Horizontal tuning for faces originates in high-level Fusiform Face Area

Recent work indicates that the specialization of face visual perception relies on the privileged processing of horizontal angles of facial information. This suggests that stimulus properties assumed to be fully resolved in primary visual cortex (V1; e.g., orientation) in fact determine human vision until high-level stages of processing. To address this hypothesis, the present fMRI study explored the orientation sensitivity of V1 and high-level face-specialized ventral regions such as the Occipital Face Area (OFA) and Fusiform Face Area (FFA) to different angles of face information. Participants viewed face images filtered to retain information at horizontal, vertical or oblique angles. Filtered images were viewed upright, inverted and (phase-)scrambled. FFA responded most strongly to the horizontal range of upright face information; its activation pattern reliably separated horizontal from oblique ranges, but only when faces were upright. Moreover, activation patterns induced in the right FFA and the OFA by upright and inverted faces could only be separated based on horizontal information. This indicates that the specialized processing of upright face information in the OFA and FFA essentially relies on the encoding of horizontal facial cues. This pattern was not passively inherited from V1, which was found to respond less strongly to horizontal than other orientations likely due to adaptive whitening. Moreover, we found that orientation decoding accuracy in V1 was impaired for stimuli containing no meaningful shape. By showing that primary coding in V1 is influenced by high-order stimulus structure and that high-level processing is tuned to selective ranges of primary information, the present work suggests that primary and high-level levels of the visual system interact in order to modulate the processing of certain ranges of primary information depending on their relevance with respect to the stimulus and task at hand.