Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination.
Feeding behaviors require intricately coordinated activation among the muscles of the jaw, tongue, and face, but the neural anatomical substrates underlying such coordination remain unclear. In this study, we investigate whether the premotor circuitry of jaw and tongue motoneurons contain elements for coordination. Using a modified monosynaptic rabies virus-based transsynaptic tracing strategy, we systematically mapped premotor neurons for the jaw-closing masseter muscle and the tongue-protruding genioglossus muscle. The maps revealed that the two groups of premotor neurons are distributed in regions implicated in rhythmogenesis, descending motor control, and sensory feedback. Importantly, we discovered several premotor connection configurations that are ideally suited for coordinating bilaterally symmetric jaw movements, and for enabling co-activation of specific jaw, tongue, and facial muscles. Our findings suggest that shared premotor neurons that form specific multi-target connections with selected motoneurons are a simple and general solution to the problem of orofacial coordination.DOI: http://dx.doi.org/10.7554/eLife.02511.001.
Department of Neurobiology, Duke University Medical Center, Durham, United States.
Edward
E
Stanek
Department of Neurobiology, Duke University Medical Center, Durham, United States.
Steven
S
Cheng
Department of Neurobiology, Duke University Medical Center, Durham, United States.
Jun
J
Takatoh
Department of Neurobiology, Duke University Medical Center, Durham, United States.
Bao-Xia
BX
Han
Department of Neurobiology, Duke University Medical Center, Durham, United States Department of Cell Biology, Duke University Medical Center, Durham, United States fan.wang@duke.edu.
Fan
F
Wang
D000818:Animals; D001369:Axons / Q000378:metabolism; D001933:Brain Stem / Q000502:physiology; D002795:Choline O-Acetyltransferase / Q000378:metabolism; D049452:Green Fluorescent Proteins / Q000378:metabolism; D007002:Hypoglossal Nerve / Q000502:physiology; D007568:Jaw / Q000502:physiology; D008406:Masseter Muscle / Q000294:innervation; D051379:Mice; D009043:Motor Activity / Q000502:physiology*; D009046:Motor Neurons / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology*; D018377:Neurotransmitter Agents / Q000378:metabolism; D010641:Phenotype; D013569:Synapses / Q000502:physiology*; D014059:Tongue / Q000502:physiology
D018377:Neurotransmitter Agents; C485184:enhanced green fluorescent protein; D049452:Green Fluorescent Proteins; D002795:Choline O-Acetyltransferase
jaw motoneurons; monosynaptic rabies virus; orofacial coordination; premotor circuit; tongue motoneurons