A cortical circuit for orchestrating oromanual food manipulation

Abstract

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 PTFezf2and ITPlxnD1activity were closely correlated with picking up the pasta, adopting a sitting posture, oromanual manipulation, and hand-assisted biting. RFO inactivation and inhibition of RFO PTsFezf2and ITsPlxnD1impaired 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 PTsFezf2project to multiple subcortical areas associated with forelimb and orofacial control. These results suggest that ITsPlxnD1select and coordinate the feeding program involving multiple body parts and PTsFezf2implement the fine details of movements. Our study reveals a neural circuit basis of hand-mouth coordination for object manipulation.

Continuous estimation of reaching space in superficial layers of the motor cortex

“…It is only recently, however, that studies have begun to investigate how directional arm movements are encoded in the rodent cortex 8,27,28 . Through anatomical, optogenetic and microstimulation experiments, the MAC has been pinpointed as the principal cortical region related to the control of reaching in mice 6,3,8 . Therefore, we aimed to determine the tuning properties of reach-related neurons within this region by performing two-photon microscopy imaging of layer 2/3 neurons while head-fixed mice reached for drops of water presented at 3 different locations around their snout (Left, Center and Right, Figure 1ab, supplementary figure 1).…”

“…Manipulating objects in our surroundings is an integral part of our everyday life and is key to survival. Rodents, much like primates, rely on their hands to manipulate and eat food and deploy motor programs specially adapted to each type of food 1,2,3 . Coordination and execution of such complex behaviors occur at multiple levels of the neuraxis, with the motor cortex playing a central role 4,5 .…”

“…Coordination and execution of such complex behaviors occur at multiple levels of the neuraxis, with the motor cortex playing a central role 4,5 . For instance, microstimulation, inactivation, anatomical and physiological experiments suggest that the medial part of the anterior motor cortex (Medial Anterior Cortex, MAC 6 ) is involved in controlling reach-to-grasp movements in the mouse 7,3,8 . Moreover, there is convergent evidence across different species that the cerebral cortex is functionally organized into distributed action maps that orchestrate ethologically relevant behaviors [9][10][11][12] .…”

Cortico-thalamic communication for action coordination in a skilled motor sequence

“…Laboratory mice display skilled motor behaviors such as reach, grasp, and manipulate to consume food and water 2,36,37 . Recent technical advances in machine learning-powered behavior tracking and analysis 38 , wide-field imaging of neural activities 39–41 , and cell-type targeted recording and manipulation enable a multi-faceted and integrated analysis of the neural circuit basis of these behaviors 42 .…”

“…To date, most neural circuit studies in mice have focused on movement parts, e.g. the forelimb 40,43–48 or orofacial movement 49–55 , but not their serial order and coordination across body as an integrated behavior (but see 36,56 ). Here, through high-resolution quantitative analysis of a chemosensory-guided reach and grasp to drink behavior (RGD) 45 , we have revealed the serial ordering and coordination of a set of forelimb (aim, advance, supinate, grasp, withdraw) and oral (mouth open, lick) actions to retrieve water to drink.…”