Elsevier

NeuroImage

Volume 27, Issue 1, 1 August 2005, Pages 247-252
NeuroImage

Rapid Communication
Taking an “intentional stance” on eye-gaze shifts: A functional neuroimaging study of social perception in children

https://doi.org/10.1016/j.neuroimage.2005.03.027Get rights and content

Abstract

During middle childhood, children develop an increasing understanding of intentions and other social information conveyed through dynamic facial cues such as changes in eye-gaze direction. Recent work in our laboratory has focused on using functional magnetic resonance imaging (fMRI) in adults to map the neural circuitry subserving the visual analysis of others' actions and the intentions underlying these actions. In these studies, the superior temporal sulcus (STS) region has been continually implicated in processing shifts in eye gaze. Further, these studies have indicated that STS activity is modulated by the context within which eye-gaze shifts occur, suggesting that this region is involved in social perception via its role in the analysis of the intentions of observed actions. Still, no studies have investigated the neural circuitry supporting eye-gaze processing in children. We used event-related fMRI to examine brain activity in 7- to 10-year-old healthy children observing an animated virtual actor who shifted her eyes towards either a target object or empty space. Consistent with prior studies in adults, the STS, middle temporal gyrus, and inferior parietal lobule were sensitive to the intentions underlying the stimulus character's eye movements. These findings suggest that the neural circuitry underlying the processing of eye gaze and the detection of intentions conveyed through shifts in eye gaze in children are similar to that found previously in adults. We discuss these findings and potential implications for mapping the neurodevelopment of the social cognition and social perception abnormalities characteristic of autism.

Introduction

From early in ontogeny, infants demonstrate an appreciation of the wealth of information provided by faces (Morton and Johnson, 1991). Faces offer multiple social cues, including the bearer's identity (Bruce and Young, 1986), emotional state (Bassili, 1989, Ekman, 1982), focus of attention (Langton, 2000, Langton et al., 2000), and intentions (Baron-Cohen, 1995, Baron-Cohen et al., 2001). These cues are central to children's cognitive, language, and social development (Wood, 1999) and offer the basis for children's comprehension of others' mental states, a development commonly referred to as theory of mind (Premack and Woodruff, 1978).

Several functional neuroimaging studies have highlighted the role of the superior temporal sulcus (STS) region in processing observed eye movements (Hoffman and Haxby, 2000, Puce et al., 1998, Wicker et al., 1998). Subsequent work has demonstrated that the STS region is sensitive to the social context within which a gaze shift occurs; that is, whether the gaze is perceived to be consistent or inconsistent with the subject's expectation regarding the intention of the person making the eye movement (Pelphrey et al., 2003). In that study, which used a paradigm with adults that was nearly identical to the one used in the present study, a strong effect of context was observed in the right posterior STS region in which observation of gaze shifts away from a target (incongruent shifts) evoked a hemodynamic response (HDR) with extended duration and greater amplitude compared to gaze shifts toward the target (congruent shifts). Additional studies have replicated this finding in the context of reaching-to-grasp sequences (Pelphrey et al., 2004a) and have suggested that the STS region is a component of the neural circuitry supporting the visual analysis of social information conveyed by gaze direction, body movement, and other types of biological motion (Allison et al., 2000, Castelli et al., 2002, Pelphrey et al., 2004b).

In contrast to our knowledge of the role of the STS and other brain regions involved in social perception in adults, very little is known about this circuitry in children. While a handful of fMRI studies have examined the roles of the fusiform gyrus (Passarotti et al., 2003) and the amygdala (McClure et al., 2004, Thomas et al., 2001, Wang et al., 2004) in children, no fMRI studies with children have examined the STS region or its role in processing eye gaze. An evoked response potential study of adults and 4- to 15-year-old children (Taylor et al., 2001) reported a slower maturation of face-related components evoked during processing of upright whole faces as compared to those evoked by the processing of isolated eyes. These findings suggest that the functional development of the STS region may progress more quickly than other face processing regions such as the fusiform gyrus.

Here, we used event-related fMRI to investigate brain regions involved in processing eye gaze and the intentions conveyed by shifts in eye gaze in typically developing 7- to 10-year-old children. During fMRI scanning, children watched as a small checkerboard pattern appeared and flickered in an animated character's visual field (Fig. 1). On congruent (goal-directed) trials, the character shifted her gaze towards the checkerboard (Fig. 1, top panel), confirming the subject's expectations. On incongruent (non-goal-directed) trials, the character shifted her gaze towards empty space (Fig. 1, bottom panel), violating the subject's expectations. We expected to observe gaze-evoked activity in the STS and other brain regions known to be involved in eye-gaze processing in adults. Based on our prior findings using this and similar fMRI paradigms (Pelphrey et al., 2003, Pelphrey et al., 2004a, Pelphrey et al., 2004b), we hypothesized that activity in the STS region evoked by observation of gaze shifts would differ between congruent and incongruent trials, reflecting the ability of typically developing children to link the perception of the gaze shift with its mentalistic significance.

Section snippets

Subjects

Eight (7 females, 1 male) right-handed, healthy, 7- to 10-year-old children [age range 7.1 to 10.3 years (M = 9.22 years)], participated in the study. Prior to participation, we obtained verbal assent from each subject and written consent from parents. Children were screened through parental report for history of neurological complications and/or psychiatric disorders, or current or past use of psychoactive medications. The protocol was approved by the Duke University Medical Center

Eye-gaze-evoked activity

Observation of the congruent and incongruent eye movement sequences activated a network of twelve functional regions of interest comprised of nine anatomical locations and two hemispheres. Statistics for these regions of interest, including centers of activation, MNI coordinates, and voxel counts, are listed in the upper panel of Table 1. As illustrated in Figs. 2A and B, activity elicited by observation of eye-gaze shifts (i.e., the union of the congruent and incongruent conditions) was

Discussion

In this study, we sought to investigate the neural substrates of eye-gaze processing in children and to examine the sensitivity of brain regions involved in processing eye gaze to the intentions underlying shifts in eye gaze. Based on previous findings in adults, we postulated that, in children, a circuit of frontal, temporal, and parietal regions would be involved in processing eye movements. Children viewed two conditions in which an animated virtual character shifted the direction of her

Conclusion

These findings advance previous fMRI studies of social perception and social cognition by demonstrating that the neural substrates subserving eye-gaze processing and detection of the intentions underlying shifts in eye gaze are similar in school-aged children and adults. Results indicated that the STS, middle temporal gyrus, and inferior parietal lobule are sensitive to the intentional nature of eye-gaze shifts. Additionally, the consistency of our results with adult findings highlights the

Acknowledgments

We thank K. Karcher, M. B. Nebel, J. P. Morris, and E. Carter for assistance with several aspects of this research. Our interpretation of the findings benefited greatly from conversations with Dr. Margot Taylor and Dr. Peter Mundy. This research was supported by NIMH grants K01 MH071284-1 and by a grant from the Foundation of Hope for Research and Treatment of Mental Illness. Dr. McCarthy is a V. A. Senior Research Career Scientist.

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