Faces are represented holistically in the human occipito-temporal cortex

Abstract

Two identical top parts of a face photograph look different if their bottom parts differ. This perceptual illusion, the ‘face composite effect’, is taken as strong evidence that faces are processed as a whole rather than as a collection of independent features. To test the hypothesis that areas responding preferentially to faces in the human brain represent faces holistically, we recorded functional magnetic resonance imaging (fMRI) during an adaptation paradigm with the composite face illusion. In both the middle fusiform gyrus (MFG) and the inferior occipital gyrus (IOG), we observed a significantly larger response to the same top face when it was aligned with different bottom parts than with the same bottom part, with a most robust effect in the right middle fusiform gyrus. This difference was not found when the top and the bottom face parts were spatially misaligned or when the faces were presented upside-down. These findings indicate that facial features are integrated into holistic face representations in areas of the human visual cortex responding preferentially to faces.

Introduction

It has long been noted that a human face is perceived as an undecomposed whole rather than as collection of individual features (Galton, 1883). Holistic face processing has been empirically demonstrated in behavioral studies, showing that the identification of a facial feature is highly dependent on the whole face context (e.g. Sergent, 1984a, Young et al., 1987, Tanaka and Farah, 1993). However, it remains unknown how individual features are integrated into holistic face representations in the human brain. Neuroimaging studies identified several occipito-temporal cortical areas responding preferentially to faces in humans, with a right hemispheric dominance (e.g. Sergent et al., 1992, Puce et al., 1995, Kanwisher et al., 1997, Rossion et al., 2000). Two of these areas are located in the ventral pathway, in the lateral middle fusiform gyrus (MFG), also known as the “fusiform face area” (‘FFA’, Kanwisher et al., 1997), and posterior to it, in a region of the inferior occipital cortex (IOG), also known as the “occipital face area” (‘OFA’, Gauthier et al., 2000).¹ These areas play a critical role in the extraction of individual face representations (Gauthier et al., 2000, Rossion et al., 2003, Grill-Spector et al., 2004, Schiltz et al., 2006). In line with the hierarchical nature of the primate visual system (Felleman and Van Essen, 1991), it has been proposed that the face-sensitive neurons of the inferior occipital gyrus (IOG) represent facial features, whereas whole facial identities would be represented in the middle fusiform gyrus (MFG) (Haxby et al., 2000).

To identify the cortical areas in the human brain which represent faces holistically, we designed an fMR-adaptation paradigm (Grill-Spector and Malach, 2001, Henson, 2003, Grill-Spector et al., 2006) using the most compelling demonstration of holistic face processing reported in the behavioral literature, namely the ‘composite face effect’ (Young et al., 1987). In the ‘composite face effect’, two identical top parts of a face are perceived as being different if their respective bottom parts belong to different identities. However, this perceptual illusion vanishes if the top and the bottoms parts of the faces are laterally offset (i.e. misaligned) or inverted (Fig. 1) (Young et al., 1987). The composite face effect has been observed for familiar and unfamiliar faces, in recognition or face matching experiments (e.g. Young et al., 1987, Le Grand et al., 2004, Goffaux and Rossion, in press). Here, we used a 2 × 2 block design with the factors ‘image format’ and ‘repetition’ to test for a neuronal composite effect. In areas coding faces holistically, we hypothesized to find a larger response in the ‘different’ compared to the ‘identical’ face condition (fMR-adaptation), but only when the top and the bottom parts were spatially aligned and the faces were presented upright. That is, when subjects have the subjective impression of viewing different top parts of faces during a block of trials (Fig. 1).