Contrasting Specializations for Facial Motion within the Macaque Face-Processing System

Abstract

SUMMARY Facial motion transmits rich and ethologically vital information [1, 2], but how the brain interprets this complex signal is poorly understood. Facial form is analyzed by anatomically distinct face patches in the macaque brain [3, 4], and facial motion activates these patches and surrounding areas [5, 6]. Yet it is not known whether facial motion is processed by its own distinct and specialized neural machinery, and if so, what that machinery’s organization might be. To address these questions, we used functional magnetic resonance imaging (fMRI) to monitor the brain activity of macaque monkeys while they viewed low- and high-level motion and form stimuli. We found that, beyond classical motion areas and the known face patch system, moving faces recruited a heretofore-unrecognized face patch. Although all face patches displayed distinctive selectivity for face motion over object motion, only two face patches preferred naturally moving faces, while three others preferred randomized, rapidly varying sequences of facial form. This functional divide was anatomically specific, segregating dorsal from ventral face patches, thereby revealing a new organizational principle of the macaque face-processing system.

Whole-agent selectivity within the macaque face-processing system

“…Thus, two important facets of social cognition, natural motion processing and whole-animal integration, form along anatomically perpendicular axes. Only face patch AF, at the terminus of both axes, shows selectivity for both whole agents and natural facial motion (15). This convergence of streams representing complementary aspects of social agents is reminiscent of a recent theory of the human brain organization, which suggests that multiple functional pathways separately process static and dynamic animacy cues before converging at a site of integrated agent representation (35,37).…”

“…Although whole-agent integration emerges across the face patches-bolstering recent evidence that these patches represent social information beyond face form (15,36)-this integration does not develop along the same ventral-to-dorsal trajectory as natural motion selectivity, but rather the posterior-to-anterior axis of the face processing system (Fig. 5): Subadditive responses in posterior patches PL and ML gave way to additive responses in MD and MF and, eventually, a superadditive response in AF (and likely AL).…”

“…To determine how face and body patches respond to the conjunction of face and body, we first used fMRI to identify face patches PL (posterior lateral), ML (middle lateral), MF (middle fundus), MD (middle dorsal), AL (anterior lateral), and AF (anterior fundus) (15), and body patches midSTS (middle STS) and antSTS (anterior STS) (9) in four monkeys. We measured average activity within these areas while the monkeys viewed pictures of lone faces, lone bodies, and whole monkeys comprised of face and body ( Fig.…”

“…This experiment was carried out in parallel with a previously reported experiment on facial motion representations (15), included the same set of subjects, and shared stimulation, data collection, and analysis methods.…”

“…One indication that this transition may occur within the face system is that dorsal patches are specifically sensitive to the naturalness of facial motion (15), an important quality for social understanding (16). Integration of face and body is an ideal signature with which to confirm whether social processing begins in the face patches because, unlike traits such as "theory of mind" that are challenging to test with precision (17), it is easily operationalized.…”