Patches of face-selective cortex in the macaque frontal lobe

Abstract

In primates, specialized occipital-temporal face areas support the visual analysis of faces, but it is unclear whether similarly specialized areas exist in the frontal lobe. Using functional magnetic resonance imaging in alert macaques, we identified three discrete regions of highly face-selective cortex in ventral prefrontal cortex, one of which was strongly lateralized to the right hemisphere. These prefrontal face patches may constitute dedicated modules for retrieving and responding to facial information.

Figure 1.

Face-selective patches in prefrontal cortex of four macaques. a) Face-selective patches from four macaques superimposed on coronal anatomical slices. Activated regions showed a significantly greater response to faces than to four categories of non-face objects. The first column shows the orbital face patch (PO), the second column shows the ventrolateral face patch (PL), and the third column shows the face patch at the ventral tip of the anterior bank of the inferior arcuate sulcus (PA); patches are indicated by white arrows. The AP position of each slice is indicated at the top left corner of each slice (in mm relative to the interaural canal). Sulcal labels for (a) and (b): ps: principle sulcus, al: lower ramus of arcuate sulcus, sf: Sylvan fissure, los: lateral orbital sulcus, ipd: infraprincipal dimple. b) Prefrontal face patches overlaid on reconstructed inflated left and right frontal lobes of the four monkeys. Order of monkeys from top to bottom same as in (a). c) Coronal, horizontal, and sagittal slices through the right hemisphere PO of monkey M4. d) Mean time courses extracted from the face patches shown in (a), averaged across monkeys and across hemispheres for patches that were bilateral. To generate the data shown here and in (e) below, even runs were used to define ROI’s for the face patches in each monkey, and odd runs were used to extract the time courses and activation values. Three different visual stimulation conditions were presented: faces (light grey epochs; F: human faces, M: monkey faces), non-face objects (dark grey epochs; H: hands, G: gadgets, V: vegetables and fruits, B: headless bodies), and scrambled versions of the same images (white epochs). e) Bar graph showing % fMRI signal change to faces (light grey bars) and to non-face objects (dark grey bars) in the three prefrontal face patches. Error bars indicate 95% confidence intervals. f) Top: atlas of macaque prefrontal cortex, adapted from Petrides and Pandya. Lateral view on the left, ventral view on the right. The junction between areas 9/46v, 45A, and 47/12 coincides with the anterior end of the infraprincipal dimple (ipd). ala: anterior bank of lower ramus of arcuate sulcus. Bottom: Activation to faces and non-face objects (hands, gadgets, vegetables and fruits, and bodies) versus grid-scrambled patterns. The prefrontal face patches are indicated by green outlines. In both of these monkeys (M3 and M4), the infraprinciple dimple could be seen in the anatomical MR images, and PL was located partially within this dimple. See Supplementary Text 1 for discussion of area assignments for the three prefrontal face patches.

Figure 2.

Sensitivity of prefrontal and temporal face patches to facial expression. a) Example images of neutral and expressive macaque faces used to test selectivity of prefrontal face patches for expressive versus neutral faces. b) Average time course from PO, PL, and PA to neutral faces (medium grey), expressive faces (light grey), and non-face objects (dark grey). Data averaged across three monkeys (M1, M3, M4). c) Bar graph showing % fMRI signal change to neutral faces (medium grey), expressive faces (light grey), and non-face objects (dark grey). Data averaged across three monkeys (M1, M3, M4). Error bars indicate 95% confidence intervals. d) Coronal slice showing activation to expressive versus neutral faces in monkey M1. PO was the only region activated by this contrast at p = 0.001.