Neural microgenesis of personally familiar face recognition

Significance We addressed the open question of how the human brain recognizes personally familiar faces. A dynamic visual-stimulation paradigm revealed that familiar face recognition is achieved first and foremost in medial and anterior temporal regions of the extended face-processing system. These regions, including the amygdala, respond categorically to individual familiar faces. In contrast, activation in posterior core face-preferential regions is associated with the amount of visual information available, irrespective of familiarity. Through integration of core and extended face-processing systems, these observations provide a common framework for understanding the neural basis of familiar face recognition. Despite a wealth of information provided by neuroimaging research, the neural basis of familiar face recognition in humans remains largely unknown. Here, we isolated the discriminative neural responses to unfamiliar and familiar faces by slowly increasing visual information (i.e., high-spatial frequencies) to progressively reveal faces of unfamiliar or personally familiar individuals. Activation in ventral occipitotemporal face-preferential regions increased with visual information, independently of long-term face familiarity. In contrast, medial temporal lobe structures (perirhinal cortex, amygdala, hippocampus) and anterior inferior temporal cortex responded abruptly when sufficient information for familiar face recognition was accumulated. These observations suggest that following detailed analysis of individual faces in core posterior areas of the face-processing network, familiar face recognition emerges categorically in medial temporal and anterior regions of the extended cortical face network.