Difference between hypoglossal and phrenic activities during lung inflation and swallowing in the rat

Abstract

We aimed in this study to elucidate the discharge properties and neuronal mechanisms of the dissociation between hypoglossal and phrenic inspiratory activities in decerebrate rats, which had been subjected to neuromuscular blockade and artificially ventilated. The discharge of the hypoglossal nerve and the intracellular activity of hypoglossal motoneurones were monitored during respiration and fictive-swallowing evoked by electrical stimulation of the superior laryngeal nerve, and were compared with the activity of the phrenic nerve. The hypoglossal nerve activity was characterized by its onset preceding the phrenic nerve activity ('pre-I' activity). By manipulating artificial respiration, we could augment the 'pre-I' activity, and could elicit another type of hypoglossal activity decoupled from the phrenic-associated inspiratory bursts ('decoupled' activity). We further scrutinized the correlatives of 'pre-I' and 'decoupled' activities in individual hypoglossal motoneurones. Hypoglossal motoneurones consisted of inspiratory (n = 42), expiratory (n = 18) and non-respiratory (n = 1) neurones and were classified by their swallowing activity into depolarized, hyperpolarized, hyperpolarized-depolarized and unresponsive groups. All of the inspiratory neurones were depolarized in accordance with the 'pre-I' and 'decoupled' activities, and all of the expiratory neurones were hyperpolarized during these activities. Fictive swallowing, which was characterized by its frequent emergence just after the phrenic inspiratory activity, was also evoked just after the 'decoupled' hypoglossal activity, suggesting that this activity may have similar effects on swallowing as the 'overt' inspiratory activity. Such a coupling between 'decoupled' and swallowing activities was also revealed in each motoneurone. These findings suggest that the 'pre-I' and 'decoupled' activities may reflect some internal inspiratory activity of the respiratory centre and that hypoglossal motoneurones may be driven by a distinct group of premotor neurones that possibly play a role in the coordination of respiration and swallowing.