The bottom-up and top-down processing of faces in the human occipitotemporal cortex

Xiaoxu Fan,Peng Zhang,Sheng He,Fan Wang,Hanyu Shao

doi:10.7554/elife.48764

Abstract

Although face processing has been studied extensively, the dynamics of how face-selective cortical areas are engaged remains unclear. Here, we uncovered the timing of activation in core face-selective regions using functional Magnetic Resonance Imaging and Magnetoencephalography in humans. Processing of normal faces started in the posterior occipital areas and then proceeded to anterior regions. This bottom-up processing sequence was also observed even when internal facial features were misarranged. However, processing of two-tone Mooney faces lacking explicit prototypical facial features engaged top-down projection from the right posterior fusiform face area to right occipital face area. Further, face-specific responses elicited by contextual cues alone emerged simultaneously in the right ventral face-selective regions, suggesting parallel contextual facilitation. Together, our findings chronicle the precise timing of bottom-up, top-down, as well as context-facilitated processing sequences in the occipital-temporal face network, highlighting the importance of the top-down operations especially when faced with incomplete or ambiguous input.

Highlights

There is ample evidence to show that the processing of face information involves a distributed neural network of face-sensitive areas in the occipitotemporal cortex and beyond (Duchaine and Yovel, 2015; Haxby et al, 2000)
Three bilateral face-selective areas are considered as the core face-processing system, defined in functional Magnetic Resonance Imaging studies as regions showing significantly higher response to faces than objects, which are Occipital Face Area (OFA) in the inferior occipital gyrus (Gauthier et al, 2000; Haxby et al, 1999), Fusiform Face Area (FFA) in the fusiform gyrus (Kanwisher et al, 1997; Grill-Spector et al, 2004) and a face-sensitive area in the posterior superior temporal sulcus (Hoffman and Haxby, 2000; Puce et al, 1998)
Hierarchical models postulate that face specific processes are initiated in the OFA based on local facial features, the information is forwarded to higher level regions, such as FFA, for holistic processing (Haxby et al, 2000; Fairhall and Ishai, 2007; Liu et al, 2002)

Summary

Introduction

There is ample evidence to show that the processing of face information involves a distributed neural network of face-sensitive areas in the occipitotemporal cortex and beyond (Duchaine and Yovel, 2015; Haxby et al, 2000). Hierarchical models postulate that face specific processes are initiated in the OFA based on local facial features, the information is forwarded to higher level regions, such as FFA, for holistic processing (Haxby et al, 2000; Fairhall and Ishai, 2007; Liu et al, 2002). This model is supported by neuroimaging studies showing functional properties of face-selective areas and is consistent with generic local-to-global views of object processing.

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Conclusion