We investigated the neural correlates of facial processing changes in healthy aging using fMRI and an adaptation paradigm. In the scanner, participants were successively presented with faces that varied in identity, viewpoint, both, or neither and performed a head size detection task independent of identity or viewpoint. In right fusiform face area (FFA), older adults failed to show adaptation to the same face repeatedly presented in the same view, which elicited the most adaptation in young adults. We also performed a multivariate analysis to examine correlations between whole-brain activation patterns and behavioral performance in a face-matching task tested outside the scanner. Despite poor neural adaptation in right FFA, high-performing older adults engaged the same face-processing network as high-performing young adults across conditions, except the one presenting a same facial identity across different viewpoints. Low-performing older adults used this network to a lesser extent. Additionally, high-performing older adults uniquely recruited a set of areas related to better performance across all conditions, indicating age-specific involvement of this added network. This network did not include the core ventral face-processing areas but involved the left inferior occipital gyrus, frontal, and parietal regions. Although our adaptation results show that the neuronal representations of the core face-preferring areas become less selective with age, our multivariate analysis indicates that older adults utilize a distinct network of regions associated with better face matching performance, suggesting that engaging this network may compensate for deficiencies in ventral face processing regions.

It is well established that the human visual system contains a distributed network of regions that are involved in processing faces, but our understanding of how faces are represented within these face-sensitive brain areas is incomplete. We used fMRI to investigate whether face-sensitive brain areas are solely tuned for whole faces, or whether they contain heterogeneous populations of neurons tuned to individual components of the face as well as whole faces, as suggested by physiological investigations in nonhuman primates. The middle fusiform gyrus (fusiform face area, or FFA) and the inferior occipital gyrus (occipital face area, or OFA) produced robust BOLD activation to synthetic whole face stimuli, but also to the internal facial features and head outlines. BOLD responses to whole face stimuli in FFA were significantly reduced after adaptation to whole faces, but not after adaptation to features or head outlines, whereas activation to head outlines was reduced after adaptation to both whole faces and head outlines. OFA showed no significant adaptation effects for matching adaptation and test conditions, but did exhibit cross-adaptation between whole faces and head outlines. The internal face features did not produce any significant adaptation within either FFA or OFA. Our results are consistent with a model in which independent populations of whole face-, feature-, and head outline-tuned neurons exist within face-sensitive regions of human occipito-temporal cortex, which in turn would support tasks such as viewpoint processing, emotion classification, and identity discrimination.