Swallow Motor Pattern Is Modulated by Fixed or Stochastic Alterations in Afferent Feedback

Abstract

Afferent feedback can appreciably alter the pharyngeal phase of swallow. In order to measure the stability of the swallow motor pattern during several types of alterations in afferent feedback, we assessed swallow during a conventional water challenge in four anesthetized cats, and compared that to swallows induced by fixed (20 Hz) and stochastic (1-20Hz) electrical stimulation applied to the superior laryngeal nerve. The swallow motor patterns were evaluated by electromyographic activity (EMG) of eight muscles, based on their functional significance: laryngeal elevators (mylohyoid, geniohyoid, and thyrohyoid); laryngeal adductor (thyroarytenoid); inferior pharyngeal constrictor (thyropharyngeus); upper esophageal sphincter (cricopharyngeus); and inspiratory activity (parasternal and costal diaphragm). Both the fixed and stochastic electrical stimulation paradigms increased activity of the laryngeal elevators, produced short-term facilitation evidenced by increasing swallow durations over the stimulus period, and conversely inhibited swallow-related diaphragm activity. Both the fixed and stochastic stimulus conditions also increased specific EMG amplitudes, which never occurred with the water challenges. Stochastic stimulation increased swallow excitability, as measured by an increase in the number of swallows produced. Consistent with our previous results, changes in the swallow motor pattern for pairs of muscles were only sometimes correlated with each other. We conclude that alterations in afferent feedback produced particular variations of the swallow motor pattern. We hypothesize that specific SLN feedback might modulate the swallow central pattern generator during aberrant feeding conditions (food/liquid entering the airway), which may protect the airway and serve as potentially important clinical diagnostic indicators.

Keywords: deglutition; diaphragm; electrical stimulation; facilitation; schluckatmung; stochastic; swallow.

FIGURE 1

Example trial of the stochastic electrical stimulation condition illustrating the stimulation artifact and plot of stimulation frequency in Hz. Activity on the thyrohyoid marks the occurrence of the eight swallows. Note the amplitude and duration facilitation on the thyrohyoid EMG and the duration facilitation on the thyroarytenoid EMG. The stimulus artifact is also present on the thyroarytenoid EMG.

FIGURE 2

Representative EMG examples of repetitive swallow during water infusion and with stochastic electrical stimulation of the SLN. This example demonstrates the effect of condition on EMG amplitude with a global increase in mylohyoid, geniohyoid, thyrohyoid and a decrease in the parasternal and costal diaphragm. Additionally, the gray arrows indicate the short-term facilitation across the swallow series on the thyrohyoid and thyropharyngeus. Note the differential response of the geniohyoid and thyrohyoid to the stimulation even though both are innervated by the same nerve. *Labels a laryngeal adductor reflex. All EMGs in this figure have been integrated, and the tonic activity on the thyroarytenoid EMG is stimulus artifact.

FIGURE 3

(A) Example of changes in the swallow pattern produced by fixed and stochastic frequency stimulation with a water swallow for comparison. There are small changes in EMG initiation with the stimulation conditions. The vertical dotted line marks onset of the relaxation of the upper esophageal sphincter (UES), which allows the bolus to pass into the esophagus. Diaphragm activity (termed “schluckatmung”) is present during the water swallow. Short-term amplitude facilitation from the first to the ninth swallow is seen in EMGs of the mylohyoid with fixed frequency stimulation, and in the thyrohyoid and thyropharyngeus with stochastic stimulation. Artifact is present on EMGs with stimulation. (B) Box plots of swallow durations for bouts of repeated swallows, during different simulation conditions (box heights are standardized across all three conditions). *Represents significance p < 0.05.