Abstract
How a visual stimulus is initially categorized as a face in a network of human brain areas remains largely unclear. Hierarchical neuro-computational models of face perception assume that the visual stimulus is first decomposed in local parts in lower order visual areas. These parts would then be combined into a global representation in higher order face-sensitive areas of the occipito-temporal cortex. Here we tested this view in fMRI with visual stimuli that are categorized as faces based on their global configuration rather than their local parts (two-tones Mooney figures and Arcimboldo's facelike paintings). Compared to the same inverted visual stimuli that are not categorized as faces, these stimuli activated the right middle fusiform gyrus (“Fusiform face area”) and superior temporal sulcus (pSTS), with no significant activation in the posteriorly located inferior occipital gyrus (i.e., no “occipital face area”). This observation is strengthened by behavioral and neural evidence for normal face categorization of these stimuli in a brain-damaged prosopagnosic patient whose intact right middle fusiform gyrus and superior temporal sulcus are devoid of any potential face-sensitive inputs from the lesioned right inferior occipital cortex. Together, these observations indicate that face-preferential activation may emerge in higher order visual areas of the right hemisphere without any face-preferential inputs from lower order visual areas, supporting a non-hierarchical view of face perception in the visual cortex.
Highlights
The human brain can detect a face in a visual scene in a fraction of a second (e.g., Lewis and Edmonds, 2003; Rousselet et al, 2003; Fei-Fei et al, 2007; Crouzet et al, 2010), yet the neural mechanisms subtending the initial categorization of a visual stimulus as a face remain largely unclear
The patient data was never compared to appropriate control data, the patients suffered from general visual impairments, they were tested in variants of the face/ non-face decision task, and response times were never considered
In the functional magnetic resonance imaging (fMRI) experiment with Mooney faces, PS was again as accurate as control participants (72.8%; control group average is 69.1%, SD = 8.5%; t6 = 0.41; p = 0.35; age-matched participant (AM): 83%; Crawford and Garthwaite, 2002) and as fast (1384 ms, controls’ average = 1216 ms, SD = 335 ms; t6 = 0.89; p = 0.21; AM: 1000 ms).In normal participants, we found a significant effect in the two right hemisphere higher order “face areas” (FFA, pSTS), but not in the left OFA (FFA, t = 3.33, p < 0.016; pSTS, t = 3.59, p < 0.012; left OFA, t = 1.15, p = 0.30; Table 1; Figures 4A and 5 and Figure A3A of Appendix)
Summary
The human brain can detect a face in a visual scene in a fraction of a second (e.g., Lewis and Edmonds, 2003; Rousselet et al, 2003; Fei-Fei et al, 2007; Crouzet et al, 2010), yet the neural mechanisms subtending the initial categorization of a visual stimulus as a face remain largely unclear. Neuroimaging studies have identified a set of areas in the human visual cortex that respond significantly more to pictures of faces than to other object shapes (Sergent et al, 1992) potentially playing an important role in categorization of a visual stimulus as a face These areas, as identified in functional magnetic resonance imaging (fMRI), are of few square millimeter and are located outside of well-defined retinotopic visual cortex (Halgren et al, 1999), in the lateral part of the inferior occipital lobe (“Occipital Face Area,” OFA, e.g., Gauthier et al, 2000), more anteriorly in the middle fusiform gyrus (the “Fusiform Face Area,” FFA, e.g., Kanwisher et al, 1997) and in the posterior part of the superior temporal sulcus (pSTS, e.g., Puce et al, 1998). These three areas are considered to form the core section of an extensive network of cortical areas that are sensitive to faces (Haxby et al, 2000; Ishai, 2008; Fox et al, 2009; Weiner and GrillSpector, 2010), and which can be identified in the non-human primate brain (Tsao et al, 2008).
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