Face-sensitive responses in the occipital inferior cortex of normal humans through feedback inputs from the fusiform gyrus ?: Evidence from neuroimaging studies of brain-damaged prosopagnosic patients

In humans, neuroimaging studies have identified two major visual extrastriate areas presenting face-sensitive responses: in the inferior occipital cortex (‘occipital face area’, OFA), and the middle fusiform gyrus (the ‘fusiform face area’, FFA), with a right hemispheric dominance. It has been proposed that the OFA, located anteriorly to foveal V4v (Halgren et al., 1999), has a critical role in the early perception of facial features and provides the feedforward outputs to later stages of face processing in both the FFA and the STS (Haxby et al., 2000). However, we have recently reported a normal activation of the right FFA despite a lesion encompassing the region of the right OFA in a brain-damaged prosopagnosic patient, PS (Rossion et al., 2003), suggesting that the face-sensitive responses observed at the level of the OFA in normals may rather arise from feedback connections from the FFA. Here we provide complementary fMRI evidence supporting this view. First, the normal differential activation for faces and objects in the right FFA of PS was observed only for left visual field presentations and is thus unlikely to originate from contralateral intact regions of the occipital cortex (e.g. left OFA). Second, the time-course in the right FFA and left OFA of PS for centrally presented items suggests an earlier differential activity between faces and objects in the most anterior region, the FFA. Finally, we imaged another (prosop)agnosic patient (NS, Delvenne et al., 2004) with a lesion encompassing the right FFA but sparing all posterior visual areas, and failed to disclose any face-sensitive response in his nonetheless structurally and functionnally intact occipital cortex. Together, these findings illustrate the necessary role of both the right FFA and OFA for accurate face perception, and reinforce the hypothesis that a dominant (feedback) connection from the FFA to the OFA subtends face-sensitive responses observed in the latter area when processing faces.