Spatio-temporal dynamics and laterality effects of face inversion, feature presence and configuration, and face outline.

Ksenija Marinkovic,Anders M. Dale,Maureen G. Courtney,Eric Halgren,Thomas Witzel

doi:10.3389/fnhum.2014.00868

Abstract

Although a crucial role of the fusiform gyrus (FG) in face processing has been demonstrated with a variety of methods, converging evidence suggests that face processing involves an interactive and overlapping processing cascade in distributed brain areas. Here we examine the spatio-temporal stages and their functional tuning to face inversion, presence and configuration of inner features, and face contour in healthy subjects during passive viewing. Anatomically-constrained magnetoencephalography (aMEG) combines high-density whole-head MEG recordings and distributed source modeling with high-resolution structural MRI. Each person's reconstructed cortical surface served to constrain noise-normalized minimum norm inverse source estimates. The earliest activity was estimated to the occipital cortex at ~100 ms after stimulus onset and was sensitive to an initial coarse level visual analysis. Activity in the right-lateralized ventral temporal area (inclusive of the FG) peaked at ~160 ms and was largest to inverted faces. Images containing facial features in the veridical and rearranged configuration irrespective of the facial outline elicited intermediate level activity. The M160 stage may provide structural representations necessary for downstream distributed areas to process identity and emotional expression. However, inverted faces additionally engaged the left ventral temporal area at ~180 ms and were uniquely subserved by bilateral processing. This observation is consistent with the dual route model and spared processing of inverted faces in prosopagnosia. The subsequent deflection, peaking at ~240 ms in the anterior temporal areas bilaterally, was largest to normal, upright faces. It may reflect initial engagement of the distributed network subserving individuation and familiarity. These results support dynamic models suggesting that processing of unfamiliar faces in the absence of a cognitive task is subserved by a distributed and interactive neural circuit.

Highlights

Faces have captured a great deal of attention in the neuroimaging field, resulting in important insights into the brain networks that underlie material-specific processing
Generators of face-induced N170 are highly consistent with the fMRI activity in the right fusiform gyrus (FG) (Puce et al, 1997) fMRI studies confirm engagement of distributed occipital, temporal, and frontal areas (Ishai et al, 2004; Chan and Downing, 2011)
It propagates anteriorly via the ventral visual stream to the predominantly right ventral temporal areas peaking at ∼160 ms (M160), and further on to the anterior ventrolateral temporal and prefrontal regions at ∼240 ms (M240)

Summary

Introduction

Faces have captured a great deal of attention in the neuroimaging field, resulting in important insights into the brain networks that underlie material-specific processing. Studies using temporally precise methodology such as ERPs (Event-Related Potentials) and MEG (Magnetoencephalography) reveal a face-sensitive deflection peaking at around 170 ms (N170 and its magnetic counterpart M170) estimated to that region (Lu et al, 1991; Halgren et al, 2000; Liu et al, 2000; Watanabe et al, 2003; Schweinberger et al, 2007; Eimer, 2011; Miki et al, 2011; Rossion and Jacques, 2011; Taylor et al, 2011) Intracranial studies confirm both the timing and the location of the primary generator of these potentials in the inferotemporal region (Allison et al, 1994; Halgren et al, 1994a; McCarthy et al, 1997; Puce et al, 1997; Barbeau et al, 2008) and indicate that the face processing is subserved by a distributed network comprising anterior temporal and prefrontal regions (Halgren et al, 1994b; Klopp et al, 1999; Marinkovic et al, 2000; Barbeau et al, 2008). Generators of face-induced N170 are highly consistent with the fMRI activity in the right fusiform gyrus (FG) (Puce et al, 1997) fMRI studies confirm engagement of distributed occipital, temporal, and frontal areas (Ishai et al, 2004; Chan and Downing, 2011).

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