Elsevier

NeuroImage

Volume 36, Issue 3, 1 July 2007, Pages 1004-1014
NeuroImage

The extrastriate cortex distinguishes between the consequences of one's own and others' behavior

https://doi.org/10.1016/j.neuroimage.2007.03.030Get rights and content

Abstract

The extrastriate body area (EBA) is traditionally considered a category-selective region for the visual processing of static images of the human body. Recent evidence challenges this view by showing motor-related modulations of EBA activity during self-generated movements. Here, we used functional MRI to investigate whether the EBA distinguishes self- from other-generated movements, a prerequisite for the sense of agency. Subjects performed joystick movements while the visual feedback was manipulated on half of the trials. The EBA was more active when the visual feedback was incongruent to the subjects' own executed movements. Furthermore, during correct feedback evaluation, the EBA showed enhanced functional connectivity to posterior parietal cortex, which has repeatedly been implicated in the detection of sensorimotor incongruence and the sense of agency. Our results suggest that the EBA represents the human body in a more integrative and dynamic manner, being able to detect an incongruence of internal body or action representations and external visual signals. In this way, the EBA might be able to support the disentangling of one's own behavior from another's.

Introduction

The extrastriate body area (EBA), a region in occipital–temporal cortex, has been described as a category-selective region that responds predominantly to static pictures of the human body and not to pictures of other stimulus categories such as objects (e.g., a spoon, a brush, etc.) (Downing et al., 2001, Downing et al., 2006b, Urgesi et al., 2004, Peelen and Downing, 2005, Saxe et al., 2006, Peelen et al., 2006, Spiridon et al., 2006). This domain-specificity hypothesis of EBA function has been recently challenged by a demonstration of increased EBA activity for self-generated pointing movements, independent of the perception of the limb (Astafiev et al., 2004, Astafiev et al., 2005; cf. Peelen and Dowing, 2005), suggesting that EBA's function is not purely perceptive but extends into the motor domain. Other authors have made similar suggestions for activation in coordinates matching previously published EBA coordinates or for the overlapping/adjacent motion-specific area hMT+ (Schenk et al., 2000, Oreja-Guevara et al., 2004, Hamilton et al., 2005, Jackson et al., 2006).

The findings of Astafiev et al., 2004, Astafiev et al., 2005 suggested an encoding of internal, action-related signals such as central motor and proprioceptive feedback signals within the EBA. This opened the possibility that the EBA is also involved in distinguishing whether actions are caused by oneself or by another person. This self–other distinction is a prerequisite for the sense of agency, the ability to recognize oneself as the originator or initiator of one's own behavior (Gallagher, 2000). This internal –and not necessarily conscious– comparison between efferent signals arising from action preparation and reafferent sensory signals arising from action execution and observation or, in other words, the comparison between predicted and actual sensory outcome (Wolpert et al., 1995, Blakemore et al., 1998, Blakemore and Frith, 2003), has been proposed as one important mechanism for the sense of agency. This influential account has triggered a line of experiments that manipulated reafferent sensory, particularly visual, signals to create a mismatch between action intentions, predictions, and actual outcomes.

Using functional magnetic resonance imaging (fMRI), we sought to evaluate a contribution of the EBA to the sense of agency by detecting mismatches between internal and external action- or feedback-related signals. We used a task in which subjects performed simple joystick movements while the visual feedback of their movements was manipulated in half of the trials. On such trials, subjects were told they would see the visual feedback to movements carried out by the experimenter. Our task was based on a previously published experimental manipulation (e.g., Nielsen, 1963, Farrer and Frith, 2002, Farrer et al., 2003, Fourneret and Jeannerod, 1998, Franck et al., 2001, Knoblich and Kircher, 2004, MacDonald and Paus, 2003), which creates a mismatch between the executed movement and its observed, visual outcome. We used an independent functional localizer to identify the EBA individually for each subject, and then examined activity in the EBA during the joystick task. Importantly, there were no images of body parts or other complex visual stimuli during the task, so any differences in activity in EBA could not be attributed to visual perception of the human body or other complex visual images.

It is important to note a discrepancy with recent research on the EBA: some propose it is most active during self-generated movements in the absence of visual feedback (Astafiev et al., 2004, Astafiev et al., 2005, Jeannerod, 2004), whereas other findings suggest that the EBA is most active during viewing of other people's bodies (Chan et al., 2004, Saxe et al., 2006). We suggest that the EBA detects violations of internal body or action representations and external visual signals (in accordance with Avikainen et al., 2003, Chan et al., 2004, Saxe et al., 2006), a mechanism that the sense of agency may rely on when actions are identified as self-generated or generated by other agents. Such a capacity would go beyond a merely visual and static representation of the human body within the EBA and suggest the need to reconsider the function of the EBA.

Section snippets

Subjects

Nineteen healthy male volunteers with no significant psychiatric or neurological history were studied. Data from one subject were excluded because of poor task performance, from two subjects because of head movement, and from two subjects because of image artifacts. Thus, data from the remaining 14 subjects (mean age 25.6 years; range 19–33 years) are reported. All subjects were right-handed, as assessed by the Edinburgh Handedness Inventory (Oldfield, 1971). Informed consent was obtained

Behavioral results

Forty-six ± 1% of all trials were congruent feedback correctly judged as self-generated (“congruent-self”; C-S); 5 ± 1% of trials were congruent feedback incorrectly judged as other- (i.e., experimenter) generated (“congruent-other”; C-O); 24 ± 3% of trials were incongruent feedback incorrectly judged as self-generated (“incongruent-self”; I-S); and 26 ± 3% of trials were incongruent feedback correctly judged as other-generated (“incongruent-other”; I-O; Fig. 2). The conditions differed significantly

Discussion

Until recently, the EBA has been considered a selective, category-specific area for the static visual representation of the human body (Downing et al., 2001, Downing et al., 2006b, Peelen and Downing, 2005, Peelen et al., 2006). The finding that movement of one's own limbs, without any vision of the movement or the limb, also modulates activity within the EBA challenged this view suggesting that the EBA is not only responsive to visual signals but also to endogenous signals during motor

Acknowledgments

N.D. was supported by a grant from the Volkswagen Foundation (AZ II/80 594 awarded to A.N.). G.R.F. was supported by the German Research Foundation (KFO-112). The authors thank B. Elghahwagi and G. Oefler for scanning assistance, T. Stoecker, O. Haumann, and C. Grefkes for help with installing the MRI-joystick. Furthermore, we thank P. Downing and M. Peelen for the EBA localizer stimuli and helpful comments.

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