Amygdala activation for eye contact despite complete cortical blindness

Abstract

Cortical blindness refers to the loss of vision that occurs after destruction of the primary visual cortex. Although there is no sensory cortex and hence no conscious vision, some cortically blind patients show amygdala activation in response to facial or bodily expressions of emotion. Here we investigated whether direction of gaze could also be processed in the absence of any functional visual cortex. A well-known patient with bilateral destruction of his visual cortex and subsequent cortical blindness was investigated in an fMRI paradigm during which blocks of faces were presented either with their gaze directed toward or away from the viewer. Increased right amygdala activation was found in response to directed compared with averted gaze. Activity in this region was further found to be functionally connected to a larger network associated with face and gaze processing. The present study demonstrates that, in human subjects, the amygdala response to eye contact does not require an intact primary visual cortex.

Figure 1.

Example of stimuli used in this study.

Figure 2.

BOLD response in Patient T.N. when presented with photographs of direct gaze (DG) versus averted gaze (AG). a, A significant activation was found in Patient T.N.'s right amygdala when blocks of faces with DGs were contrasted with photographs of faces with AGs. Using a fixed model, voxels showing a significantly greater response (p_(FWE) < 0.05) for DG when contrasted with AG were displayed on Patient T.N.'s T1 structural scan. A significantly increased response (z-score = 5.02, p_(FWE) corrected = 0.004) was found in the right amygdala (MNI coordinates, 24; −12; −10; volume, 67 mm³), consistent with previous findings regarding gaze processing in normally sighted individuals (Kawashima et al., 1999) and affective blindsight in this patient (Pegna et al., 2005). b, β values representing activation in the right amygdala (MNI coordinates, 24; −12; −10) for nonfiltered (normal), high-pass filtered and low-pass filtered images, showing no differences in-between conditions. The values illustrated here were obtained from the most significant voxel in the DG versus AG contrast and were not used for statistical computation. c, Contrast estimates were significant for DG versus AG (bars indicate 90% confidence intervals).

Figure 3.

PPI of right amygdala activation with locus ceruleus and right lingual gyrus activation. A, Seed region. B, Network of regions whose connectivity with the right amygdala was significantly greater in DG than AG (p_(FWE) < 0.05, cluster extent threshold k > 10). Scatter plots below show the relative activity, trial by trial, in the amygdala and two regions: (i) locus ceruleus (bottom left), which has previously been shown to respond to subliminal threatening stimuli) (Liddell et al., 2005) and (ii) the right lingual gyrus (bottom right), for DG (red) and AG (blue).

Figure 4.

BOLD response in a group of 10 healthy age-matched men for the contrast gaze straight > gaze averted (p < 0.001, cluster extent threshold > 10 voxels). In a random model, we demonstrated that the classic regions related to the gaze contact are activated. The right amygdala complex is also activated, but additional activation is revealed (left amygdala and hippocampus, right fusiform area). Some regions close to the region revealed during the PPI on the Patient T.N.'s right amygdala are activated.