Early sensitivity for eyes within faces: a new neuronal account of holistic and featural processing

Abstract

Eyes are central to face processing however their role in early face encoding as reflected by the N170 ERP component is unclear. Using eye tracking to enforce fixation on specific facial features, we found that the N170 was larger for fixation on the eyes compared to fixation on the forehead, nasion, nose or mouth, which all yielded similar amplitudes. This eye sensitivity was seen in both upright and inverted faces and was lost in eyeless faces, demonstrating it was due to the presence of eyes at fovea. Upright eyeless faces elicited largest N170 at nose fixation. Importantly, the N170 face inversion effect (FIE) was strongly attenuated in eyeless faces when fixation was on the eyes but was less attenuated for nose fixation and was normal when fixation was on the mouth. These results suggest the impact of eye removal on the N170 FIE is a function of the angular distance between the fixated feature and the eye location. We propose the Lateral Inhibition, Face Template and Eye Detector based (LIFTED) model which accounts for all the present N170 results including the FIE and its interaction with eye removal. Although eyes elicit the largest N170 response, reflecting the activity of an eye detector, the processing of upright faces is holistic and entails an inhibitory mechanism from neurons coding parafoveal information onto neurons coding foveal information. The LIFTED model provides a neuronal account of holistic and featural processing involved in upright and inverted faces and offers precise predictions for further testing.

Keywords: Eye-tracking; Eyes; Faces; Holistic; Inversion; N170.

Figure 1

Left panel: examples of one face presented at each fixation location in the inverted and upright conditions. Participants fixated in the center of the monitor represented here by each white rectangle (images are to scale) and the face was offset in such a way that gaze fixated 6 possible face locations: forehead, nasion, left eye, right eye, tip of the nose, and mouth. Note that eye positions are from a viewer perspective (i.e. left eye is on the left of the picture). This particular positioning of the face to obtain the desired feature fixated resulted in the face situated almost entirely in the upper visual field when fixation was on the mouth in upright faces and almost entirely in the lower visual field when fixation was on the forehead, while the opposite pattern was seen for inverted faces. Right panel, up: one face exemplar with picture size and distances between features in visual angles. The yellow circles represent the interest areas of 1.8° centered on each feature that were used to reject eye gaze deviations in each fixation condition. Right panel, bottom: houses, eyeless and intact face examples, with fixation crosses overlaid on the intact face to indicate where the fixation would occur (note that fixation crosses were never presented overlaid on faces in the actual experiment).

Figure 2

P1 and N170 ERP components for intact faces at nasion fixation and for houses (fixated in the center) presented upright and inverted. Components were measured at CB1 and CB2 electrodes. Note the much larger N170 response to faces and the larger inversion effect for faces than houses.

Figure 3

Mean N170 latency recorded at each fixation location for upright and inverted faces (averaged across hemispheres and face type; upper panel) and left and right hemispheres (LH and RH respectively, averaged across face types and orientations; lower panel). Errors bars represent standard errors to the means.

Figure 4

Left panel: ERP components for upright intact and upright eyeless faces displayed at each fixation location (CB2 electrode). The larger P1 and N170 for intact than eyeless faces are clearly seen for eye fixations while a larger N170 for eyeless than intact faces is clearly visible for nose fixation. Right panel: N170 to intact and eyeless upright faces for all fixation locations (CB2 electrode). The larger N170 for eye fixations is clearly seen for intact faces while a larger N170 for nose fixation is clearly seen for eyeless faces.

Figure 5

N170 inversion effect displayed for intact and eyeless faces at each fixation location (left panels: ERP waveforms displayed at CB2 site; right panel up: bar plots with standard errors, averaged across CB1 and CB2 electrodes; right panel bottom: bar plots of the inverted-upright N170 amplitude difference for each category across both hemispheres). A clear inversion effect is seen for all fixation locations for intact faces, and the magnitude of this FIE does not differ between fixation locations. For eyeless faces, no N170 FIE was seen for forehead fixation, a very small effect was seen for nasion and both eye fixations, and a clear effect was seen for nose and mouth fixations. The FIE at mouth fixation did not differ significantly between intact and eyeless faces.

Figure 6

Left panel: ERP components for inverted intact and inverted eyeless faces displayed at each fixation location (CB2 site). The larger N170 for intact than eyeless faces is clearly seen for forehead, nasion, and both eye fixations while N170 was identical for the two face categories for mouth fixation. Right panel: N170 to intact and eyeless inverted faces for all fixation locations (CB2 site). The larger N170 for eye fixations is clearly seen for intact faces while a larger N170 for nose and mouth fixations is clearly seen for eyeless faces.

Figure 7

Schematic representation of how lateral inhibitions work according to the LIFTED model and the contribution of the visual information to the scalp recorded N170 ERP component. Three fixation location conditions are represented: mouth, nose and left eye. The smaller blue circles represent the fovea; the larger blue circles represent the parafovea, i.e. the approximate distance from fixation under which peripheral features contribute to the inhibition and to the overall neuronal response (N170). The overrepresentation of the fixated feature due to cortical magnification is represented as a disproportionately large feature. In upright faces, this overrepresentation is cancelled by lateral inhibitions (red arrows) from neurons coding for parafoveal features onto neurons coding for the foveated feature. The strength of the lateral inhibitions depends on the distance between the fixated and peripheral features (stronger when distances are shorter, represented by thicker arrows). In inverted faces, lateral inhibitions are no longer seen. See main text for the explanation of the N170 variations in each fixation condition.