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Cortex drives orofacial behaviors through distinct brainstem networks

Abstract

Focal activation of motor cortex has been shown to enact behaviorally meaningful motor output. These include defensive behaviors, ethological limb movements, and chewing. Yet the details of how the cortical circuitry interfaces with the brainstem premotor circuits is unknown. We studied the hierarchical nature of this control with respect to orofacial motor acts that involve the vibrissae, jaw, and forelimb. The spinal trigeminal nucleus pars oralis (SpVO) and interpolaris rostralis (SpVIr) contain premotor neurons known to directly synapse on vibrissa, jaw, and forelimb motoneurons. In addition to cortical input, SpVO and SpVIr receive direct sensory signals from the periphery. Their ability to integrate descending motor input and peripheral sensory information positions them as ideal candidates to delimit the specificity of cortex-to-brainstem-to-muscle feed forward networks. Here we show that two distinct clusters of premotor neurons, one in SpVO and a second in SpVIr, control partially overlapping sets of motor actions. We used a transectional virus strategy to encode a red-shifted channelrhodopsin (ChR) in SpVO- and SpVIr-projecting motor cortex neurons. Activation of these two different cortical populations evokes distinct muscle activation during long stimuli. Similar stimulations of localized regions of motor cortex in Thy1-ChR mice show patterns of muscle activity and forelimb and jaw movements that correspond to behaviorally meaningful movements. All together, our data illustrates the functional specificity of motor circuits that originate in cortex and descend onto specific premotor populations. We suggest that the specificity of projections from neurons in motor cortex to premotor nuclei is a major determinate in the coordination of motor actions into behavior.

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