Impaired fixation to eyes following amygdala damage arises from abnormal bottom-up attention

Abstract

SM is a patient with complete bilateral amygdala lesions who fails to fixate the eyes in faces and is consequently impaired in recognizing fear (Adolphs et al., 2005). Here we first replicated earlier findings in SM of reduced gaze to the eyes when seen in whole faces. Examination of the time course of fixations revealed that SM's reduced eye contact is particular pronounced in the first fixation to the face, and less abnormal in subsequent fixations. In a second set of experiments, we used a gaze-contingent presentation of faces with real time eye tracking, wherein only a small region of the face is made visible at the center of gaze. In essence, viewers explore the face by moving a small searchlight over the face with their gaze. Under such viewing conditions, SM's fixations to eye region of faces became entirely normalized. We suggest that this effect arises from the absence of bottom-up effects due to the facial features, allowing gaze location to be driven entirely by top-down control. Together with SM's failure to fixate the eyes in whole faces primarily at the very first saccade, the findings suggest that the saliency of the eyes normally attract our gaze in an amygdala-dependent manner. Impaired eye gaze is also a prominent feature of several psychiatric illnesses in which the amygdala has been hypothesized to be dysfunctional, and our findings and experimental manipulation may hold promise for interventions in such populations, including autism and fragile X syndrome.

Figure 1

Example of experimental setup and stimuli for the gaze-contingent task. (a) The participant sees only a small aperture of the face that is centered at the direction of gaze. This aperture moves around on the face in real time as the participant’s eyes move. (b) Close-up of the stimuli seen in (a). A circle outlined the area of the screen where the face could be revealed in a gaze-contingent manner. The evenly spaced grid of small dots was included after pilot testing found that it was difficult for pilot subjects to make a saccade to an empty area of the screen.

Figure 2

Eye and face Regions of Interest (ROIs) are shown, overlaid on the mean face image. The eye ROI covered 22% of the area of the entire face, and so fixations to the eye region would be expected 22% of the time by chance alone.

Figure 3

Fixation heat maps showing locations of face fixations for patient SM and control participants for both the 1-back gender task and passive viewing task. Fixations were smoothed with a 27-pixel FWHM Gaussian filter, corresponding to 2° visual angle. Each heatmap is displayed in arbitrary units, but corresponds to fixation duration/smoothed area. Heatmaps are displayed on the mean of all face images. Each individual heatmap is scaled from zero fixations (blue) to the point of maximal fixation (red). The group difference heatmap shows areas SM fixated more than controls (blue), and vice versa (red), with green meaning there was no difference between groups. Please refer to ROI analyses (see Results) for statistical analyses.

Figure 4

Locations of first face fixations for control participants and SM for both the 1-back gender task and the passive viewing task combined. Each dot represents 1 individual fixation (control fixations, n = 500; SM fixations, n = 100).

Figure 5

Proportion of time fixating the eye region across fixation number. SM (red) had fewer initial fixations to the eyes, but more so on subsequent fixations (control participants = blue). Errorbars reflect the standard deviation. *p = 0.005, N.S. = not significant.

Figure 6

Fixation cross location does not account for SM’s reduced fixation to the eyes. Even when the fixation cross was positioned above the face, SM still bypassed the eyes to look at the lower regions of the face. The scale is in arbitrary units, but reflects the relative proportion of time fixating each particular area of the face, collapsed across the width of the face. The solid blue line represents the mean of controls, and the dotted blue lines represent individual subjects.

Figure 7

Gaze-contingent viewing of faces normalizes eye fixations in SM. (a) Line plots of the proportion of time fixating the eyes vs. non-eyes of the face for first fixations (left) and all fixations (right) during the baseline and gaze-contingent tasks. SM is shown in red, and comparison subjects are shown in blue. *p = 0.008, ^#p = 0.06 (trend). (b) Heatmaps across all fixations for SM and control participants during the baseline task and gaze-contingent task. The scale represents normalized fixation duration for each group separately, from no fixation to maximum fixation duration. Heatmaps are smoothed with a 27-pixel (2°) FWHM Gaussian filter.