neural correlates of theory-of-mind reasoning: an event ......neural correlates of theory-of-mind...

Neural Correlates of Theory-of-Mind Reasoning: An Event-Related Potential StudyAuthor(s): Mark A. Sabbagh and Marjorie TaylorSource: Psychological Science, Vol. 11, No. 1 (Jan., 2000), pp. 46-50Published by: Sage Publications, Inc. on behalf of the Association for Psychological ScienceStable URL: http://www.jstor.org/stable/40063494 .

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NEURAL CORRELATES OF THEORY-OF-MIND REASONING: An Event-Related Potential Study

Mark A. Sabbagh and Marjorie Taylor

PSYCHOLOGICAL SCIENCE

Research Report

University of Oregon

Abstract - Everyday understanding of human behavior 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 impaired theory of mind may lie at the heart of psychological disorders that are characterized by deficits in social understanding, such as autism. In this study, we employed the event-related potential methodology to index the activity of neural systems that are engaged during theory -of -mind reasoning in adults. Specifically, neural activity elicited by tasks that required thinking about mental as compared with nonmental representations (i.e., beliefs vs. photographs) was characterized by afocally enhanced positivity over left frontal areas, which was diminished over left parietal areas. These findings provide an important perspective on both children 's theory -of -mind development and the neurobiology of disorders in which theory of mind seems to be impaired.

Many philosophers, psychologists, and anthropologists support the view that everyday understanding of human behavior rests on a theory of mind - an appreciation of how people's behaviors relate to their internal mental states, such as beliefs (Wellman, 1990). An important cognitive prerequisite to having a theory of mind is the ability to think about mental states as representations of reality (Perner, 1991). Recent research suggests that thinking about mental representations of reality (e.g., beliefs) may be computationally dissociated from thinking about other kinds of representations of reality (e.g., photographs). For in- stance, autistic children typically fail the standard false-belief task in which participants are asked to reason about a person's mental representation of a particular scene that has become outdated, or false, because that scene has changed in his or her absence. Yet, they show strong performance on similarly structured false-photograph tasks in which participants are asked to recognize that a photograph can be outdated if the scene changes after the photograph has been taken (Leekam & Perner, 1991; Leslie & Thaiss, 1992). For young pre- schoolers, performance on these two tasks is typically not correlated (Slaughter, 1998). These dissociations are striking given that the false- belief and false-photograph tasks are similar in inferential structure, memory load, and story content; they differ only in the nature of the representation.

To account for these dissociations, a number of researchers have suggested that there may be a distinct neural system that supports reasoning about mental states and is impaired in the case of autism (Baron-Cohen, 1994). A handful of studies have attempted to investigate this question directly (e.g., Fletcher et ah, 1995; Goel, Grafman, Sadato, & Hallett, 1995). However, none have used tasks as well matched as the false-belief and false-photograph tasks, thereby leav- ing unanswered a number of questions regarding their interpretation.

The present study capitalized on the matched nature of the false-belief and false-photograph tasks to investigate the brain electrophysiological activity associated with reasoning about mental versus nonmental

representations in adults. Identifying a brain electrophysiological marker for theory-of-mind

reasoning is important for two reasons. First, there is presently a wide

range of theories regarding the cognitive mechanisms and rate-

limiting factors underlying theory-of-mind reasoning in young children (see Carruthers & Smith, 1996). Gaining a cognitive neuroscience perspective on this question could be an important step in constraining theorizing and guiding research in this interesting area. Second, identifying such a marker has the potential to provide insight into the neurophysiological bases of autism. Although the search for a common neurological substrate in autism has been elusive (Min- shew & Rattan, 1992), several researchers have identified a number of brain electrophysiological abnormalities that seem to be common in individuals with autism, such as electroencephalographic (EEG) abnormalities at left frontal locations (e.g., Dawson, Klinger, Panagi- otides, & Lewy, 1995) and abnormal cognitive event-related potential (ERP) characteristics (i.e., P300; e.g., Lincoln, Courchesne, Harms, & Allen, 1993). Convergence between the electrophysiological correlates of theory-of-mind reasoning in normal adults and the known

cognitive and electrophysiological characteristics of autism would

give insight into the neuropathology of this developmental disorder.

METHOD

Participants

Twenty-three right-handed college students participated in this

study for pay. Participants were between the ages of 1 8 and 42 years (median = 21). There were 12 females and 1 1 males. All participants reported that they were native English speakers without history of

significant psychiatric or neurological illness.

ERP Collection

Electrophysiological data were recorded from the scalp using a 128-channel Geodesic Sensor Net (Tucker, 1993), a network of 128

Ag/AgCl sponge sensors knitted into an elastic geodesic tension structure. The Sensor Net has an even interelectrode distance of 2.7 cm, and electrode impedances between 10 and 20 kfl. The EEG was

amplified (band-pass filtered at 0.1 Hz- 100 Hz), digitized at 250 Hz for 1,256 ms starting 256 ms prior to the onset of the test stimulus.

Single-trial data were edited with algorithmic artifact-rejection soft- ware that combed the data for evidence of lateral eye movements, eyeblinks, and muscle artifacts. All participants had at least 25 artifact-free trials per condition. These artifact-free trials were averaged, transformed using the average-reference method (Hjorth, 1982), cor-

Address correspondence to Mark Sabbagh, Developmental Psychology, 525 E. University Ave., Ann Arbor, MI 48104-1 109; e-mail: sabbagh @umich. edu.

46 Copyright © 2000 American Psychological Society VOL. 1 1, NO. 1, JANUARY 2000





rected to baseline, and digitally filtered (low-pass filter with 20-Hz cutoff) to reduce environmental noise.

Participants were tested in a sound-attenuated booth approximately 50 cm from a computer screen. An adjustable chin rest ensured that this distance remained constant and minimized head movement. A closed-circuit video system allowed monitoring of participants' posi- tion, eye movements, eyeblinks, and correct placement of the Sensor Net throughout each 1 .5-hr session.

Experimental Task and Procedure

Participants were presented with 80 short (six-line) narratives, 40

describing a character's belief regarding the location of two objects and 40 describing a character who took a photograph of two objects. In both types of stories, the representations were subsequently outdated when one of the two objects was displaced during the character's absence. To ensure that the narratives differed only on the relevant dimension (beliefs vs. photos), each story had both a belief and a photo variant (see Table 1 ). Both variants of each story were

presented to all participants. The 80 stories were presented in one of two random orders.

Narratives were presented line by line and read at the participants' own pace. Participants were asked to ensure that they comprehended each line fully before they moved on to the next. To facilitate good comprehension and ensure that they were completing the task by making reference to the representations in question, we told participants to "make a mental picture" of the events depicted in each line.

At the end of each narrative, participants were asked control questions designed to assess their attention to story details and a test

question about the location of one of the objects according to the character's belief or photograph. Questions were presented word by word at a 512-ms interstimulus interval. Participants did not know which object (displaced or not displaced) they were going to be asked about until the final word of the question (e.g., "According to [Mary/ the photo], where is the [object]?"), which served as the stimulus onset for the ERP analysis. ERP data were collected for a 1,500-ms time

period, during which participants were asked to mentally generate the answer while remaining fixated on the screen. The computer then

displayed a possible answer to the question, and the participants' task was to press the appropriate key to indicate, after a 1 ,000-ms delay,

Table 1. Examples of belief and photo stones

Belief Story Ben put a folder and a clipboard on his desk.

His friend, Maggie, noticed that he had lots of work to do. Then, Maggie went out for a coffee.

While Maggie was gone, Ben moved the clipboard. Ben put the clipboard on the bookshelf.

He left the folder on his desk.

Photo Story Ben put a folder and a clipboard on his desk.

His friend, Maggie, took a picture of these things. Then, Maggie put the camera away.

After a little while, Ben moved the clipboard. Ben put the clipboard on the bookshelf.

He left the folder on his desk.

whether the computer's answer was correct (yes/no). The computer's answer was correct 50% of the time.

RESULTS

There were no significant differences in the participants' accuracy for belief versus photo questions (Ms = 94% and 95% correct, re- spectively), paired t(22) = 1.04, p > .10. Further, there were no significant differences in the time it took participants to read the belief stories versus the photo stories (Ms = 18.79 s and 18.35 s, respec- tively), paired t(22) = 1.54, p > .10. These findings suggest that the two types of stories were equivalent in reading and comprehension difficulty.

Nonparametric Wilcoxon signed-ranks tests and factorial analyses of variance (ANOVAs) were used in concert to characterize differences in the ERPs associated with beliefs versus photos. The Wil- coxon signed-ranks tests were performed for all time points on all 1 28 channels (p < .05, two-tailed). To avoid false positives, we adopted strict criteria whereby differences were considered significant only if they were (a) maintained on a single channel for eight continuous samples (32 ms) and (b) neighbored by at least two other channels that showed a similar pattern of activity. Assuming independence, this procedure is associated with a very stringent alpha level (p < 3.9 x 10"1 '). Starting at 300 ms poststimulus, ERPs for the belief condition were more positive than ERPs for the photograph condition at a cluster of four left frontal sensors and less positive than ERPs for the

photograph condition at a cluster of four left parietal sensors (see Fig. 1). These differences were maintained intermittently throughout the ERP epoch, and were most clearly recapitulated at 820 ms poststimulus. No differences meeting the significance criteria were present at

right-hemisphere sites. A series of follow-up 2 (condition) x 2 (hemisphere) repeated

measures ANOVAs were carried out to further characterize both the frontal and the parietal effects. Voltages from representative channels (sites corresponding to 10-20 sites) identified in the nonparametric analyses and from their right-hemisphere analogues (frontal: FP1, FP2; parietal: P3, P4) were averaged across two different time windows: 300-400 ms (25 samples) and 600-840 ms (60 samples). The ANOVAs for the frontal sites revealed a significant Condition x

Hemisphere interaction in both time windows, F(l, 22) = 13.60, p < .005, for 300-400 ms and F(l, 22) = 9.93, p < .005, for 600-840 ms (see Fig. 2). Planned means comparisons indicated that the interactions were due to a focal increase in the positivity associated with beliefs at FP1 (left frontal) relative to FP2 (right frontal) in both time windows, F(l, 22) = 1 1.22, p < .005, for 300-400 ms and F(l, 22) = 10.01, p < .005, for 600-840 ms. There was also a hemispheric asymmetry (more positive at FP1 than FP2) for the belief condition in 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. Contrary to the non-

parametric findings, the ANOVAs for the parietal sites did not reveal

significant main effects or interactions. To confirm the replicability of these findings, we randomly split

the subject sample into two groups (Group \: n = 12, Group 2: n =

1 1) and conducted the same analyses. The analyses for both groups revealed a pattern of differences congruent with that of the full-sample analysis.

VOL. 1 1, NO. 1, JANUARY 2000 47




Theory of Mind and Event-Related Potentials

Fig. 1. Event-related potentials in the photograph (thin lines) and belief (thick lines) conditions, recorded from selected frontal and parietal sites. Gray-shaded regions 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 characterize the brain electro- physiology of theory-of-mind reasoning in adults using the false- belief and false-photograph tasks in an ERP paradigm. In doing so, we have provided an important link between theory-of-mind abilities and their neural underpinnings, a link that can play an important role in constraining research and theorizing about theory-of-mind development and disorders (Klein & Kihlstrom, 1998). Results indicated that ERPs elicited by these two tasks differed beginning at 300 ms poststimulus: Beliefs were associated with an enhanced positivity over left frontal sites and a stronger negativity over left parietal sites. Given the close structural match between these two tasks, and the control analyses indicating that the two kinds of stories were of equal reading difficulty, we can be confident that this dissociation indexes activity that can be attributed to theory-of-mind reasoning.

Both the time course and the spatial distribution of the dissociations are noteworthy. With respect to time course, the dissociations we observed in the 300- to 400-ms window and in the 600- to 840-ms window are thought to index the point at which contextual variables appear in the ERP record (e.g., Chung et al., 1996). It is possible that the dissociations we observed reflect the processes associated with integrating mental versus nonmental representations within a given context. With respect to spatial distribution, the focal nature of the increased positivity for beliefs (see Fig. 3) suggests the possibility of a radially oriented generator within the left frontal lobe. Though this idea is speculative, the possibility of a left frontal generator is con- sistent with two positron emission tomography studies that found increased activation of the left medial frontal gyrus during tasks that

required social cognitive reasoning (Fletcher et al., 1995; Goel et al., 1995).

Implications for Theories of Theory of Mind

Executive function and inhibitory control Recent studies have suggested that performance on false-belief

tasks hinges on having adequate inhibitory control (Carlson, Moses, & Hix, 1998; Ozonoff, Pennington, & Rogers, 1991). We doubt that

inhibitory-control differences alone can account for the observed differences between false-belief and false-photograph tasks because the two tasks are well matched for inhibitory demands. In addition, the extended time course over which the ERP differences were maintained is inconsistent with the time course of brain activation shown in previous ERP studies designed to investigate inhibitory control more directly (Keifer, Marzinzik, Weisbrod, Scherg, & Spitzer, 1998).

Subtle task differences Despite the fact that the belief and photograph tasks were struc-

turally well matched, it is possible that they imposed different cognitive demands. For example, beliefs differ from photographs in the

explicitness of their origins. A photograph is an explicitly made representation: The photograph is taken and the scene is represented. In contrast, understanding that a person's perception of a scene results in a belief about that scene requires an inference (Wimmer, Hogrefe, & Perner, 1988). A second difference between beliefs and photographs

48 VOL. 1 1, NO. 1, JANUARY 2000





Fig. 2. Mean amplitude of evoked potentials recorded from selected frontal sites in the photograph and belief conditions. Results are shown separately for two time windows: 300-400 ms poststimulus (a) and 600-840 ms poststimulus (b).

is that only beliefs require integrating propositional contents with

propositional attitudes (Perner, 1991). That is, a belief involves a commitment to a representation (i.e., thinking that a situation is true), and not just a representation itself (i.e., photograph of a past situation). Both of these observations suggest that reasoning about beliefs re-

quires an additional inferential or integrative step that is not required when thinking about photos. It is possible that the left frontal differences reflect this cognitive disparity (Grafman, Holyoak, & Boiler, 1995).

Theory -of -mind "module "

A number of researchers have suggested that the mental operations required for thinking about mental representations may be carried out in an automatic and modularized fashion (Baron-Cohen, 1994; Broth- ers & Ring, 1992). However, the late onset and extended time course

Fig. 3. Three-dimensional interpolations of the scalp electrical activity recorded at 820 ms poststimulus. The interpolations were created using the spherical splines method (Perrin, Pernier, Bertrand, & Echallier, 1989).

of the ERP differentiations cast doubt on the idea that reasoning about mental representations is automatic. Nevertheless, it remains possible that there is a specialized region of cortex responsible for thinking about mental representations. This localization proposal is not neces-

sarily inconsistent with the suggestion that the difference can be attributed to more general mental operations (Karmiloff-Smith, 1992).

Implications for Autism

Identifying a neurophysiological marker for theory-of-mind rea-

soning has potentially important implications for considering the

neurobiological bases of autism. Lincoln et al. (1993) have found that individuals with autism have a greatly reduced P300 (or P3) compo- nent in response to novel stimuli in the standard oddball paradigm. Although it is difficult to identify strong cognitive similarities between the oddball paradigm and the methods used in the present study, it is interesting to note that cognitive processes engaging at 300 ms

poststimulus seem to be especially important for considering specifically mental representations, and are known to be impaired in autism.

A second aspect of our findings that can be linked with known

neurological deficits in autism concerns the location of the main effects. In standard neuropsychiatric tests, autistic individuals show

greater impairment on items designed to tap left- as opposed to right- hemisphere dysfunction (Dawson, 1983). In addition, autistic individuals have demonstrated reduced EEG power over frontal electrode sites, and this effect is more pronounced over the left hemisphere

VOL. 1 1, NO. 1, JANUARY 2000 49




Theory of Mind and Event-Related Potentials

(Dawson et al., 1995). The present findings linking theory-of-mind reasoning with regions in the left frontal lobe suggest that these char- acteristic neurophysiological abnormalities seen in autistic individuals may be related to their social cognitive deficits.

Acknowledgments - This research was supported by a National Science Foundation Graduate Fellowship to Mark Sabbagh, and by a McDonnell- Pew Investigator-Initiated Cognitive Neuroscience Award to Marjorie Taylor. Special thanks go to Brandon Pol for his assistance in data collection, and to Dare Baldwin, Ben Clegg, Gregg DiGirolamo, Bill Gehring, Louis Moses, Helen Neville, and Don Tucker for their assistance at various stages of study design and manuscript preparation.

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(Received 1 1/30/98; Accepted 2/2/99)

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