The present study examined electrophysiological brain response to faces while manipulating point of gaze. Prior hemodynamic work has shown increased activity in face-related brain regions associated with viewing of the internal features of the face; research has not yet addressed whether directing attention to eyes versus mouths differentially modulates activity, whether modulation is contingent upon superimposition of a crosshair on a face, or whether modulation occurs at early stages of face processing. Consistent with prior research, the current study detected an N170 elicited by faces that, relative to non-face stimuli, was enhanced in amplitude over lateral posterior scalp and was shorter in latency over right hemisphere electrodes.
Though low-level visual perception, indexed by the P1, did not vary as a function of fixation position, both the amplitude and latency of the N170 were modulated by point of gaze on the face. As predicted, fixation to upper face regions, corresponding to the eyes, was associated with enhanced N170 amplitude relative to fixations to the central face or undirected fixations in the absence of a crosshair. An unpredicted effect indicated that fixation to lower face regions, corresponding to the mouth, was also associated with enhanced N170 amplitude relative to central or undirected face fixations. Comparable amplitude effects for both eyes and mouths in the context of an intact face contrast with prior ERP research on isolated facial features, which showed relatively enhanced N170 amplitude to eyes but not mouths (Bentin et al., 1996
). Because enhanced amplitude was also observed for mouths in this study, results are inconsistent with interpretations of the N170 as representative of an eye detector or the combination of face-sensitive and eye-sensitive neurons. Attention to parts of the face in the context of an intact face elicited processing distinct from attention to features in isolation; this concords with research implicating the N170 as a marker for configural perception (Rossion et al., 2000
N170 latency was also modulated by fixation position. When no crosshair was presented, N170 occurred at a shorter latency than when fixations were directed to the eyes or mouth. This may reflect a differential disengagement effect. When no crosshair was presented (viewing a blank screen before onset of the face stimulus), disengagement was unnecessary; attention to a percept would initiate with face onset. In contrast, when a crosshair preceded a face, viewers needed to disengage with the crosshair and subsequently engage with the face. This latency effect may also reflect the contribution of cognitive processing demands, as crosshairs were also targets in the attention monitoring task.
With respect to both N170 amplitude and latency, attention to eyes and mouths elicited comparable brain activity. Differential responsiveness to eyes and mouths relative to mid-face may reflect the relatively increased social salience of these features or the quantity of visual information present in these regions of the face. Alternatively, this selective responsiveness to both eyes and mouths, the regions of the face in which motion is most likely to occur, may reflect the contribution of brain regions subserving biological motion, such as the superior temporal sulcus (STS; Pelphrey, Morris, Michelich, Allison & McCarthy, 2005
). The N170 is responsive to facial movements (Puce, Smith & Allison, 2000
) and has been localized to several sources in inferotemporal cortex, including the STS (Itier & Taylor, 2004
). Results are consistent with the hypothesis that the N170 reflects an amalgamation of temporally overlapping activity in FG and STS (and, potentially, other proximal locations in inferotemporal cortex; Itier, Alain, Sedore & Mcintosh, 2007
). This would account for subtle distinctions in response patterns of the N170 and hemodynamic FG activation despite broad similarity in terms of face-selectivity, as well as evidence of direct correlations between N170 amplitude and latency and FG activation (Iidaka, Matsumoto, Haneda, Okada & Sadato, 2006).
Our findings bear relevance to studies of face perception in clinical populations, such as those with autism spectrum disorder (ASD). Individuals with ASD have been shown to exhibit atypical brain activity during face perception (McPartland et al., 2004
; Schultz et al., 2000
), which has been hypothesized to simply reflect differential viewing strategies, such as looking to the mouth instead of the eyes (Dalton et al., 2005
). Though present results make clear that fixation does indeed influence ERP response to faces, our findings of similar response patterns for eye and mouth fixations suggest that differential tendencies to look at eyes or mouths would not account for differences between individuals with ASD and typical counterparts. It is, of course, also possible that manipulation of point of gaze affects individuals with ASD in an entirely distinct way, in which case the current results from typical individuals might not apply. Ongoing work in our laboratory is examining the influence of point of gaze on face perception in ASD.
Understanding of the neural mechanisms of face perception also informs studies of social cognition. ERP and hemodynamic indices of face perception have also been implicated as markers of experience with non-face visual stimuli (Gauthier, Skudkarski, Gore & Anderson, 2000
; Tanaka & Curran, 2001
); it is not yet understood to what degree affective experience (e.g., developing a fondness for objects with which one frequently engages) contributes to these neural mechanisms. Likewise, FG activation is observed in social-perceptual tasks that do not involve faces (Schultz et al., 2003
). Neuropeptides involved in social behavior also suggest interrelationships among face perceptual systems and broader social cognition; administration of oxytocin has been shown to increase eye gaze and pro-social sentiments in typical and clinical populations (Guastella, Mitchell & Dadds, 2008
; Andari, Duhamel, Zalla, Herbrecht, Leboyer & Sirigu, 2010
). Moving forward, studies of face perception should consider neurochemistry and must frame findings in light of overarching social behavior.
There are several limitations of the current study. Though the target detection task ensured that participants viewed the crosshair with high consistency, visual attention was not directly measured. We are now concurrently recording EEG and visual attention as measured by an eye-tracker to more precisely quantify the relationship between visual attention to faces and electrophysiological brain activity. The size of face stimuli and the relative proximity of crosshair positions in the current study leave open the possibility that foveation to each position resulted in overlapping visual fields. Though our significant results suggest distinct visual perception for each crosshair position, it is possible that effects would be more pronounced with larger faces that permitted greater separation of crosshair positions; this work is currently in progress in our laboratory. The results of the current study might also be attributable to differences in composition of the overall visual field induced by the fixation manipulation. Upper and lower fixations would both likely include more non-face portions of the screen than central fixation. If this interfered with configural perception, as in inversion, it could account for the delayed and enhanced N170 in these conditions. This explanation, however, fails to account for differential effects for central versus absent crosshair. Because eyes and mouths are necessarily at the periphery of a visual stimulus relative to central fixation, this possibility cannot be directly examined without rearranging the face or making it sufficiently large that the visual field remains entirely on the face during eye or mouth fixation; both of these options would likely introduce artifacts that would obscure the influence of gaze on the N170 (Bentin et al., 1996
; Rousselet, Husk, Bennett & Sekuler, 2005
). Finally, we employed grayscale stimuli; though this is consistent with the majority of ERP studies of face perception, color images may have yielded different results. For example, ERPs might be differentially elicited by attention to mouths with more realistic, pink lips.
This study demonstrated that face-sensitive ERPs are modulated by looking patterns to intact faces. Rather than the eye-specific effects observed in ERP studies of isolated features, attention to the eyes and mouths similarly influenced neural response at the earliest stages of face perception. These results may reflect the influence of richness of visual information, social salience, or the contribution of brain regions subserving biological motion perception. This was the first electrophysiological study to manipulate visual attention during face perception, and findings emphasize the import of ERP's temporal precision in understanding social perceptual processes.