Differential innervation of protruder and retractor muscles of the tongue in rat

Abstract

Protrusion and retraction of the tongue are essential components of such orofacial behaviors as mastication, respiration, and swallowing. Stimulation of the medial branch of the hypoglossal nerve yields tongue protrusion, while stimulation of the lateral branch yields tongue retraction in rat. We exploited the transsynaptic transport capabilities of pseudorabies virus to determine specific circuits that innervate protruder and retractor muscles of the rat tongue. Each group of muscles is innervated by distinct populations of hypoglossal motoneurons: caudal ventral and ventrolateral motoneurons form the largest proportion of those innervating protruders, whereas rostral dorsal motoneurons innervate retractors. Our primary finding was differential innervation of protruder and retractor motoneurons by premotoneurons in the lateral tegmental field: premotoneurons innervating protruder motoneurons were more ventral and ventromedial than those innervating retractor motoneurons. In addition, protruder motoneurons received projections from the ipsilateral lateral parabrachial nucleus but not spinal trigeminal nucleus or medial and ventral subnuclei of the solitary tract; the converse was true for retractor motoneurons. These results suggest segregation of functional networks that control hypoglossal motoneurons. The dorsal medulla, in or around the solitary tract, contains neurons specific to retractor motoneurons, and the region ventrolateral to the hypoglossal nucleus contains circuitry specific to protruder motoneurons. Common innervation of medial and lateral branch motoneurons is provided by premotoneurons in the raphe and gigantocellular reticular formation of the medial medulla. The midline medullary nuclei with diverse projections may coordinate complex behavior or modulate general motoneuron excitability, whereas the lateral reticular formation, with anatomically discrete projections, may control motoneurons that contribute to distinct orofacial behaviors.