Identification of lingual motor control circuits using two strains of pseudorabies virus

Abstract

First-order interneurons that project to hypoglossal motoneurons are distributed within reticular formation subdivisions in the pons and medulla in areas thought to control licking, swallowing, chewing, and respiration. Movement of the tongue in each of these functions is achieved by the coordinated action of both intrinsic and extrinsic lingual muscles. Interneuron populations that project to these different lingual motoneuronal pools appear to be largely overlapping in the reticular formation. Because of the functional coupling between intrinsic and extrinsic muscles during most tongue movements, one might predict that individual pre-hypoglossal interneurons project to multiple motoneuronal pools. To test this hypothesis, one strain of pseudorabies virus was injected into the styloglossus muscle (an extrinsic lingual muscle) and a second strain of pseudorabies virus was injected into the intrinsic lingual muscles of the anterior tongue in the same preparation. Rats were perfused with fixative 84–96 h later, and dual-labeling immunohistochemistry was performed to reveal populations of single- and double-labeled brainstem neurons. Motoneurons innervating the different lingual muscles were spatially segregated within the hypoglossal motor nucleus, and no double-labeled motoneurons were observed. In contrast, pre-hypoglossal neurons projecting to each lingual motoneuron pool were highly overlapping in the reticular formation, and many were double-labeled. These observations suggest that coactivation of lingual muscles can be achieved, at least in part, through divergent projections of first-order interneurons to anatomically and functionally distinct pools of lingual motoneurons in the hypoglossal nucleus.