Elsevier

NeuroImage

Volume 21, Issue 2, February 2004, Pages 744-750
NeuroImage

Inferring false beliefs from the actions of oneself and others: an fMRI study

https://doi.org/10.1016/S1053-8119(03)00665-7Get rights and content

Abstract

The ability to make judgments about mental states is critical to social interactions. Simulation theory suggests that the observer covertly mimics the activity of the observed person, leading to shared states of mind between the observer and the person observed. We tested this hypothesis by investigating the neural networks activated while subjects watched videos of themselves and of others lifting a box, and judged the beliefs of the actors about the weight of the box. A parietal premotor circuit was recruited during action perception, and the activity started earlier when making judgments about one's own actions as opposed to those of others. This earlier activity in action-related structures can be explained by simulation theory on the basis that when one observes one's own actions, there is a closer match between the simulated and perceived action than there is when one observes the actions of others. When the observers judged the actions to reflect a false belief, there was activation in the superior temporal sulcus, orbitofrontal, paracingulate cortex and cerebellum. We suggest that this reflects a mismatch between the perceived action and the predicted action's outcomes derived from simulation.

Introduction

The ability to make judgments about mental states is critical to social interactions. We are able to perceive and predict other people's intentions from their nonverbal behavior. It is suggested that we understand other people's behaviors by simulation Decety and Grèzes, 1999, Gallese and Goldman, 1998, Jeannerod, 1994, Wolpert et al., 2003, particularly in cases where the information available is not easily encoded into language (Adolphs, 1999). The assumption is that when we observe others, we mentally simulate the actions that we see.

There is behavioral evidence that the action representation system contributes to the perception of actions Knoblich and Prinz, 2001, Liberman and Mattingly, 1985, Orliaguet et al., 1997, Runeson and Frykholm, 1983, Shiffrar and Freyd, 1993, Viviani and Stucchi, 1992, and this idea has found recent support from neurophysiological data, both from cell recording in monkeys and neuroimaging studies in humans Decety and Grèzes, 1999, Gallese et al., 1996, Rizzolatti et al., 1996. In the macaque monkey brain, a class of neurons called “mirror” neurons was discovered both in the parietal and in the premotor cortex that discharge not only when the monkey performed an action but also when observing the experimenter or another monkey performing the same action di Pellegrino et al., 1992, Fogassi et al., 1998, Gallese et al., 1996. Similarly, in humans, the parietal and the premotor cortex have been found to be activated during action observation Buccino et al., 2001, Decety et al., 1997, Grafton et al., 1996, Grèzes and Decety, 2001, Rizzolatti et al., 1996. Those results suggested that action observation automatically triggers action simulation, a mechanism that could be at the basis of action understanding Adolphs, 2003, Decety and Grèzes, 1999, Gallese, 2003, Jeannerod, 1994, Rizzolatti et al., 2001.

However, humans are not only able to recognize actions from observation, but can also predict and infer underlying causes, intentions and beliefs from the behavior of others. To do so, the information that is directly available consists mostly of the movements of the agent in space and time in the physical or social environment (Barresi and Moore, 1996). The present study explores the neural basis of everyday human competence to make judgments about mental states through the observation of the nonverbal behavior of other people, and aims to clarify to what extent this ability relies on simulation. We scanned subjects, using event-related fMRI, while they viewed actions being performed on video. We consider two issues.

First, it has been shown that observers can make judgments from kinematic patterns (point-lights displays) about the expectation of subjects when picking up boxes of different weights. Specifically, they can distinguish whether the actors have been deceived or not about the weight of the box (Runeson and Frykholm, 1983). In the present study, we therefore presented videos of actors picking up boxes. When preparing these videos, on some trials the actors were correctly informed of the weight of the box and therefore had a correct expectation, whereas on other trials the actors had been misinformed and therefore had an incorrect expectation. We required the subjects to judge whether the actors had a true or false expectation. By comparing these trial types, we aimed to identify the neural circuits that are involved in the attribution of mental states from the observation of behavior.

Second, it has been demonstrated that subjects can recognize kinematic displays of self-generated drawings and handwriting strokes as being their own, and are better at predicting the end-point of an action that is their own than an action that is performed by others Knoblich and Prinz, 2001, Knoblich et al., 2002. Based on the assumption that both action production and action perception are driven by the representation of the outcomes of the action Hommel et al., 2001, Prinz, 1997, it has been proposed that when one perceives one's own actions, there is a closer match between the predicted and actual outcomes of the action than there is when we perceive the action of others (Knoblich and Prinz, 2001). In the present study, we therefore compared the perception of one's own actions and those of others. Unlike others studies, in the present experiment, subjects were not required to explicitly take a first-person or third-person perspective (Ruby and Decety, 2001) or to make judgment about whether an action was performed by themselves or by others (Farrer and Frith, 2002). The task was to infer mental states through the observation of actions. If simulation subserves the ability to attribute mental states through action observation, we predicted differences within the motor system for the comparison between the perception of one's own actions and those of others.

Section snippets

Subjects

Six subjects (four men and two women; range: 25–39 years) with no neurological or psychiatric history participated in the imaging study. All gave informed consent according to procedures approved by the Joint Ethics Committee of the National Hospital for Neurology and Neurosurgery (UCLH NHS Trust) and Institute of Neurology (UCL).

Stimuli

Eight actors (four men and four women) were videotaped with over 50 trials of lifting and carrying a box of varying weights (1, 6, 12 or 18 kg). Each recorded act

Behavioral results

Subjects were able to correctly detect the expectation of the actors from their nonverbal behaviors and were significantly above chance (d′ = 0.78, t test P = 0.025). Subjects tended to be less accurate in detecting when they have been deceived (d′ = 0.63) than when the others were deceived (d′ = 0.99), but the difference in the d' measures for judgements about one's own actions and of others was not significant (paired t test, P = 0.288). The ANOVAs revealed a significant main effect of action

Discussion

This study explores the neural basis of everyday human competence in predicting and explaining human behavior, including the capacity to understand the mental states of others through the observation of their nonverbal behavior. One possible explanation of this competence is given by simulation theory according to which human beings are able to attribute mental states to others by using the resource of their own behavior control system. The theory is that to adopt the perspective of others, we

Inferring false vs. correct expectation

It is suggested that by mental simulation, subjects are able to make predictions concerning the perceived action and compare the predicted and observed outcomes (Wolpert et al., 2003). This allows the observer to draw an inference concerning the mental states of the actor. In the present experiment, the subjects were instructed to decide whether the action kinematics of the actors while lifting a box reflected a correct or a false expectation about the weight of the box. When contrasting the

Conclusions

The aim of this experiment was to specifically examine the neural mechanisms that are involved in making judgements about mental states from nonverbal behavior, and to determine to what extent simulation subserves this ability. In the present experiment, the subjects made judgements about the expectations of the actor, where the video either showed their own actions or those of others. We found activations in the parietal and premotor cortex which we relate to the simulation of the observed

Acknowledgements

We are grateful for the assistance of the radiographers. This work was supported by a EU Fifth Framework Program (Contract No. QLG3-CT-2002-00746) and by the Wellcome Trust.

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