Neural Correlates of Theory-of-Mind Reasoning: An Event-Related Potential Study
Author(s): Mark A. Sabbagh and Marjorie Taylor
Source: Psychological Science, Vol. 11, No. 1 (Jan., 2000), pp. 46-50
Published by: Sage Publications, Inc. on behalf of the Association for Psychological Science
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PSYCHOLOGICALSCIENCE
Research Report
NEURAL CORRELATES OF THEORY-OF-MIND REASONING:
An Event-Related Potential Study
MarkA. Sabbaghand MarjorieTaylor
Universityof Oregon
Abstract- Everydayunderstandingof humanbehavior rests on having a theory of mind- the ability to relate people 's actions to underlying mental states such as beliefs and desires. It has been suggested
that an impairedtheoryof mind may lie at the heart of psychological
disorders that are characterizedby deficits in social understanding,
such as autism.In this study, we employedthe event-relatedpotential
methodologyto index the activity of neural systems that are engaged
during theory-of-mind reasoning in adults. Specifically, neural activity elicited by tasks that requiredthinkingabout mental as compared
with nonmental representations(i.e., beliefs vs. photographs) was
characterizedby afocally enhancedpositivity over leftfrontal areas,
which was diminishedover left parietal areas. Thesefindings provide
an importantperspective on both children's theory-of-mind developmentand the neurobiologyof disordersin which theoryof mindseems
to be impaired.
The presentstudycapitalizedon the matchednatureof the false-belief
and false-photographtasks to investigatethe brainelectrophysiological activity associated with reasoningabout mental versus nonmental
representationsin adults.
Identifyinga brainelectrophysiologicalmarkerfor theory-of-mind
reasoningis importantfor two reasons.First,there is presentlya wide
range of theories regarding the cognitive mechanisms and ratelimiting factors underlyingtheory-of-mindreasoning in young children (see Carruthers & Smith, 1996). Gaining a cognitive
neuroscienceperspectiveon this question could be an importantstep
in constrainingtheorizingandguidingresearchin this interestingarea.
Second, identifyingsuch a markerhas the potentialto provideinsight
into the neurophysiologicalbases of autism. Although the search for
a common neurological substratein autism has been elusive (Minshew & Rattan,1992), severalresearchershave identifieda numberof
brain electrophysiologicalabnormalitiesthat seem to be common in
individuals with autism, such as electroencephalographic(EEG) abManyphilosophers,psychologists,and anthropologistssupportthe normalities at left frontal locations (e.g., Dawson, Klinger, Panagiview thateverydayunderstandingof humanbehaviorrests on a theory otides, &
Lewy, 1995) and abnormalcognitive event-relatedpotential
of mind- an appreciationof how people's behaviors relate to their (ERP)characteristics(i.e., P300; e.g., Lincoln,Courchesne,Harms,&
internalmentalstates, such as beliefs (Wellman, 1990). An important Allen, 1993).
Convergence between the electrophysiologicalcorrecognitive prerequisiteto having a theoryof mind is the ability to think lates of theory-of-mindreasoning in normal adults and the known
aboutmentalstatesas representationsof reality(Perner,1991). Recent
cognitive and electrophysiological characteristicsof autism would
researchsuggests thatthinkingaboutmentalrepresentationsof reality
give insight into the neuropathologyof this developmentaldisorder.
(e.g., beliefs) may be computationallydissociatedfrom thinkingabout
other kinds of representationsof reality (e.g., photographs).For instance, autistic childrentypically fail the standardfalse-belief task in
METHOD
which participantsare asked to reason about a person's mental representationof a particularscene that has become outdated,or false,
Participants
because that scene has changed in his or her absence. Yet, they show
in
tasks
on
structured
strong performance similarly
false-photograph
Twenty-three right-handedcollege students participatedin this
which participantsare asked to recognize that a photographcan be
for pay. Participantswere between the ages of 18 and 42 years
study
outdated if the scene changes after the photographhas been taken
=
There were 12 females and 11 males. All participants
(Leekam & Perner, 1991; Leslie & Thaiss, 1992). For young pre- (median 21).
were native English speakers without history of
that
they
reported
schoolers, performanceon these two tasks is typically not correlated
or neurologicalillness.
psychiatric
significant
(Slaughter,1998). These dissociationsare strikinggiven thatthe falsebelief and false-photographtasks are similar in inferentialstructure,
memory load, and story content;they differ only in the natureof the
ERP Collection
representation.
To account for these dissociations, a numberof researchershave
Electrophysiologicaldata were recorded from the scalp using a
suggested that there may be a distinct neural system that supports 128-channelGeodesic Sensor Net (Tucker, 1993), a networkof 128
reasoningabout mental states and is impairedin the case of autism
Ag/AgCl sponge sensorsknittedinto an elastic geodesic tension struc(Baron-Cohen,1994). A handfulof studies have attemptedto inves- ture. The Sensor Net has an even interelectrodedistance of 2.7 cm,
tigate this questiondirectly(e.g., Fletcheret ah, 1995; Goel, Grafman, and electrode
impedances between 10 and 20 kfl. The EEG was
Sadato, & Hallett, 1995). However, none have used tasks as well
filtered at 0.1 Hz- 100 Hz), digitized at 250 Hz
amplified
(band-pass
matchedas the false-belief and false-photographtasks, thereby leavfor 1,256 ms starting256 ms prior to the onset of the test stimulus.
ing unanswereda numberof questions regardingtheir interpretation.
Single-trialdata were edited with algorithmicartifact-rejectionsoftware that combed the data for evidence of lateral eye movements,
Address correspondenceto Mark Sabbagh, Developmental Psychology, eyeblinks, and muscle artifacts.All participantshad at least 25 arti525 E. UniversityAve., Ann Arbor,MI 48104-1 109; e-mail: sabbagh@umich. fact-free trials per condition. These artifact-freetrials were averaged,
edu.
transformedusing the average-referencemethod (Hjorth, 1982), cor46
Copyright© 2000 AmericanPsychological Society
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VOL. 11, NO. 1, JANUARY 2000
PSYCHOLOGICALSCIENCE
Mark A. Sabbaghand MarjorieTaylor
rected to baseline, and digitally filtered (low-pass filter with 20-Hz whetherthe computer'sanswer was correct(yes/no). The computer's
answer was correct 50% of the time.
cutoff) to reduce environmentalnoise.
Participantswere tested in a sound-attenuatedbooth approximately
50 cm from a computerscreen. An adjustablechin rest ensured that
this distance remained constant and minimized head movement. A
RESULTS
closed-circuitvideo system allowed monitoringof participants'posiand
correct
of
the
Sensor
tion, eye movements,eyeblinks,
placement
There were no significantdifferences in the participants'accuracy
Net throughouteach 1.5-hr session.
for belief versus photo questions (Ms = 94% and 95% correct, respectively), paired t(22) = 1.04, p > .10. Further,there were no
Experimental Task and Procedure
significantdifferencesin the time it took participantsto readthe belief
= 18.79 s and 18.35 s, respecParticipantswere presentedwith 80 short (six-line) narratives,40 stories versus the photo stories (Ms
=
>
.10.
These findings suggest that the
1.54,
t(22)
p
describinga character'sbelief regardingthe location of two objects tively), paired
and 40 describinga characterwho took a photographof two objects. two types of stories were equivalent in reading and comprehension
In both types of stories, the representationswere subsequentlyout- difficulty.
dated when one of the two objects was displaced during the characNonparametricWilcoxon signed-rankstests and factorialanalyses
ter's absence. To ensure that the narratives differed only on the of variance (ANOVAs) were used in concert to characterizedifferrelevantdimension (beliefs vs. photos), each story had both a belief ences in the ERPs associated with beliefs versus photos. The Wiland a photo variant(see Table 1). Both variantsof each story were coxon signed-rankstests were performedfor all time points on all 128
presentedto all participants.The 80 stories were presentedin one of channels (p < .05, two-tailed). To avoid false positives, we adopted
strict criteriawherebydifferences were consideredsignificantonly if
two randomorders.
Narrativeswere presentedline by line and readat the participants' they were (a) maintainedon a single channel for eight continuous
own pace. Participantswere asked to ensure that they comprehended samples(32 ms) and (b) neighboredby at least two otherchannelsthat
each line fully before they moved on to the next. To facilitate good showed a similar patternof activity. Assuming independence,this
comprehensionand ensure that they were completing the task by procedureis associated with a very stringentalpha level (p < 3.9 x
making referenceto the representationsin question, we told partici- 10"1'). Startingat 300 ms poststimulus,ERPs for the belief condition
pants to "makea mental picture"of the events depicted in each line. were more positive than ERPs for the photographconditionat a clusAt the end of each narrative,participantswere asked controlques- ter of four left frontal sensors and less positive than ERPs for the
tions designed to assess their attention to story details and a test photographconditionat a clusterof four left parietalsensors (see Fig.
question about the location of one of the objects according to the 1). These differences were maintainedintermittentlythroughoutthe
character'sbelief or photograph.Questions were presentedword by ERP epoch, and were most clearly recapitulatedat 820 ms poststimuword at a 512-ms interstimulusinterval. Participantsdid not know lus. No differences meeting the significance criteriawere present at
which object (displacedor not displaced)they were going to be asked right-hemispheresites.
aboutuntil the final word of the question (e.g., "Accordingto [Mary/
A series of follow-up 2 (condition) x 2 (hemisphere) repeated
the photo],where is the [object]?"),which servedas the stimulusonset measuresANOVAs were carriedout to furthercharacterizeboth the
for the ERP analysis. ERP data were collected for a 1,500-ms time frontaland the
parietaleffects. Voltages from representativechannels
period,duringwhich participantswere asked to mentallygeneratethe (sites correspondingto 10-20 sites) identified in the nonparametric
answer while remaining fixated on the screen. The computer then
analyses and from their right-hemisphereanalogues (frontal: FP1,
displayeda possible answerto the question,and the participants'task FP2; parietal:P3, P4) were averaged across two different time winwas to press the appropriatekey to indicate, after a 1,000-ms delay, dows: 300-400 ms
(25 samples) and 600-840 ms (60 samples). The
ANOVAs for the frontal sites revealed a significant Condition x
Hemisphereinteractionin both time windows, F(l, 22) = 13.60, p <
Table 1. Examplesof belief and photo stones
.005, for 300-400 ms and F(l, 22) = 9.93, p < .005, for 600-840 ms
(see Fig. 2). Planned means comparisonsindicated that the interacBelief Story
were due to a focal increase in the positivity associated with
tions
Ben put a folder and a clipboardon his desk.
beliefs at FP1 (left frontal)relative to FP2 (rightfrontal)in both time
His friend, Maggie, noticed that he had lots of work to do.
windows, F(l, 22) = 11.22, p < .005, for 300-400 ms and F(l, 22)
Then, Maggie went out for a coffee.
= 10.01, p < .005, for 600-840 ms. There was also a hemispheric
While Maggie was gone, Ben moved the clipboard.
Ben put the clipboardon the bookshelf.
asymmetry(more positive at FP1 thanFP2) for the belief conditionin
He left the folder on his desk.
both time windows, F(l, 22) = 15.14, p < .005, for 300-400 ms and
F(l, 22) = 13.91, p < .005, for 600-840 ms. Contraryto the nonPhoto Story
parametricfindings, the ANOVAs for the parietalsites did not reveal
Ben put a folder and a clipboardon his desk.
significant main effects or interactions.
His friend, Maggie, took a pictureof these things.
To confirm the replicabilityof these findings, we randomlysplit
the
camera
Then, Maggie put
away.
the subject sample into two groups (Group \: n = 12, Group2: n =
After a little while, Ben moved the clipboard.
Ben put the clipboardon the bookshelf.
11) and conducted the same analyses. The analyses for both groups
He left the folder on his desk.
revealeda patternof differencescongruentwith thatof the full-sample
analysis.
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47
PSYCHOLOGICALSCIENCE
Theory of Mind and Event-RelatedPotentials
Fig. 1. Event-relatedpotentials in the photograph(thin lines) and belief (thick lines) conditions, recorded from selected frontal and parietal sites. Gray-shadedregions indicate time
windows in which the condition differences met criteria for statistical significance. Circled
sites showed condition differences at 300-400 ms and at 600-840 ms.
DISCUSSION
The purpose of this study was to characterizethe brain electrophysiology of theory-of-mind reasoning in adults using the falsebelief andfalse-photographtasks in an ERP paradigm.In doing so, we
have providedan importantlink between theory-of-mindabilities and
their neural underpinnings,a link that can play an importantrole in
constrainingresearch and theorizing about theory-of-minddevelopment and disorders(Klein & Kihlstrom,1998). Results indicatedthat
ERPs elicited by these two tasks differed beginning at 300 ms poststimulus:Beliefs were associatedwith an enhancedpositivityover left
frontalsites and a strongernegativityover left parietalsites. Given the
close structuralmatchbetween these two tasks, and the controlanalyses indicating that the two kinds of stories were of equal reading
difficulty, we can be confident that this dissociation indexes activity
that can be attributedto theory-of-mindreasoning.
Both the time course and the spatial distributionof the dissociations are noteworthy.With respectto time course, the dissociationswe
observed in the 300- to 400-ms window and in the 600- to 840-ms
window are thoughtto index the point at which contextual variables
appearin the ERP record(e.g., Chung et al., 1996). It is possible that
the dissociations we observed reflect the processes associated with
integratingmental versus nonmental representationswithin a given
context. With respect to spatial distribution,the focal nature of the
increasedpositivity for beliefs (see Fig. 3) suggests the possibility of
a radiallyorientedgeneratorwithin the left frontallobe. Though this
idea is speculative, the possibility of a left frontal generatoris consistent with two positron emission tomography studies that found
increasedactivationof the left medial frontalgyrus duringtasks that
48
requiredsocial cognitive reasoning(Fletcheret al., 1995; Goel et al.,
1995).
Implications for Theories of Theory of Mind
Executivefunction and inhibitorycontrol
Recent studies have suggested that performanceon false-belief
tasks hinges on havingadequateinhibitorycontrol(Carlson,Moses, &
Hix, 1998; Ozonoff, Pennington, & Rogers, 1991). We doubt that
inhibitory-controldifferences alone can accountfor the observeddifferences between false-belief and false-photographtasks because the
two tasks are well matched for inhibitorydemands. In addition,the
extended time course over which the ERP differences were maintained is inconsistentwith the time course of brain activationshown
in previous ERP studies designed to investigate inhibitory control
moredirectly(Keifer,Marzinzik,Weisbrod,Scherg,& Spitzer, 1998).
Subtle task differences
Despite the fact that the belief and photographtasks were structurally well matched, it is possible that they imposed different cognitive demands. For example, beliefs differ from photographsin the
explicitness of their origins. A photographis an explicitly made representation:The photographis taken and the scene is represented.In
contrast,understandingthata person's perceptionof a scene resultsin
a belief about that scene requiresan inference (Wimmer,Hogrefe, &
Perner, 1988). A second difference between beliefs and photographs
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PSYCHOLOGICALSCIENCE
Mark A. Sabbaghand MarjorieTaylor
Fig. 3. Three-dimensionalinterpolationsof the scalp electrical activity recordedat 820 ms poststimulus.The interpolationswere created
using the spherical splines method (Perrin, Pernier, Bertrand, &
Echallier, 1989).
of the ERP differentiationscast doubton the idea thatreasoningabout
mentalrepresentationsis automatic.Nevertheless,it remainspossible
that there is a specialized region of cortex responsible for thinking
about mental representations.This localization proposalis not necessarily inconsistent with the suggestion that the difference can be attributedto more general mental operations(Karmiloff-Smith,1992).
Fig. 2. Mean amplitudeof evoked potentialsrecordedfrom selected
frontal sites in the photograph and belief conditions. Results are
shown separatelyfor two time windows: 300-400 ms poststimulus(a)
and 600-840 ms poststimulus(b).
Implications for Autism
Identifying a neurophysiologicalmarkerfor theory-of-mindreasoning has potentially important implications for considering the
is that only beliefs require integratingpropositional contents with
neurobiologicalbases of autism.Lincoln et al. (1993) have found that
propositionalattitudes (Perner, 1991). That is, a belief involves a individualswith autism have a greatly reducedP300 (or P3) compocommitmentto a representation(i.e., thinkingthat a situationis true), nent in
response to novel stimuli in the standardoddball paradigm.
andnotjust a representationitself (i.e., photographof a past situation).
Although it is difficult to identify strong cognitive similarities beBoth of these observations suggest that reasoning about beliefs re- tween the oddball
paradigmand the methodsused in the presentstudy,
quiresan additionalinferentialor integrativestep that is not required it is interestingto note that cognitive processes engaging at 300 ms
when thinkingabout photos. It is possible that the left frontaldifferpoststimulusseem to be especially importantfor consideringspecifiences reflect this cognitive disparity (Grafman,Holyoak, & Boiler,
cally mentalrepresentations,and are known to be impairedin autism.
1995).
A second aspect of our findings that can be linked with known
deficits in autism concerns the location of the main efneurological
"
"module
In
standard
-mind
fects.
neuropsychiatrictests, autistic individuals show
Theory-of
A numberof researchershave suggestedthatthe mentaloperations greaterimpairmenton items designed to tap left- as opposed to rightrequiredfor thinkingaboutmentalrepresentationsmay be carriedout hemisphere dysfunction (Dawson, 1983). In addition, autistic indiin an automaticand modularizedfashion (Baron-Cohen,1994; Broth- viduals have demonstratedreducedEEG power over frontalelectrode
ers & Ring, 1992). However, the late onset and extended time course sites, and this effect is more pronouncedover the left hemisphere
49
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PSYCHOLOGICALSCIENCE
Theory of Mind and Event-RelatedPotentials
(Dawson et al., 1995). The present findings linking theory-of-mind
reasoningwith regions in the left frontallobe suggest that these characteristicneurophysiologicalabnormalitiesseen in autisticindividuals
may be relatedto their social cognitive deficits.
Acknowledgments- This researchwas supportedby a National Science
FoundationGraduateFellowship to MarkSabbagh,and by a McDonnellPew Investigator-InitiatedCognitive Neuroscience Award to Marjorie
Taylor. Special thanks go to BrandonPol for his assistance in data collection, andto Dare Baldwin,Ben Clegg, Gregg DiGirolamo,Bill Gehring,
Louis Moses, Helen Neville, and Don Tuckerfor theirassistanceat various
stages of study design and manuscriptpreparation.
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