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 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, ITsPlxnD1 project 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.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
This version of the manuscript has been revised to update the Acknowledgement section.
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
LIST OF ABBREVIATIONS
- ACAd
- anterior cingulate area, dorsal part
- AId
- agranular insular area, dorsal part
- APN
- anterior pretectal nucleus
- CB
- cerebellum
- CEAc
- central amygdalar nucleus, capsular part
- CL
- central lateral nucleus of the thalamus
- CP
- caudoputamen
- FRP
- frontal pole
- GPe
- globus pallidus, external segment
- GPi
- globus pallidus, internal segment
- GRN
- gigantocellular reticular nucleus
- GU
- gustatory areas
- HPF
- hippocampal formation
- HY
- hypothalamus
- IRN
- intermediate reticular nucleus
- MD
- mediodorsal nucleus of the thalamus
- MdD
- medullary reticular nucleus, dorsal part
- MDRN
- medullary reticular nucleus
- MdV
- medullary reticular nucleus, ventral part
- MOp
- primary motor area
- MOs
- secondary motor area
- MRN
- midbrain reticular nucleus
- OLF
- olfactory areas
- ORBl
- orbital area, lateral part
- PAL
- pallidum
- PARN
- parvicellular reticular nucleus
- PCN
- paracentral nucleus
- PF
- parafascicular nucleus
- PG
- pontine gray
- PL
- prelimbic area
- PO
- posterior complex of the thalamus
- PPN
- pedunculopontine nucleus
- PSV
- principal sensory nucleus of the trigeminal
- pyx
- pyramidal decussation
- RSPagl
- retrosplenial area, lateral agranular part
- RSPd
- retrosplenial area, dorsal part
- SC
- superior colliculus
- SCm
- superior colliculus, motor related
- SI
- substantia innominata
- SMT
- submedial nucleus of the thalamus
- sp
- cortical subplate
- Spd
- spinal cord
- SPV
- spinal nucleus of the trigeminal
- SSp-bfd
- primary somatosensory area, barrel field
- SSp-ll
- primary somatosensory area, lower limb
- SSp-m
- primary somatosensory area, mouth
- SSp-n
- primary somatosensory area, nose
- SSp-tr
- primary somatosensory area, trunk
- SSp-ul
- primary somatosensory area, upper limb
- SSp-un
- primary somatosensory area, unassigned
- SSs
- secondary somatosensory area
- STN
- subthalamic nucleus
- STR
- striatum
- V
- motor nucleus of trigeminal
- VAL
- ventral anterior-lateral complex of the thalamus
- VII
- facial motor nucleus
- VISa
- anterior area
- VISam
- anteromedial visual area
- VISC
- visceral area
- VISp
- primary visual area
- VISpm
- posteromedial visual area
- VISrl
- rostrolateral visual area
- VM
- ventral medial nucleus of the thalamus
- VPM
- ventral posteromedial nucleus of the thalamus
- ZI
- zona incerta
