Automatic orofacial behaviors remap within cortical substrates for voluntary motor control in freely moving primates

Abstract

Orofacial behaviors, like yawning and emotional facial expressions, involve phylogenetically conserved subcortical circuits. Yet, their context-dependent modulation in primates suggests overlooked cortical contributions. Here, we wirelessly recorded from 640 ventral motor and premotor sites in two freely moving macaques during spontaneous orofacial actions combining automatic and voluntary components to varying degrees (yawning, threat, bite, drink). We identified coupling between synaptic input (local field potential) and spiking output in 169 spatially distributed sites during yawning, while threat display was sparsely represented. Yawn-related sites exhibited an early beta-band suppression followed by high-gamma power enhancement. Of 401 isolated single neurons, 95 (predominantly putative medium-sized pyramidal cells) encoded yawning, mostly together with voluntary biting and drinking actions. No modulation was found during the observation of yawning by conspecifics. Yawn-related units either switched or maintained their mouth opening/closing tuning across yawning and more voluntary actions, suggesting counteracting and synergistic downstream influences on yawning motor control. In contrast, threat-related units predominantly preserved their opening/closing tuning during biting and drinking. Head-free intracortical microstimulation of sites hosting yawn-related units preferentially evoked localized mouth and face movements, supporting their causal role in orofacial motor control. Finally, projecting neural activity into a low-dimensional manifold showed that voluntarily controlled and largely automatic behaviors engaged distinct population dynamics while preserving the discriminability of individual orofacial displays. These findings reveal that cortical substrates of voluntary motor control can be recruited to shape otherwise automatic orofacial displays.