Projections to the trigeminal, facial, ambiguus, and hypoglossal motor nuclei were determined by using horseradish peroxidase histochemistry. Most of the afferent projections to these motor nuclei were from the brainstem reticular formation, frequently in areas adjacent to other synergetic motor nuclei. The reticular formation lateral to the hypoglossal nucleus and reticular structures surrounding the trigeminal motor nucleus projected to each of these other brainstem motor nuclei involved in oral-facial function. Afferent projections to these motor nuclei also were organized along the rostrocaudal axis. Within the reticular formation most of the afferent projections to the trigeminal motor nucleus originated rostral to the majority of neurons projecting to the hypoglossal and ambiguus nuclei, which in turn were rostral to the primary source of reticular afferents to the facial nucleus. In comparison, projections from the sensory trigeminal nuclei and nucleus of the solitary tract were sparse. The interneuron pools that project to the orofacial motoneurons provide one further link in understanding the brainstem substrates for integrating oral and ingestive behaviors.

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Previous behavior studies (Grill & Norgren, 1978) demonstrated that gustatory stimuli produce stereotyped orofacial movements that constitute the observable concomitants of ingestion and rejection. For further clarification of the relation between these orofacial movements (the buccal phase of ingestion) and the act of swallowing (the pharyngeal phase), electromyographic responses to intraoral sapid stimulation were recorded from a subset of orofacial and pharyngeal muscles in a freely moving chronic preparation. Activity in a jaw opening muscle (anterior digastric), a facial muscle (zygomatic), tongue protruder (genioglossus), tongue retractor (styloglossus), and a pharyngeal constrictor used in swallowing (thyropharyngeus) differentiated between ingestive sequences to water (W), sucrose (S), and NaCl (N) and a rejection response elicited by quinine monohydrochloride (Q). Ingestion responses to W, S, and N consisted of rhythmic alterations between genioglossus and styloglossus activity (intraoral licks) accompanied by episodic bursts of pharyngeal constrictor activity (swallowing). Both bout duration and the number of swallows increased at higher concentrations of S and N. In contrast, Q stimulation elicited a rejection response, characterized by several licks and followed by long duration contractions of the zygomatic and anterior digastric muscles (gapes). During gapes, styloglossus activity rather than genioglossus activity was simultaneous with that of the anterior digastric. At higher concentrations of Q, the latency to gape decreased and the latency to swallow increased. The earliest components of the response to S, N, or Q were virtually indistinguishable from one another, results suggesting that tactile (fluid) stimulation initiates the ingestive sequence and that gustatory stimuli modulate this ongoing activity.

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Numerous studies suggest an essential role for the intermediate (IRt) and parvocellular (PCRt) reticular formation (RF) in consummatory ingestive responses. Although the IRt and PCRt contain a large proportion of neurons with projections to the oromotor nuclei, these areas of the RF are heterogeneous with respect to neurotransmitter phenotypes. Glutamatergic, GABAergic, cholinergic, and nitrergic neurons are all found in the PCRt and IRt, but the projections of neurons with these phenotypes to the motor trigeminal (mV) and hypoglossal nucleus (mXII) has not been fully evaluated. In the present study, after small injections of Fluorogold (FG) into mV and mXII, sections were processed immunohistochemically to detect retrogradely labeled FG neurons in combination with the synthetic enzymes for nitric oxide (nitric oxide synthase) or acetylcholine (choline acetyltransferase) or in situ hybridization for the synthetic enzyme for GABA (GAD65/67) or the brainstem vesicular transporter for glutamate (VGLUT2). In three additional cases, FG injections were made into one motor nucleus and cholera toxin (subunit b) injected in the other to determine the presence of dual projection neurons. Premotor neurons to mXII (pre-mXII) were highly concentrated in the IRt. In contrast, there were nearly equal proportions of premotor-trigeminal neurons (pre-mV) in the IRt and PCRt. A high proportion of pre-oromotor neurons were positive for VGLUT2 (pre-mXII: 68%; pre-mV: 53%) but GABAergic projections were differentially distributed with a greater projection to mV (25%) compared to mXII (8%). Significant populations of cholinergic and nitrergic neurons overlapped pre-oromotor neurons, but there was sparse double-labeling (<10%). The IRt also contained a high proportion of neurons that projected to both mV and MXII. These different classes of premotor neurons in the IRt and PCRt provide a substrate for the rhythmic activation of lingual and masticatory muscles.

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