Neural Synchrony Links Sensorimotor Cortices in a Network for Facial Motor Control

Primate societies rely on the production and interpretation of social signals, in particular those displayed by the face. Facial movements are controlled, according to the dominant neuropsychological schema, by two separate circuits, one originating in medial frontal cortex controlling emotional expressions, and a second one originating in lateral motor and premotor areas controlling voluntary facial movements. Despite this functional dichotomy, cortical anatomy suggests that medial and lateral areas are directly connected and may thus operate as a single network. Here we test these contrasting hypotheses through structural and functional magnetic resonance imaging (fMRI) guided electrical stimulation and simultaneous multi-channel recordings from key face motor areas in the macaque monkey brain. These areas include medial face motor area M3 (located in the anterior cingulate cortex); two lateral face-related motor areas: M1 (primary motor) and PMv (ventrolateral premotor); and S1 (primary somatosensory cortex). Cortical responses evoked by intracortical stimulation revealed that medial and lateral areas can exert significant functional impact on each other. Simultaneous recordings of local field potentials in all face motor areas further confirm that during facial expressions, medial and lateral face motor areas significantly interact, primarily in the alpha and beta frequency ranges. These functional interactions varied across different types of facial movements. Thus, contrary to the dominant neuropsychological dogma, control of facial movements is not mediated through independent (medial/lateral) functional streams, but results from an extensive interacting sensorimotor network.