Neurophysiological Organization of the Middle Face Patch in Macaque Inferior Temporal Cortex

Abstract

While early cortical visual areas contain fine scale spatial organization of neuronal properties, such as orientation preference, the spatial organization of higher-level visual areas is less well understood. The fMRI demonstration of face-preferring regions in human ventral cortex and monkey inferior temporal cortex (“face patches”) raises the question of how neural selectivity for faces is organized. Here, we targeted hundreds of spatially registered neural recordings to the largest fMRI-identified face-preferring region in monkeys, the middle face patch (MFP), and show that the MFP contains a graded enrichment of face-preferring neurons. At its center, as much as 93% of the sites we sampled responded twice as strongly to faces than to nonface objects. We estimate the maximum neurophysiological size of the MFP to be ∼6 mm in diameter, consistent with its previously reported size under fMRI. Importantly, face selectivity in the MFP varied strongly even between neighboring sites. Additionally, extremely face-selective sites were ∼40 times more likely to be present inside the MFP than outside. These results provide the first direct quantification of the size and neural composition of the MFP by showing that the cortical tissue localized to the fMRI defined region consists of a very high fraction of face-preferring sites near its center, and a monotonic decrease in that fraction along any radial spatial axis.

SIGNIFICANCE STATEMENT The underlying organization of neurons that give rise to the large spatial regions of activity observed with fMRI is not well understood. Neurophysiological studies that have targeted the fMRI identified face patches in monkeys have provided evidence for both large-scale clustering and a heterogeneous spatial organization. Here we used a novel x-ray imaging system to spatially map the responses of hundreds of sites in and around the middle face patch. We observed that face-selective signal localized to the middle face patch was characterized by a gradual spatial enrichment. Furthermore, strongly face-selective sites were ∼40 times more likely to be found inside the patch than outside of the patch.