Characterization and mechanisms of the pharyngeal swallow activated by stimulation of the esophagus

Abstract

Stimulation of the esophagus activates the pharyngeal swallow response (EPSR) in human infants and animals. The aims of this study were to characterize the stimulus and response of the EPSR and to determine the function and mechanisms generating the EPSR. Studies were conducted in 46 decerebrate cats in which pharyngeal, laryngeal, and esophageal motility was monitored using EMG, strain gauges, or manometry. The esophagus was stimulated by balloon distension or luminal fluid infusion. We found that esophageal distension increased the chance of occurrence of the EPSR, but the delay was variable. The chance of occurrence of the EPSR was related to the position, magnitude, and length of the stimulus in the esophagus. The most effective stimulus was long, strong, and situated in the cervical esophagus. Acidification of the esophagus activated pharyngeal swallows and sensitized the receptors that activate the EPSR. The EPSR was blocked by local anesthesia applied to the esophageal lumen, and electrical stimulation of the recurrent laryngeal nerve caudal to the cricoid cartilage (RLNc) activated the pharyngeal swallow response. We conclude that the EPSR is activated in a probabilistic manner. The receptors mediating the EPSR are probably mucosal slowly adapting tension receptors. The sensory neural pathway includes the RLNc and superior laryngeal nerve. We hypothesize that, because the EPSR is observed in human infants and animals, but not human adults, activation of EPSR is related to the elevated position of the larynx. In this situation, the EPSR occurs rather than secondary peristalsis to prevent supraesophageal reflux when the esophageal bolus is in the proximal esophagus.

Keywords: esophagus; pharyngeal swallow; superior laryngeal nerve.

Fig. 1.

The effect of balloon distension of the esophagus. These are recordings of geniohyoideus (GH) and cricopharyngeus (CP) electromyography (EMG) during esophago-upper esophageal sphincter (UES) contractile reflex (EUCR) or esophagus-stimulated pharyngeal swallow response (EPSR) in response to distensions of the esophagus at various esophageal locations. The EUCRs are associated with increased CP EMG, and the EPSRs are associated with increased GH and CP EMG activated in a sequential fashion. Note that only 1 EPSR was activated per stimulus, and the delays between stimulus and EPSR were variable. EPSRs were more likely to occur at higher distensions and at more rostral esophageal locations of the stimulus. Occasionally, spontaneous swallows occurred between stimuli. Bal, balloon. Balloon distensions were 1.0–2.0 cm in diameter of a 3-cm-long balloon in the esophagus at 2–17 cm from the CP.

Fig. 2.

The variability of the delay between stimulus and EPSR. These are recordings of GH, thyrohyoideus (TH), CP, and cricothyroideus (CT) EMG in response to various distensions of the cervical esophagus 5 cm from the CP. Note that the delay between stimulus and response for the EPSR varied considerably. The arrows indicate the time of initiation of the EPSR. The dimensions below the distension recordings are the diameters of the balloon distensions.

Fig. 3.

Effect of slow ramp distension of the esophagus on esophageal responses. These are TH, CP, esophagus 2 cm from the CP (E2), E4, and E6 EMG recordings during EUCR or EPSR in response to a slow ramp distension of the esophagus at the cervical (5 cm from the CP) and proximal thoracic (11 cm from CP) regions of the esophagus. Note that the EPSR occurred either during the slow distension (threshold at 34 mmHg) or at the end of the slow distension. These distensions activated the EUCR before the EPSR.

Fig. 4.

Comparison of the effects of NaCl and HCl on rate of spontaneous pharyngeal swallows (PS). These are TH, CP, E1, and E4 EMG recordings and E11 and E14 manometric recordings in response to fluid infusion, NaCl or HCl, into the proximal thoracic esophagus (8 cm from the CP). Note that HCl, but not NaCl, infusion significantly increased the rate of spontaneous pharyngeal swallows. The pharyngeal swallows are indicated by the increased TH and CP EMG in a sequential fashion. Not all pharyngeal swallows were accompanied by esophageal peristalsis (#), and not all esophageal peristalses were accompanied by pharyngeal swallows (@).

Fig. 5.

Effect of changing pH of cervical esophageal perfusate on spontaneous occurrence of pharyngeal swallows and secondary peristalses (SP). These are GH, TH, CP, and CT EMG recordings and the E7 manometric recording in response to a change in pH of the fluid perfused through the cervical esophagus. Note that selective change in pH of the thoracic esophagus from 7.2 to 1.2 greatly increased the spontaneous rate of pharyngeal swallows.

Fig. 6.

Effect of changing pH of thoracic esophageal perfusate on spontaneous occurrence of pharyngeal swallows and secondary peristalsis. These are GH, TH, and CP EMG recordings and E4 and E7 manometric recordings in response to a change in pH of the fluid perfused through the thoracic esophagus. Note that selective change in pH of the thoracic esophagus from 7.2 to 1.2 greatly increased the spontaneous rate of pharyngeal swallows and secondary peristalses.

Fig. 7.

The effect of esophageal acid exposure on the EPSR. These are TH, CP, and E2 EMG recordings during EUCR and EPSR responses to distension of the cervical esophagus before and after exposure of the esophagus to HCl for 10 min. Acid exposure increased the chance of activating the EPSR. The pressures within the distending balloons are indicated by the mmHg bar.

Fig. 8.

The effect of recurrent laryngeal nerve caudal to the cricoid cartilage (RLNc) stimulation on activation of the pharyngeal swallow response. These are GH, TH, CP, and CT EMG recordings and CP strain gauge (CP-SG) recording in response to centripetal electrical stimulation of the RLNc. Note that RLNc stimulation activated a pharyngeal swallow during the stimulation period. The vertical electrical bars on the EMG signals are the electrical artifacts of the stimulus.

Fig. 9.

Effects of lidocaine perfusion of the esophagus on EPSR and EUCR. These are GH, TH, TP, CP, and E2 EMG recordings in response to distension of a balloon in the proximal thoracic esophagus to 1.5 cm in diameter before and after lidocaine administration. Lidocaine blocked the EPSR but not the EUCR or spontaneous pharyngeal swallowing.

Fig. 10.

Graph of the effects of lidocaine perfusion of the esophagus on percent occurrence and threshold stimulus for activation of the EPSR and EUCR. Lidocaine administration significantly blocked the percent occurrence and threshold stimulus for cervical (Cerv), proximal thoracic (PThor), or average of all areas of the esophagus (Total) activation of the EPSR but not EUCR. Values are means ± SD, and the test used for EPSR was the Wilcoxon signed rank test and for EUCR was the Student's paired t-test. DThor, distal thoracic esophagus.