrari, Biol. Lett. 1, 219 (2005).
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and Artifacts, K. Dautenhahn, K. Nehanic, Eds.
(Massachusetts Institute of Technology Press, Cambridge,
MA, 2002), pp. 247–273.
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Communication and Emotion in Early Ontogeny,
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14. Materials and methods are available as supporting
material on Science Online.
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Capuchin (Cambridge Univ. Press, Cambridge, 2005).

16. Y. Hattori, H. Kuroshima, K. Fujita, Anim. Cogn. 10, 141(2007).
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Proc. Natl. Acad. Sci. U.S.A. 105, 13685 (2008).
23. We gratefully acknowledge the help of M. Huntsberry,
D. Hipp, S. Bower, F. Dege, S. Dinterman, G. Coude,
G. Sirianni, E. Polizzi, and B. Gambetta. We thankMindblind Eyes: An Absence of
Spontaneous Theory of Mind in
Asperger Syndrome
Atsushi Senju,1* Victoria Southgate,1 Sarah White,2 Uta Frith2,3
Adults with Asperger syndrome can understand mental states such as desires and beliefs(mentalizing) when explicitly prompted to do so, despite having impairments in social
communication. We directly tested the hypothesis that such individuals nevertheless fail tomentalize spontaneously. To this end, we used an eye-tracking task that has revealed thespontaneous ability to mentalize in typically developing infants. We showed that, like infants,
neurotypical adults’ (n = 17 participants) eye movements anticipated an actor’s behavior on thebasis of her false belief. This was not the case for individuals with Asperger syndrome (n = 19).
Thus, these individuals do not attribute mental states spontaneously, but they may be able to do soin explicit tasks through compensatory learning.

I

mpairment in reciprocal social interaction andcommunication is a core feature of autism
spectrum disorders, regardless of age andability. This core feature is manifest in a wide
range of social impairments, including characteristic deficits in comprehension and use of
pretend play, expressive gestures, deception, andirony (1). One influential account that can explainthese varied and characteristic impairments proposes that they are a consequence of a failure in
the neurologically based capacity to “mentalize,”that is, the automatic ability to attribute mental
states to the self and others. The first evidence forthis hypothesis, which is also known as a deficit
in theory of mind (ToM) or “mindblindness”(2, 3), comes from the finding that children with
autism fail the verbally instructed Sally-Annefalse-belief task (FBT), whereas 4-year-old
neurotypical children pass, as do children with
Down syndrome of similar verbal mental age (4).
1
Centre for Brain and Cognitive Development, Birkbeck, University of London, London, UK. 2Institute of Cognitive Neuroscience, University College London, London, UK. 3Center ofFunctionally Integrative Neuroscience, Aarhus University,
Aarhus University Hospital, Norrebrogade 44, Building 10 G,
800 Aarhus C, Denmark.

*To whom correspondence should be addressed. E-mail:a.senju@bbk.ac.uk

In this task, which is considered a stringent
test of ToM (5), one character (Sally) places a
marble in a basket and leaves the room. In her
absence, another character (Anne) moves themarble to a box. When Sally returns, children are
asked where she will look for her marble. Ifchildren understand that Sally’s actions will bebased on what she believes to be true, rather than
the actual state of affairs, they should answer that
she will look in the basket, rather than the box.
This correct answer requires the child to predict
Sally’s behavior based on her now false belief.
Despite still exhibiting atypical social featurescharacteristic of autism, individuals of higher
verbal ability, in particular those with Asperger
syndrome, can pass such false-belief attribution
tasks (6–9). This competence presents a puzzle
for the mindblindness hypothesis (10) and has
prompted the proposal that these high-ability
individuals have acquired the ability to reason
explicitly about false beliefs by compensatory
learning, whereas difficulties in spontaneous
mental-state attribution may nevertheless persist(11). To date, there is only indirect evidence insupport of this hypothesis (12–16). In this study,
we seek to provide direct evidence by contrasting
the ability to pass the standard FBT with spontaneous looking behavior during a nonverbal
form of this task.

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SCIENCEVOL 325

J. Anderson and two anonymous reviewers for valuablecomments on earlier drafts of this paper. This research
was supported by the Division of Intramural Research,
National Institute of Child Health and Human
Development, and the TECT-ESF (The Evolution of
Cooperation and Trading–European Science Foundation)
project SOCCOP (The Social and Mental Dynamics of
Cooperation).

Supporting Online Materialwww.sciencemag.org/cgi/content/full/325/5942/880/DC1
Materials and Methods
SOM Text
References and Notes
13 May 2009; accepted 30 June 200910.1126/science.1176269

In a groundbreaking study, Onishi andBaillargeon (17) used an FBT scenario to exploit
infants’ tendency to look longer at events thatthey do not expect. The authors showed that 15month-old infants looked substantially longer
when an actor searched in a location where an
object was hidden that she could not know
about (that is, when her behavior was incongruent with her belief). Southgate et al. (18)extended this paradigm so that, rather than measuring whether young children look longer at
unexpected outcomes, they measured whether
children actually anticipate the outcomes before
they happen. They designed a task that made it
possible to assess directly whether children had
an understanding of the content of an actors’
belief. Briefly, 25-month-old children were familiarized to an event in which a puppet hid aball in one of two boxes (Fig. 1A), and then an
actor reached through one of two windows to
retrieve the ball from the box (Fig. 1C). Before
she reached, a light and simultaneous chime signaled that the actor was about to open a window
to retrieve the hidden object (Fig. 1B). In the test
trial, the puppet transferred the ball from one box
to another and then removed it altogether while
the actor was looking away (Fig. 1D). An eye
tracker was used to assess whether children expected (by making anticipatory eye movements)
the actor to open the door, which would be consistent with her having a false belief about thelocation of the ball. Southgate et al. found thatthese typically developing children made eye
movements toward the window above the box,
which was consistent with the actor’s belief
about the location of the ball, despite the factthat it no longer contained the ball. These children, who would not be able to perform the traditional verbally instructed FBT, thus correctly
anticipated the actor’s behavior in line with her
false belief.
It is this task (detailed above) that we used
for the present study (see also movies S1 andS2). We asked whether adults with Asperger
syndrome would, through their anticipatory looking, reveal a similar spontaneous capacity for
false-belief attribution. At the same time, we
had to establish that neurotypical adults would
show the same anticipatory looking as young

14 AUGUST 2009883

REPORTS
However, the eye-tracking version of the
FBT revealed a very different picture. We useddifferential looking score (DLS) (20), which isconsidered a highly reliable measure of looking
bias (21, 22), compiled over a 6-s period (19).
The Asperger group showed significantly lesslooking bias toward the correct window than did
the neurotypical group [Fig. 2A, main effect ofgroup: F1,32 = 4.93, P = 0.003, hp2 = 0.13,
analysis of variance]. Follow-up t tests revealed
that the neurotypical group scored significantly
above zero [mean = 0.42, t(16) = 2.76, P =0.014, Cohen’s d = 0.67, t test], meaning that
this group showed a significant bias toward thecorrect target, in line with the actor’s false belief.
This was not the case for the Asperger group,
whose bias did not differ from zero [mean: –0.001,
t(18) = –0.010, P = 0.99, Cohen’s d = 0.002, t test].
We also coded the direction of first saccade(Fig. 2B). Here, 13 out of 17 neurotypical participants made their first eye movement toward
the correct location, which was significantly
above chance (P = 0.049, binominal test). In

Fig. 1. Selected scenes fromstimulus movies (see also
movies S1 and S2). In familiarization trials, participants
were familiarized to an eventin which (A) the puppet
placed a ball in one of twoboxes, (B) both windows were
illuminated and a chimesounded, and (C) an actor
reached through the window
above the box in which theball was placed and retrieved
the ball. The participants
were familiarized to the contingency between (B) and (C).
In (D), the puppet moves theball while the actor is looking
away. This operation induces
a false belief in the actor
about the location of the ball.
Table 1. Mean chronological age (CA), verbal IQ (VIQ), performance IQ (PIQ), full-scale IQ (FIQ) (WAIS-III UK),
composite ToM score (ToM), Strange Stories test score (SS), scores of autism quotient (AQ), and autism diagnostic
observation schedule–generic (ADOS-G).

CA
VIQ
PIQ
FIQ
ToM*
SS†
AQ‡
ADOS-G

Neurotypical

Mean

SD

Range

Mean

SD

Range

36.8
116.8
109.6
115.6
9.7
13.2
34.9
7.9

14.3
14.4
13.0
14.9
2.0
1.8
7.6
4.7

21–67
85–14480–132
89–144
4–13.5
10–16
17–48
0–17

39.6
116.1
111.5
115.3
10.6
13.6
16.5
–

11.7
13.2
10.6
11.0
1.3
1.3
7.6
–

26–63
91–138
97–132
95–1298.5–12.5
12–16
6–37
–

14 AUGUST 2009

VOL 325SCIENCEB**

0.6*The ToM tests consisted of five first-order FBTs [Sally-Anne (4), Smarties (23), interpretational false belief (24), belief-emotion andreal-apparent emotion (25)] and two second-order FBTs [ice cream van (26) and coat story (6)].
†The Strange Stories test was
taken from (27) and required the participant to either interpret another’s behavior or understand another’s emotion.
‡AS and
NT groups differed significantly on the autism-spectrum quotient confirming their diagnostic status [AQ: (28), t(34) = 7.23, P <0.001, Cohen’s d = 2.41, t test]. No other variables were significantly different between the two groups.

884

A
*

0.4
DLS

Group

Asperger syndrome

contrast, only 8 out of 19 individuals in the
Asperger group made a correct saccade first, but
this did not significantly differ from chance (P =0.647, binominal test). These results are consistent with the DLS reported above. However,the first saccade, which represents a broad
categorical response, did not differentiate significantly between the groups (P = 0.30, Fisher’s
exact test, two-tailed).
Could our results be due to gaze abnormalities in the Asperger group? It is important tonote that they could not be attributable to an
avoidance of eye gaze because the actor’s eyes
were hidden beneath a visor. However, the duration of fixations to the actor’s face was significantly shorter in the Asperger group (mean = 1.9 s)than in the neurotypical group (mean = 3.1 s)[t(34) = –2.48, P = 0.018, Cohen’s d = 0.827,
t test]. This was not due to overall shorter fixations in the Asperger group, as the duration of
fixations toward the windows (correct and incorrect combined) did not differ between groups[mean = 2.5 s in Asperger group and 1.9 s inneurotypical group; t(34) = 1.53, P = 0.14,
Cohen’s d = 0.506, t test]. The correlation between DLS and the duration of face fixation was
not significant in either the Asperger or neurotypical group. Furthermore, total time spentlooking at the five regions of interest (face, two
windows, and two boxes) did not differ between
groups (4.8 s in Asperger group and 5.1 s inneurotypical group, see supporting online material text for further details). Thus, the lack of bias
toward the “correct” target in the Asperger groupis not explained by gaze abnormalities.
Our study demonstrates that adults withAsperger syndrome do not spontaneously anticipate others’ actions in a nonverbal task, closelymodeled on the standard FBT that they pass withease. In particular, the contrast with neurotypical2-year-olds who show spontaneous looking to
the correct location on the same task (18) is quite
notable. It is unlikely that differences in motivation are to blame, because neurotypical adults
showed the same bias as typically developingchildren, and the Asperger group exhibited correct anticipatory looking on familiarization trials

0.2
0
-0.2

AS

NT

ratio of correct first lookchildren. Before the main analyses, we confirmed that all the participants showed anticipatory looking toward the correct location during
familiarization trials (19). Written informed consent was obtained from each participant before
the study began. The study was approved by
the University College London Research Ethics
Committee.
As shown in Table 1, the Asperger and neurotypical groups in our study were very similarin age and intelligence quotient (IQ). As no sex
differences were shown in any of our measures,
we pooled results over gender in each group.
We found that the participants with Asperger
syndrome performed at the same level as neurotypical adults on verbally instructed versions ofa variety of standard ToM tests, including thepreviously described Sally-Anne task. There
were no group differences in the composite
ToM score or in the Strange Stories test (bothts < 1.61, both ps > 0.1, t test). All participants
with Asperger syndrome passed the two standard FBTs.

1

*
0.5

0
AS

NT

Fig. 2. (A) Mean (T SEM) DLS (19) and (B) the
ratio of the number of participants who madecorrect first saccades in each group. AS, participants with Asperger syndrome (n = 19); NT,neurotypical participants (n = 17). *P < 0.05; **P <0.01. Dotted lines indicate chance level. Statistical
test used: (A), t test; (B), binominal test.

www.sciencemag.org

REPORTS
when no belief reasoning was required. The current results confirm indirect indications (12–15)
that individuals with Asperger syndrome have apersistent impairment in spontaneous mentalizing and are also consistent with a previous finding (16) that children with autism are more likely
to give a correct verbal answer than a correct
anticipatory look when asked to infer someone’s
preference.
Although it is plausible that the documented
early emerging spontaneous capacity to mentalize(17, 18) is a prerequisite for the later ability tojustify behavior in terms of mental states in verbal tasks, our results suggest that this need notnecessarily be the case. Instead, our data raise thesurprising possibility that an early developing
form of the cognitive ability to mentalize, evident
in spontaneous looking behavior, is not a necessary precursor of the later developing form ofmental-state attribution, which supports explicit
reasoning. The former would require spontaneous encoding of socially relevant information andautomatic online computation of others’ mental
states, whereas the latter could also be achieved
by verbally mediated reasoning prompted by
explicit task structure and instructions.
We suggest that compensatory learning can circumvent neurophysiological limitations, even without removing the original cause of the limitation.

Such compensatory learning might explain theapparent paradox between success on explicit FBTs
and continued difficulty in everyday social interaction for individuals with Asperger syndrome.
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19. Materials and methods are available as supporting
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29. We would like to thank D. Coniston for her invaluable
help in data collection and G. Csibra and C. Frith fortheir helpful discussions. A.S. was supported by an
Economic and Social Research Council (ESRC) Research
Fellowship (RES-063-27-0207), S.W. by a Medical
Research Council of UK (MRC)/ESRC fellowship (PTA
037-27-0107), and U.F. by an MRC grant (G0701484)
and the Aarhus Research Foundation.

Supporting Online Materialwww.sciencemag.org/cgi/content/full/1176170/DC1
Materials and Methods
SOM Text
References
Movies S1 and S2
11 May 2009; accepted 30 June 2009
Published online 16 July 2009;10.1126/science.1176170
Include this information when citing this paper.

14 AUGUST 2009885