Hypoglossal and reticular interneurons involved in oro‐facial coordination in the rat

Abstract

Chewing, swallowing, breathing, and vocalization in mammals require precise coordination of tongue movements with concomitant activities of the mimetic muscles. The neuroanatomic basis for this oro-facial coordination is not yet fully understood. After the stereotaxic microinjection of retrograde and anterograde neuronal tracers (biotin-dextran, Fluoro-Ruby, Fluoro-Emerald, and Fluoro-Gold) into the facial and hypoglossal nuclei of the rat, we report here a direct bilateral projection of hypoglossal internuclear interneurons onto facial motoneurons. We also confirm the existence of a small pool of neurons in the dorsal part of the brainstem reticular formation that project ipsilaterally to both facial and hypoglossal nuclei. For precise tracer injections, both motor nuclei were located and identified by the electrical antidromic activation of their constituent motoneurons. Injections of retrograde tracers into the facial nucleus consistently labeled neurons in the hypoglossal nucleus. These neurons prevalently lay in the ipsilateral side, were small in size, and, like classic intrinsic hypoglossal local-circuit interneurons, had several thin dendrites. Reverse experiments - injections of anterograde tracers into the hypoglossal nucleus - labeled fine varicose nerve fiber terminals in the facial nucleus. These fiber terminals were concentrated in the intermediate subdivision of the facial nucleus, with a strong ipsilateral prevalence. Double injections of different tracers into the facial and the hypoglossal nuclei revealed a small, but constant, number of double-labeled neurons located predominantly ipsilateral in the caudal brainstem reticular formation. Hypoglossal internuclear interneurons projecting to the facial nucleus, as well as those neurons of the parvocellular reticular formation that project to both facial and hypoglossal nuclei, could be involved in oro-facial coordination.

Study of the human hypoglossal nucleus: Normal development and morpho-functional alterations in sudden unexplained late fetal and infant death

“…A confirmation of the important role of the HGN interneurons in breathing control rises in our opinion from the study of Popratiloff et al [30]. These authors, through stereotaxic microinjection of retrograde and anterograde neuronal tracers into the brainstem of rats, demonstrated that HGN interneurons project to the facial nucleus, thus sustaining the involvement of the HGN not only in tongue movements but also in orofacial coordination of the mimetic muscles.…”

Anterograde Projections of the Motorcortical Tongue Area in the Saddle-Back Tamarin <i>(Saguinus fuscicollis)</i>

“…All species studied until now show a projection of the motorcortical face area into the caudodorsal medullary reticular formation [Kuypers, 1958a, c;Newman et al, 1989;Enomoto et al, 1995;Alipour et al, 1997], and this area is directly connected with the hypoglossal motoneurons [Ugolini, 1995;Fay and Norgren, 1997;Popratiloff et al, 2001]. It therefore may be assumed that the direct cortico-motoneuronal connection found in higher primates developed out of a cortico-reticulo-motoneuronal connection during primate evolution.…”

Comparative Histological Study of the Mammalian Facial Nucleus

“…The ventral part of the Japanese monkey and dolphin (both Risso's and bottlenose species) facial nuclei differed in the columnar arrangement from the other examined mammalian species. The ventromedial and ventrolateral subnuclei correspond to regions shown to communicate with cells of the motor trigeminal and hypoglossal nuclei via premotor interneurons within the reticular nuclei [14,19,22]; therefore, species differences may arise from the developmental strategy behind the evolution of mastication.…”

“…However, many important species-specific differences are seen in the motor neurons innervating the nasolabial and buccolabial branches [3,5,11,17]. In particular, the facial muscles innervated by the buccolabial branch are important muscular hydrostats for animal food acquisition [11].The facial nucleus is a final outlet for innervating a wide variety of facial movements involved in food acquisition, food transport, mastication, respiration, swallowing, and facial expression [2,12,14]. Facial subnuclear organization -such as the number of subnuclei, consistency of subnuclear boundaries, and size and distribution of motor neuron pools -varies, possibly reflecting differences in functional importance from species to species.…”

“…The facial nucleus is a final outlet for innervating a wide variety of facial movements involved in food acquisition, food transport, mastication, respiration, swallowing, and facial expression [2,12,14]. Facial subnuclear organization -such as the number of subnuclei, consistency of subnuclear boundaries, and size and distribution of motor neuron pools -varies, possibly reflecting differences in functional importance from species to species.…”