Joint encoding of facial identity, orientation, gaze, and expression in the middle dorsal face area

Abstract

Significance Past work on the neural mechanisms of face processing has focused on how a network of face-selective areas in the macaque monkey brain extracts facial identity. Here, we study the processing of identity, expression, and gaze information. We find that all of these signals are extracted in populations of face cells located in a face area outside the classical network. In this area, we discover a single-cell representation of facial expression that is preserved even with the changes of identity and head orientation. This face area, previously thought to be specialized for the processing of naturalistic facial movements, harbors a heterogeneous population of face cells that can process static faces to extract a wide range of socially meaningful facial information. The last two decades have established that a network of face-selective areas in the temporal lobe of macaque monkeys supports the visual processing of faces. Each area within the network contains a large fraction of face-selective cells. And each area encodes facial identity and head orientation differently. A recent brain-imaging study discovered an area outside of this network selective for naturalistic facial motion, the middle dorsal (MD) face area. This finding offers the opportunity to determine whether coding principles revealed inside the core network would generalize to face areas outside the core network. We investigated the encoding of static faces and objects, facial identity, and head orientation, dimensions which had been studied in multiple areas of the core face-processing network before, as well as facial expressions and gaze. We found that MD populations form a face-selective cluster with a degree of selectivity comparable to that of areas in the core face-processing network. MD encodes facial identity robustly across changes in head orientation and expression, it encodes head orientation robustly against changes in identity and expression, and it encodes expression robustly across changes in identity and head orientation. These three dimensions are encoded in a separable manner. Furthermore, MD also encodes the direction of gaze in addition to head orientation. Thus, MD encodes both structural properties (identity) and changeable ones (expression and gaze) and thus provides information about another animal’s direction of attention (head orientation and gaze). MD contains a heterogeneous population of cells that establish a multidimensional code for faces.