Visual activation corresponds to expected regions of interest
The activation patterns to the visual stimuli consisting of faces, houses, and flickering checkerboard were as predicted for the control subjects. The largest responses to all stimuli were in V1, and then the fusiform face area (FFA). The parahippocampal place area showed the greatest activation to the house stimuli, but very little to the others. The most anterior portion of the calcarine showed more deactivation than activation in controls.
The devastating effect of SBR’s damage to V1 can be seen by comparing the % BOLD changes in this region with controls (see Fig. 2). All stimuli evoke a large response in V1 of the control subjects, with the greatest response to the flashing checkerboard. In contrast, none of the stimuli produce consistent activation in SBR, with no activation significantly greater than zero. Indeed, the response in SBR to checkerboards was more than two standard deviations away from the control group. The anatomically defined anterior calcarine region, which was previously shown to be intact in SBR, does show large responses. In particular, the checkerboard evokes large responses in this region in SBR, while being negatively activated in control subjects.
Although SBR claimed not to be able to perceive the visual stimuli, the faces and houses evoked patterns of activation similar to those in controls in the FFA, albeit at a lower level. There was also activation in SBR’s PPA, although this was considerably more variable. SBR’s activation to faces and houses are shown in Fig. 2b. The apparent lateralization to the right hemisphere indicates that SBR’s eyes were probably not looking at the center of the screen.
Patterns of activation to mental imagery of houses, faces, and checkerboards
When asked to imagine houses, faces, or checkerboards, most control subjects were able to do this for the duration of the scan block. There was considerable variability, however, in the level and pattern of activation across subjects. The group activation is shown in Fig. 3 (lower row). The greatest activation is to the imagery of houses, where large regions of activation are present in both the anterior calcarine and the PPA. Mental imagery of faces also activates the anterior calcarine, and medial frontal regions. Despite the wide inter-subject variation in the cortical regions activated by the checkerboard condition, the fixed-effects analysis showed regions of parietal and lateral occipital cortex activated. No region of the medial occipital lobe was activated in this condition.
The equivalent patterns of activation in SBR differ according to the condition. In particular, the pattern of activation to imagery of houses is remarkably similar to the control group. The group data appear to be more reliable due to the type of analysis used. If a mixed-effects analysis is applied to the control data, the activation appears significantly lower than that in SBR (supplementary figure 1). Comparison of imagery of faces is also similar with the exception of the anterior calcarine, which is significantly activated in controls, but not at all in SBR. The reasons for this discrepancy are unclear, but presumably relate to the method used to generate the images.
The checkerboard appears to show the largest discrepancy between controls and SBR, the latter showing significant activity only in the fusiform region. In contrast, control subjects show a similar pattern of parietal and frontal activation as seen in the other conditions. However, there is considerable variability between control subjects, such that the use of a mixed-effects analysis results in minimal activation, as seen in supplementary figure 1. The similarity between the data in SBR and the group, presented as % BOLD change, is shown in Fig. 4. The pattern of activity across all the regions implicated in imagery is comparable for SBR and controls. Indeed, while SBR reported being unable to perceive the visual stimuli, he confidently reported being able to generate images of faces and houses, although he found checkerboards more difficult.
Interestingly, imagery of houses evoked a response just significantly greater than baseline in the primary visual cortex of control subjects (t = 2.0, df = 23, p < 0.05). However, the similarity of activation to imagery of houses between controls and SBR outside of V1 is striking, suggesting that a lack of V1 activation does not affect activation in extrastriate areas.
In sighted subjects, occipital responses to perception are greater than to mental imagery
Comparison of responses to visual stimulation and visual mental imagery in each of the visual regions of interest showed significant differences. A two-way ANOVA showed a highly significant effect of stimulus type in V1 (F = 62.2; p << 0.001; df = 1) and FFA (F = 10.2; p < 0.005; df = 1) with greater responses to visual stimuli. In contrast, the significant effect of stimulus type in the anterior calcarine region reflected greater activation to mental imagery (F = 23.6; p << 0.001; df = 1). The PPA was the only region that showed no effect of stimulus type.
These results contrast sharply with the data from SBR in which the activation to imagery is greater than visual stimuli in both the FFA and the PPA. There are no responses significantly different from zero in V1 for either stimulus type. In the anterior calcarine, imagery of houses evokes a considerably larger response than visual presentation, although visual presentation of both faces and checkerboards result in larger activation than imagery.
Behavioral measures of visual mental imagery
Most control subjects showed good levels of mental imagery vividness as reflected in the VVIQ, score mean of 2.3 ± 0.6. On this scale, 1 reflects extremely vivid images and 5 is unable to produce an image. SBR’s vivid imagery was reflected in his score (1.9). In addition to his high score on the VVIQ, SBR shows high imagery performance across a battery of imagery questionnaires. In addition, he was able to readily describe detailed topographical imagery, e.g., the description of the route from his house to the pub; a detailed visual childhood image of playing in the garden describing colors, objects, and people; and a description of the shape of the Sydney Opera House (Table 1).