A cortical circuit for orchestrating oromanual food manipulation

Cooperative forelimb and mouth movements during eating contribute to diet selection among vertebrates including the oromanual manipulatory skills in rodents and primates. Whereas spinal and brainstem circuits implement forelimb and orofacial actions, whether there is a specialized cortical circuit that flexibly assembles these to achieve cross-body and oromanual coordination for skilled manipulation remains unclear. Here we discover a cortical region and its cell-type-specific circuitry that orchestrates body postures and oromanual coordination for food manipulation in mice. An optogenetic screen of cortical areas and projection neuron types identified a rostral forelimb-orofacial area (RFO), wherein activation of pyramidal tract (PTFezf2) and intratelencephalic (ITPlxnD1) neurons induced concurrent posture, forelimb and orofacial eating-like movements. In a pasta-eating behavior, RFO PTFezf2 and ITPlxnD1 activity were closely correlated with picking up the pasta, adopting a sitting posture, oromanual manipulation, and hand-assisted biting. RFO inactivation and inhibition of RFO PTsFezf2 and ITsPlxnD1 impaired posture and oromanual coordination, leading to deficient pasta manipulation and biting. RFO is reciprocally connected to forelimb and orofacial sensorimotor areas as well as insular and visceral areas. Within this network, ITsPlxnD1project bilaterally to the entire network and the ventrolateral striatum and PTsFezf2 project to multiple subcortical areas associated with forelimb and orofacial control. These results suggest that ITsPlxnD1 select and coordinate the feeding program involving multiple body parts and PTsFezf2 implement the fine details of movements. Our study reveals a neural circuit basis of hand-mouth coordination for object manipulation.