Processing of Mutual and Averted Social Gaze in the Superior Temporal Sulcus

Using functional magnetic resonance imaging (fMRI), we investigated brain activity evoked by mutual and averted gaze in a compelling and commonly experienced social encounter. Through virtual-reality goggles, subjects viewed a man who walked toward them and shifted his neutral gaze either toward (mutual gaze) or away (averted gaze) from them. Robust activity was evoked in the superior temporal sulcus (STS) and fusiform gyrus (FFG). For both conditions, STS activity was strongly right lateralized. Mutual gaze evoked greater activity in the STS than did averted gaze, whereas the FFG responded equivalently to mutual and averted gaze. Thus, we show that the STS is involved in processing social information conveyed by shifts in gaze within an overtly social context. This study extends understanding of the role of the STS in social cognition and social perception by demonstrating that it is highly sensitive to the context in which a human action occurs. Gaze is a potent social cue, with mutual gaze often signaling threat or approach and averted gaze conveying submission or avoidance (Argyle & Cook, 1976; Baron-Cohen, 1995; Darwin, 1872/1965; Emery, 2000; Kleinke, 1986; Strongman & Champness, 1968). Processing of eye gaze is fundamental to social interactions, as demonstrated by its early emergence in ontogeny and disruption in autism (Hood, Willen, & Driver, 1998; Pelphrey et al., 2002). An explication of the neural substrate for gaze processing is an important step in the development of a neuroscience for social cognition. There is general agreement that the superior temporal sulcus (STS) region is involved in the perception of eye gaze (Hoffman & Haxby, 2000; Pelphrey, Singerman, Allison, & McCarthy, 2003; Puce, Allison, Bentin, Gore, & McCarthy, 1998; Puce, Smith, & Allison, 2000; Wicker, Michel, Henaff, & Decety, 1998), and recent evidence suggests that this region is sensitive to the social context in which a gaze shift occurs (Pelphrey, Singerman, et al., 2003). Thus, it might be expected that the degree to which the gaze of another person engages the observer would influence STS processing; however, neuroimaging studies that have compared mutual and averted gaze have reported conflicting findings (George, Driver, & Dolan, 2001; Hoffman & Haxby, 2000; Kawashima et al., 1999; Wicker et al., 1998). One functional magnetic resonance imaging (fMRI) study reported increased STS activity for averted compared with mutual gaze and an absence of differential activity in the fusiform gyrus (FFG; Hoffman & Haxby, 2000), whereas another reported increased activity in the FFG for mutual gaze compared with averted gaze and an absence of differential STS activity (George et al., 2001). A third fMRI study showed bilateral amygdala activity for mutual but not averted gaze (Kawashima et al., 1999). Finally, a positron emission tomography (PET) study reported equivalent STS activity for mutual and averted gaze (Wicker et al., 1998). Three of the four aforementioned studies used static faces displaying mutual or averted gaze rather than dynamic faces in which the eyes shifted gaze from a neutral point to a state of mutual or averted gaze (George et al., 2001; Hoffman & Haxby, 2000; Wicker et al., 1998). Interpreting their findings is thus more challenging because differential activity may simply reflect differential quantities of motion implied by faces with averted gaze compared with mutual gaze (Kourtzi & Kanwisher, 2000; Senior et al., 2000). Moreover, previous studies have not examined mutual and averted gaze within realistic social contexts, but rather have presented isolated posed faces as stimuli. Hence, a central question remains concerning whether (and how) the STS and other brain regions are involved in processing the social information conveyed by mutual and averted gaze in compelling and socially demanding contexts. In an early fMRI study, our laboratory first demonstrated the role of the STS in gaze processing (Puce et al., 1998), and we subsequently demonstrated that this region is sensitive to the intentionality of observed gaze shifts (Pelphrey, Singerman, et al., 2003). Here, using fMRI, we examined whether the STS participates in the visual analysis of social information conveyed by gaze shifts in an overtly social encounter that most readers will find familiar—a stranger walking past them in a hallway. Subjects viewed an animated male figure that Address correspondence to Gregory McCarthy, Duke-UNC Brain Imaging and Analysis Center, Duke University Medical Center, 163 Bell Building, P.O. Box 3918, Durham, NC 27710; e-mail: gregory. [email protected]. PSYCHOLOGICAL SCIENCE 598 Volume 15—Number 9 Copyright r 2004 American Psychological Society walked toward them and shifted his neutral gaze either toward (mutual gaze) or away (averted gaze) from them (see Fig. 1). We randomly changed the side from which the figure passed the observer, so that the identical gaze shift could serve for both mutual and averted gaze and thus control for any physical differences in the evoking stimulus. We reasoned that if gaze-related STS activity reflects the operation of a simple eye movement detector (or, more generally, a biological motion detector), the region should not respond differentially to mutual and averted gaze. We found that mutual gaze evoked greater activity in the STS than did averted gaze. In contrast, the FFG responded equivalently to mutual and averted gaze. Thus, we show that the STS is involved in processing social information conveyed by shifts in gaze within an overtly social and dynamic context, and that activity in this region is influenced by the social context (that of approach or avoidance) in which an observed human action occurs.