Neuropsychologia 48 (2010) 3657���3660 Contents lists available at ScienceDirect Neuropsychologia j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / n e u r o p s y c h o l o g i a Brief communication Face-related ERPs are modulated by point of gaze James McPartland ��� , Celeste H.M. Cheung, Danielle Perszyk, Linda C. Mayes Yale Child Study Center, Yale School of Medicine, 230 South Frontage Rd., New Haven, CT 06520, United States a r t i c l e i n f o Article history: Received 29 January 2010 Received in revised form 28 May 2010 Accepted 14 July 2010 Available online 21 July 2010 Keywords: Social neuroscience N170 Event-related potential Electroencephalogram EEG Face perception a b s t r a c t This study examined the influence of gaze fixation on face-sensitive ERPs. A fixation crosshair presented prior to face onset directed visual attention to upper, central, or lower face regions while ERPs were recorded. This manipulation modulated a face-sensitive component (N170) but not an early sensory component (P1). Upper and lower face fixations elicited enhanced N170 amplitude and longer N170 latency. Results expand upon extant hemodynamic research by demonstrating early effects at basic stages of face processing. These findings distinguish attention to facial features in context from attention to isolated features, and they inform electrophysiological studies of face processing in clinical populations. �� 2010 Elsevier Ltd. All rights reserved. 1. Introduction Human face perception is a vital social function subserved by specialized brain mechanisms. Event-related potential (ERP) studies reveal a face-sensitive negative component peaking approximately 170 ms after viewing a face (N170 Bentin, Allison, Puce, Perez, & McCarthy, 1996). Relative to other visual stimuli, the N170 elicited by faces tends to be larger in amplitude and shorter in latency. Because of its short latency, sensitivity to perturbations in face configuration (e.g., face inversion), and relative insensitiv- ity to higher order features (e.g., identity and emotion), the N170 is hypothesized to mark structural encoding, an early stage of face perception (Eimer, 2000). Isolated face parts also evoke an N170, with eyes eliciting the greatest amplitude, followed by whole faces and then noses and mouths (Bentin et al., 1996). This differential responsiveness to the eyes and an accelerated developmental mat- uration of the N170 elicited by eyes (Taylor, Edmonds, McCarthy, & Allison, 2001) has spurred speculation that the component may reflect activity in brain regions specifically subserving eye detec- tion. With respect to N170 latency, intact faces evoke the shortest latencies, followed by eyes then noses and mouths (Bentin et al., 1996). Though previous ERP research has examined N170 response to isolated facial features, attention to facial features within the con- text of an intact face remains unexplored via electrophysiological ��� Corresponding author. Tel.: +1 203 785 7179 fax: +1 203 764 4373. E-mail address: james.mcpartland@yale.edu (J. McPartland). methods. Functional magnetic resonance imaging research (fMRI) indicates that manipulating attention to the eyes and mouths mod- ulates hemodynamic activity in face-related areas, such as the fusiform gyrus (FG), with attention to these regions most strongly activating the FG in typical adults (Morris, Pelphrey, & McCarthy, 2007). These findings bear relevance to understanding face-related ERPs, as source estimation and co-recording of ERP and fMRI sug- gest neural generators of the N170 in FG (Itier & Taylor, 2004 Rossion, Joyce, Cottrell, & Tarr, 2003 Sadeh, Podlipsky, Zhdanov, & Yovel, 2010 Shibata et al., 2002). The current study extends extant neuroimaging work by using electrophysiological methods to investigate the influence of point of gaze on face-related brain activity. This approach expands upon current understanding by (a) extricating the influence of differ- ential attention to eyes versus mouths, (b) examining attention to faces in a more natural presentation, i.e., without a superim- posed fixation crosshair, and (c) applying the temporal resolution of ERP to specifically examine modulation at the earliest stages of face perception. ERPs were recorded as typical adults viewed neu- tral faces without a fixation crosshair and with a variable fixation crosshair directing attention to the upper, central, or lower face. We hypothesized that visual fixations to the eyes would elicit N170 with enhanced amplitude and shorter latency relative to other fixation positions. Though previous research has not consistently revealed face-selective effects at an earlier sensory component, the P1, we explored this ERP component to determine whether gaze manipulation effects might be exerted through low-level visuop- erceptual mechanisms. We did not predict P1 modulation by point of gaze. 0028-3932/$ ��� see front matter �� 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2010.07.020

3658 J. McPartland et al. / Neuropsychologia 48 (2010) 3657���3660 Fig. 1. Example face stimulus with overlaid crosshair displaying (a) upper, (b) central, and (c) lower positions. A fourth fixation condition entailed (d) no crosshair display. Note that, during the experiment, the crosshair preceded presentation of faces without overlap. 2. Methods Participants included 28 typically developing adults enrolled in an ongoing ERP study in the Developmental Electrophysiology Laboratory at the Yale Child Study Center (http://childstudycenter.yale.edu/del). Participants were screened by self-report for current or historical brain injury or disease and for normal or corrected-to-normal visual acuity. Thirteen participants��� data were excluded from analysis for: equipment failure (n = 1), visual impairment (n = 1), excessive EEG arti- fact (n = 11). The final sample included 15 individuals (7 females, 8 males mean age 22.9 years all right handed). All procedures were conducted with the understanding and written consent of participants and with approval of the Human Investigation Committee at the Yale School of Medicine consistent with the 1964 Declaration of Helsinki. Stimuli consisted of 204 distinct grayscale digital images of neutral faces (102 males, 102 females drawn from the Center for Vital Longevity Face Database Minear & Park, 2004) and houses. All stimuli were presented in frontal view and at a standardized viewing size (10.6��� by 8.1��� ) on a uniform black background. Faces were cropped within an oval frame to remove non-face features as per Gronenschild, Smeets, Vuurman, van Boxtel, and Jolles (2009). Stimuli were presented on a 51 cm color monitor (75 Hz, 1024 �� 768 resolution) with E-Prime 1.2 software (Schneider, Eschman, & Zuccolotto, 2002) at a viewing dis- tance of 91 cm in a sound attenuated room with low ambient illumination. EEG was recorded continuously at 250 Hz using NetStation 4.3. A 128 lead Geodesic Sensor Net 200 (Electrical Geodesics Incorporated Tucker, 1993) was fitted on the partic- ipant���s head according to the manufacturer���s specifications. Impedances were kept below 40 k . To manipulate visual attention, the vertical position of a fixation crosshair directed attention to either the (a) upper, (b) central, or (c) lower regions of the stimulus a fourth presentation condition used (d) no fixation crosshair (see Fig. 1). The horizontal position of the crosshair was held constant, and vertical position was equiprobable and varied randomly among trials. The fixation crosshair was presented for a time period varying randomly between 500 and 1000 ms and was followed immediately by a randomly selected face or house stimulus for 500 ms and then a 700 ms blank screen. To monitor attention, participants pressed a but- ton upon detection of randomly interspersed red-shaded target stimuli (10 houses, 10 faces, 20 crosshairs). All participants detected at least 95% of targets, and tar- get trials were excluded from analysis. The 15 min experiment included 428 total trials in random sequence: 204 distinct faces (10 preceded by target crosshair), 204 distinct houses (10 preceded by target crosshair), 10 face targets, 10 house targets. Data were averaged for each participant, digitally filtered (30 Hz low-pass), and transformed to correct for baseline shifts. The segmentation epoch was 100 ms before to 600 ms after stimulus onset. NetStation artifact detection settings were set to 200 V for bad channels, 150 V for eye blinks, and 100 V for eye movements. Channels with artifacts on more than 25% of trials were marked as bad channels and replaced through spline interpolation. Segments that contained eye blinks, eye movement, or more than 10 bad channels were marked as bad and excluded. Par- ticipants with more than 25% bad channels were excluded from analysis. Data were averaged across six electrodes over the left (58, 59, 64, 65, 69, 70) and right (90, 91, 92, 95, 96, 97) lateral posterior scalp electrodes were selected based on maxi- mal observed amplitude of the N170 to faces and precedent (McPartland, Dawson, Webb, Panagiotides, & Carver, 2004). Time windows for ERP analysis were chosen by visual inspection of grand aver- aged data and confirmed for individual averages. Resultant time windows extended from 63 to 149 ms for the P1 and 103 to 203 ms for the N170. Peak amplitude and latency for each component were averaged across each electrode group for each participant and exported to SPSS for analysis (SPSS 16.0 for Windows, 2008). ERP parameters were analyzed using repeated measures ANOVA, with experimen- tal condition (i.e., stimulus or fixation position) and hemisphere as within-subjects factors as per Picton et al. (2000). 3. Results 3.1. Neural response to faces To confirm the presence of a face-selective N170, faces and houses were compared across viewing conditions using univari- ate repeated measures ANOVA with condition (face/house) and hemisphere (left/right) as within-subjects factors. For amplitude, N170 to faces but not houses was reflected in a main effect of con- dition [F(1,14) = 31.11, p .01, 2 partial = .69, observed power = .99], indicating larger amplitude to faces across hemispheres. Faces also elicited an N170 with shorter latency in the right hemisphere, as reflected in the omnibus model by a condition by hemisphere inter- action [F(1,14) = 5.84, p .05, 2 partial = .29, observed power = .61] and confirmed with a post hoc paired t-test [t(14) = 2.43, p .05, 2 partial = .30, observed power = .62]. No other significant effects for N170 latency or amplitude were detected [all p .05, 2 partial .19]. Fig. 2 displays waveforms to faces and houses. 3.2. Point of gaze and ERP response To examine the potential influence of point of gaze on neural response to faces, separate univariate repeated measures ANOVAs with fixation position (upper/central/lower/absent) and hemi- sphere (left/right) as within-subjects factors were calculated for P1 and N170 latency and amplitude. P1. No significant effects were detected for P1 amplitude or latency [all p .05, 2 partial .18]. Fig. 2. Grand averaged ERP waveforms depicting response to houses and faces. Data shown are averaged across the 12 electrodes of interest across hemispheres, and fixation conditions are collapsed.