Smiling, laughing, and overt speech production are fundamental to human everyday communication. However, little is known about how the human brain achieves the highly accurate and differentiated control of such orofacial movement during natural conditions. Here, we utilized the high spatiotemporal resolution of subdural recordings to elucidate how human motor cortex is functionally engaged during control of real-life orofacial motor behaviour. For each investigated movement class—lip licking, speech production, laughing and smiling—our findings reveal a characteristic brain activity pattern within the mouth motor cortex with both spatial segregation and overlap between classes. Our findings thus show that motor cortex relies on sparse and action-specific activation during real-life orofacial behaviour, apparently organized in distinct but overlapping subareas that control different types of natural orofacial movements. Markus Kern et al. use subdural recordings to understand how the human motor cortex is engaged during orofacial motor behavior such as speech production, laughing, and smiling. They find the motor cortex makes use of sparse and action-specific activation during these behaviors, which are organized in distinct but overlapping subareas. [ABSTRACT FROM AUTHOR]