Swallowing-related Perihypoglossal Neurons Projecting to Hypoglossal Motoneurons in the Cat

Abstract

Although previous studies have examined the functional role of the neurons in the area ventrolateral to the hypoglossal nucleus (perihypoglossal neurons) in the trigemino-hypoglossal reflex, no convincing evidence for the direct connection from the perihypoglossal neurons to the hypoglossal motoneurons has yet been provided. In addition, the role of the perihypoglossal neurons in swallowing has not been studied. The purpose of this study was to investigate (1) the input-output relationship of the perihypoglossal neurons and (2) whether the afferent feedback was essential for their swallowing-related activity in chloralose-anesthetized cats. Before and after the cats were paralyzed, single-unit activities were recorded extracellularly from 30 perihypoglossal neurons during swallowing elicited by electrical stimulation of the superior laryngeal nerve. These perihypoglossal neurons responded with spike potentials after short latencies to stimulation of the inferior alveolar and hypoglossal nerves. The neurons also responded with spike potentials to single shocks applied to the superior laryngeal nerve, but were activated transiently at the initial phase of repetitive stimulation of the nerve and kept silent until the occurrence of swallowing before and after the animal was paralyzed. They showed burst activities in coincidence with swallowing. Averaging of intracellular potentials of a hypoglossal motoneuron by simultaneously recorded extracellular spikes of a perihypoglossal neuron revealed monosynaptic inhibitory post-synaptic potentials. We conclude that, in the region ventrolateral to the hypoglossal nucleus, there are neurons which relay trigeminal, hypoglossal, and vagal afferents. Furthermore, some of these perihypoglossal neurons are inhibitory hypoglossal premotor neurons that are involved in the central programming of swallowing.