Patches with links: a unified system for processing faces in the macaque temporal lobe

Abstract

The brain processes objects through a series of regions along the ventral visual pathway, but the circuitry subserving the analysis of specific complex forms remains unknown. One complex form category, faces, selectively activates six patches of cortex in the macaque ventral pathway. To identify the connectivity of these face patches, we used electrical microstimulation combined with simultaneous functional magnetic resonance imaging. Stimulation of each of four targeted face patches produced strong activation, specifically within a subset of the other face patches. Stimulation outside the face patches produced an activation pattern that spared the face patches. These results suggest that the face patches form a strongly and specifically interconnected hierarchical network.

Fig. 1.

Face-selective patches in monkey M1. (A) The flattened cortical surfaces (“flatmaps”) from both hemispheres show regions significantly more activated by faces than by other objects. Computational flattening involves distorting the spatial arrangement of the data, and under-estimates the size of the sulci (shown in dark grey). Anatomical labels: sts: superior temporal sulcus, sf: Sylvan fissure, ips: intraparietal sulcus, ls: lunate sulcus, ios: inferior occipital sulcus, ots: occipitotemporal sulcus. (B) The same contrast overlaid on high resolution coronal slices from monkey M1. The anterior-posterior position of each slice in mm relative to the interaural line is given in the top right corner; the left hemisphere is shown on the left. The face patches are labeled as in (A). (C) Mean time courses extracted from the six face patches of the right hemisphere. Three different visual stimulation conditions were presented: faces (green epochs, F: human faces, M: monkey faces), objects (orange epochs, H: hands, G: gadgets, V: vegetables and fruits, B: monkey bodies), and scrambled versions of the same images (white epochs).

Fig. 2.

Brain regions activated by microstimulation in the lateral middle face patch (ML) of monkey M1. (A) The position of the electrode in relation to the face patches (indicated by green outlines) in sagittal and coronal MRI slices; the tip of the electrode was located 3.5 mm anterior to the inter-aural line. (B) Selectivity profile of the last neuron recorded before stimulation. The bars show the mean response of this unit to images from eight different image categories (faces, fruits, gadgets, hands, bodies, monkey body parts, monkey bodies, and scrambles), error bars 95% confidence intervals. (C) Areas significantly activated by microstimulation versus no microstimulation overlaid on the flatmap. The face patches (cf. Fig. 1) are indicated by the green outlines. The stimulation site inside ML is marked by an “x”. (D) The same functional contrast overlaid on coronal slices. The face patches are indicated by green outlines. The “+” indicates the approximate stimulation site (the slice containing the actual stimulation site, at +3.5, is not included in this mosaic). (E) Mean time courses from the six face patches in the right hemisphere. Microstimulation blocks (gray epochs) were interleaved with fixation only blocks (white epochs).

Fig. 3.

Brain regions activated by microstimulation in the anterior lateral face patch (AL) of monkey M1. Same conventions as Fig. 2. (A) Electrode position in AL. (B) Example of neuronal selectivity. (C) The contrast microstimulation versus no microstimulation revealed microstimulation-induced activity in four discrete patches in the temporal lobe coinciding with AL (the stimulation site), AF, ML, and MF, as well as a fifth patch of faint activation coinciding with AM. PL was the only face patch not activated. (D) The same contrast overlaid on coronal slices. (E) Time courses from the six face patches of the right hemisphere.

Fig. 4.

Brain regions activated by microstimulation outside the lateral middle face patch (ML) in monkey M1. Same conventions as Fig. 2. (A) Electrode position just posterior to ML. (B) Example of neuronal selectivity. (C) The contrast microstimulation versus no microstimulation revealed microstimulation-induced activity around the stimulation site as well as in a distinct patch anterior to ML. (D) The same contrast overlaid on coronal slices. Note how the activation spared most of PL and the other face patches. (E) Time courses from the patch just anterior to ML and from ML.