Abstract

The eyes convey a wealth of information in social interactions. This information is analyzed by multiple brain networks, which we identified using functional magnetic resonance imaging (MRI). Subjects attempted to detect a particular directional cue provided either by gaze changes on an image of a face or by an arrow presented alone or by an arrow superimposed on the face. Another control condition was included in which the eyes moved without providing meaningful directional information. Activation of the superior temporal sulcus accompanied extracting directional information from gaze relative to directional information from an arrow and relative to eye motion without relevant directional information. Such selectivity for gaze processing was not observed in face-responsive fusiform regions. Brain activations were also investigated while subjects viewed the same face but attempted to detect when the eyes gazed directly at them. Most notably, amygdala activation was greater during periods when direct gaze never occurred than during periods when direct gaze occurred on 40% of the trials. In summary, our results suggest that increases in neural processing in the amygdala facilitate the analysis of gaze cues when a person is actively monitoring for emotional gaze events, whereas increases in neural processing in the superior temporal sulcus support the analysis of gaze cues that provide socially meaningful spatial information.

Highlights

  • The eyes move in the service of visual perception and to support communication by indicating direction of attention, intention, or emotion [7]

  • The neural network for gaze processing isolated by this analysis included three key regions: the posterior portion of the Superior temporal sulcus (STS) bilaterally, corresponding to Brodmann’s areas 22 and 39 (BA 22,39), the same area previously identified in gaze studies [27,47]; a right prefrontal region centered in the frontal eye fields (BA 8,9); and a ventral prefrontal region centered in the inferior frontal gyrus (BA 44,45)

  • Patterns of activation revealed with fMRI in these two experiments showed that distinct contributions arise from brain networks in four regions thought to be involved in gaze processing

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Summary

Introduction

The eyes move in the service of visual perception and to support communication by indicating direction of attention, intention, or emotion [7]. Adults tend to automatically shift their attention in the direction of another person’s gaze [20], and when this happens, the outcome is that both people are attending to the same thing. This phenomenon of joint attention has been shown to facilitate the development of language and social cognition in children, and to facilitate theory of mind skills—the understanding of another person’s mental state [5,38,41]. Direct eye contact—when two people gaze directly at one another—is an important aspect of gaze behavior [35]. Perceiving eye contact directs and fixes attention on the observed face [23] and in visual

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