Position selectivity in face-sensitive visual cortex to facial and nonfacial stimuli: an fMRI study.

David F Nichols,Hugh R Wilson,Lisa R Betts

doi:10.1002/brb3.542

Abstract

BackgroundEvidence for position sensitivity in object‐selective visual areas has been building. On one hand, most of the relevant studies have utilized stimuli for which the areas are optimally selective and examine small sections of cortex. On the other hand, visual field maps established with nonspecific stimuli have been found in increasingly large areas of visual cortex, though generally not in areas primarily responsive to faces.Methods fMRI was used to study the position sensitivity of the occipital face area (OFA) and the fusiform face area (FFA) to both standard rotating wedge retinotopic mapping stimuli and quadrant presentations of synthetic facial stimuli. Analysis methods utilized were both typical, that is, mean univariate BOLD signals and multivoxel pattern analysis (MVPA), and novel, that is, distribution of voxels to pattern classifiers and use of responses to nonfacial retinotopic mapping stimuli to classify responses to facial stimuli.ResultsPolar angle sensitivity was exhibited to standard retinotopic mapping stimuli with a stronger contralateral bias in OFA than in FFA, a stronger bias toward the vertical meridian in FFA than in OFA, and a bias across both areas toward the inferior visual field. Contralateral hemispheric lateralization of both areas was again shown using synthetic face stimuli based on univariate BOLD signals, MVPA, and the biased contribution of voxels toward multivariate classifiers discriminating the contralateral visual field. Classifiers based on polar angle responsivity were used to classify the patterns of activation above chance levels to face stimuli in the OFA but not in the FFA.ConclusionsBoth the OFA and FFA exhibit quadrant sensitivity to face stimuli, though the OFA exhibits greater position responsivity across stimuli than the FFA and includes overlap in the response pattern to the disparate stimulus types. Such biases are consistent with varying position sensitivity along different surfaces of occipito‐temporal cortex.

Highlights

Theoretically driven descriptions of the distribution of function within the visual cortex proposed a progression from initially highly position sensitive processing to later position insensitivity but with increasingly specialized processing, for example, object-selective cortex (Mishkin, Ungerleider, & Macko, 1983)
Clear differences can be observed between the occipital face area (OFA) and fusiform face area (FFA), with the OFA showing strong lateralization of hemispheres biased toward the contralateral visual field, but with both hemispheres of the FFA seeming to cluster near the vertical meridians, without as much lateralization
Further analysis of the trials for which classification was not correct showed that errors were systematically biased toward the same left-right visual field as the correct position in the OFA (t7 = 3.33, p = .013), but not necessarily in the FFA (t7 = 1.90, p = .100). These results indicate that the position sensitivity for facial stimuli in the OFA is, at least in part, driven by localized receptive field structure that is general across stimuli, but position sensitivity in the FFA likely requires facial stimuli to be used in order to observe it

Summary

| INTRODUCTION

Theoretically driven descriptions of the distribution of function within the visual cortex proposed a progression from initially highly position sensitive processing to later position insensitivity but with increasingly specialized processing, for example, object-selective cortex (Mishkin, Ungerleider, & Macko, 1983). Position sensitivity has clearly been demonstrated in face-sensitive cortex using fMRI – initially with a foveal bias (Levy, Hasson, Avidan, Hendler, & Malach, 2001; Hasson, Levy, Behrmann, Hendler, & Malach, 2003; but see Yue, Cassidy, Devaney, Holt, & Tootell, 2011), a contralateral visual field bias (Hemond, Kanwisher, & Op de Beeck, 2007), sensitivity to position along the vertical meridian (Schwarzlose, Swisher, Dang, & Kanwisher, 2008), and quadrant specificity (Kravitz, Kriegeskorte, & Baker, 2010) Such sensitivity follows logically from restricted spatial receptive fields that show limited position tolerance, as had previously been shown by object-selective IT neurons in monkeys using electrophysiology (see DiCarlo & Maunsell, 2003) and more recently in face-sensitive neural patches in monkeys using fMRI (Rajimehr, Bilenko, Vanduffel, & Tootell, 2014), but it was still necessary to show similar effects in humans. While much of the results are expected to replicate earlier findings of positional sensitivity with facial stimuli in face-s ensitive visual cortex, the novel use of standard, retinotopy stimuli will allow for a more in-depth study of the positional sensitivities within these areas

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Abstract Abstract

Findings

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