Intracellular activity of motoneurons of the rostral nucleus ambiguus during swallowing in sheep.

Abstract

The nervous mechanisms that generate swallowing are still largely unknown. It has been suggested that a central pattern generator that contains a serial network of linked neurons must produce the successive excitation of motoneurons (Mns) and then the sequential activation of muscle through excitatory connections. Inhibitory connections have also been envisioned but never evidenced at the membrane level of the swallowing neurons. We investigated, by intracellular recordings, the behavior of 96 Mns in the rostral nucleus ambiguus during swallowing induced by application of superior laryngeal nerve stimulation to anesthetized sheep. The Mns were identified by antidromic activation following stimulation of glossopharyngeal, pharyngoesophageal, or cervical vagal nerves. Nine Mns showed a bell-shaped depolarization during the buccal or the early pharyngeal stage of swallowing. They probably projected to muscles of the soft palate (palatopharyngeal) and upper pharynx (stylopharyngeal, hyopharyngeal). Thirty-eight Mns exhibited a chloride-dependent hyperpolarization, indicating that they were under an active inhibition throughout the buccopharyngeal stage of swallowing. These Mns constitute a heterogeneous pool: some of them, producing spontaneous inspiratory discharges, probably innervated laryngeal or pharyngeal muscles; others might also be Mns of the esophagus, whose swallowing pattern was modified because of the anesthesia (suppression of the esophageal peristalsis). Forty-nine Mns showed a chloride-dependent hyperpolarization with a variable duration at the onset of swallowing, followed by a depolarization that could take place during either the buccopharyngeal (HD1-Mns) or the esophageal (HD2- and HD3-Mns) stage of deglutition. HD1-Mns probably projected to the median and inferior constrictors of the pharynx. HD2-Mns produced depolarizations with longer latencies and durations than those of the HD1-Mns. They probably projected to either the superior esophageal sphincter or the cervical esophagus (CE). HD3-Mns showed a buccopharyngeal hyperpolarization that was followed first by a lower-amplitude hyperpolarization accompanying the proximal CE contraction and then by a delayed depolarization. These Mns probably innervated the inferior CE or thoracic esophagus. We conclude that the initial inhibition exerted on the HD-Mns, by delaying the excitation of Mns, may play a role in the nervous mechanisms involved in temporal organization of the swallowing motor sequence. We suggest that swallowing disorders in humans such as dysphagia by failure of cricopharyngeal relaxation, diffuse esophageal spasm, and achalasia might be caused by impaired inhibitory mechanisms.