Abstract

Swallow-breathing coordination safeguards the lower airways from tracheal aspiration of bolus material as it moves through the pharynx into the esophagus. Impaired movements of the shared muscles or structures of the aerodigestive tract, or disruptions in the interaction of brainstem swallow and respiratory central pattern generators (CPGs) result in dysphagia. To maximize lower airway protection these CPGs integrate respiratory rhythm generation signals and vagal afferent feedback to synchronize swallow with breathing. Despite extensive study, the roles of central respiratory activity and vagal feedback from the lungs as key elements for effective swallow-breathing coordination remain unclear. The effect of altered timing of bronchopulmonary vagal afferent input on swallows triggered during electrical stimulation of the superior laryngeal nerves or by injection of water into the pharyngeal cavity was studied in decerebrate, paralyzed, and artificially ventilated cats. We observed two types of single swallows that produced distinct effects on central respiratory-rhythm across all conditions: post-inspiratory type swallows disrupted central-inspiratory activity without affecting expiration, whereas expiratory type swallows prolonged expiration without affecting central-inspiratory activity. Repetitive swallows observed during apnea reset the E2 phase of central respiration and produced facilitation of swallow motor output nerve burst durations. Moreover, swallow initiation was negatively modulated by vagal feedback and was reset by lung inflation. Collectively, these findings support a novel model of reciprocal inhibition between the swallow CPG and inspiratory or expiratory cells of the respiratory CPG where lung distension and phases of central respiratory activity represent a dual peripheral and central gating mechanism of swallow-breathing coordination.

Highlights

  • Swallowing, a centrally-mediated sequential activation of the muscles of the tongue, larynx, pharynx and the esophagus, ensures adequate ingestion of saliva, liquids, and food

  • Our results show an increase in duration, but not amplitude, of cranial nerve bursts within the swallow-series associated with superior laryngeal nerves (SLNs)-induced repetitive swallowing during central apnea

  • This study provides evidence for two main types of swallowbreathing relationships with differential effects on central respiratory activity

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Summary

Introduction

Swallowing, a centrally-mediated sequential activation of the muscles of the tongue, larynx, pharynx and the esophagus, ensures adequate ingestion of saliva, liquids, and food. Expiratory airflow generally precedes and follows swallow execution (Dick et al, 1993; Martin et al, 1994; Paydarfar et al, 1995; Feroah et al, 2002; Wheeler Hegland et al, 2009; Bonis et al, 2011) This relationship is thought to provide the maximum protection of the lower airways against pulmonary aspiration (Kijima et al, 1999; Yamamoto and Nishino, 2002; Martin-Harris et al, 2003, 2005; Pitts et al, 2013). Swallows occurring during the Exp-I transition or during inspiration present the highest risk for tracheal aspiration and are frequently encountered in patients with dysphagia (Terzi et al, 2007, 2010; Nishino, 2013)

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