Monosynaptic circuitry of trigeminal proprioceptive afferents coordinating jaw movement with visceral and laryngeal activities in rats

Abstract

Jaw movement is intimately related to various oromotor and visceral functions such as feeding, swallowing, vocalization, respiration and cardiac function. Neuronal circuitry that links jaw movement and these visceral and oromotor functions is largely unknown. The purpose of this study is to determine whether the trigeminal proprioceptive and jaw-muscle spindle afferents send axons to and synapse with the motoneurons innervating visceral organs and laryngeal muscles utilizing multiple double-labeling and physiological approaches. Double labeling of anterograde tracing combined to retrograde transport was performed by injection of biotinylated dextran amine into the mesencephalic trigeminal nucleus and cholera toxin B subunit or horseradish peroxidase into the vagus nerve and the recurrent laryngeal nerve. Mesencephalic trigeminal nucleus neuronal terminals contacted with visceral and laryngeal muscle motoneurons in the ambiguus nucleus and the nearby intermediate reticular zone. By electron microscopic observation, we confirmed that mesencephalic trigeminal nucleus terminals made asymmetric axodendritic synapses with these motoneurons. Double labeling of physiologically characterized jaw muscle spindle afferent neurons combined with anti-choline acetyltransferase immunohistochemistry showed that jaw-muscle spindle afferent boutons closely contacted choline acetyltransferase-immunoreactive motoneurons in the ambiguus nucleus and intermediate reticular zone. This report is the first to demonstrate that the trigeminal proprioceptive afferents synapsed upon visceral and laryngeal muscle motoneurons and provide neuronal networks for the jaw–visceral and jaw–laryngeal coordination.