Vibration over the larynx increases swallowing and cortical activation for swallowing

Abstract

Sensory input can alter swallowing control in both the cortex and brainstem. Electrical stimulation of superior laryngeal nerve afferents increases reflexive swallowing in animals, with different frequencies optimally effective across species. Here we determined 1) if neck vibration overlying the larynx affected the fundamental frequency of the voice demonstrating penetration of vibration into the laryngeal tissues, and 2) if vibration, in comparison with sham, increased spontaneous swallowing and enhanced cortical hemodynamic responses to swallows in the swallowing network. A device with two motors, one over each thyroid lamina, delivered intermittent 10-s epochs of vibration. We recorded swallows and event-related changes in blood oxygenation level to swallows over the motor and sensory swallowing cortexes bilaterally using functional near infrared spectroscopy. Ten healthy participants completed eight 20-min conditions in counterbalanced order with either epochs of continuous vibration at 30, 70, 110, 150, and 70 + 110 Hz combined, 4-Hz pulsed vibration at 70 + 110 Hz, or two sham conditions without stimulation. Stimulation epochs were separated by interstimulus intervals varying between 30 and 45 s in duration. Vibration significantly reduced the fundamental frequency of the voice compared with no stimulation demonstrating that vibration penetrated laryngeal tissues. Vibration at 70 and at 150 Hz increased spontaneous swallowing compared with sham. Hemodynamic responses to swallows in the motor cortex were enhanced during conditions containing stimulation compared with sham. As vibratory stimulation on the neck increased spontaneous swallowing and enhanced cortical activation for swallows in healthy participants, it may be useful for enhancing swallowing in patients with dysphagia.NEW & NOTEWORTHY Vibratory stimulation at 70 and 150 Hz on the neck overlying the larynx increased the frequency of spontaneous swallowing. Simultaneously vibration also enhanced hemodynamic responses in the motor cortex to swallows when recorded with functional near-infrared spectroscopy (fNIRS). As vibrotactile stimulation on the neck enhanced cortical activation for swallowing in healthy participants, it may be useful for enhancing swallowing in patients with dysphagia.

Keywords: functional near-infrared spectroscopy; hemodynamic response; motor cortex; sensory cortex; sensory stimulation.

Copyright © 2017 the American Physiological Society.

Figures

Fig. 1.

A vibratory device with 2 motors, each placed over the lamina on one side of the thyroid cartilage. The neck motors are connected to contacts and contained in a molded plastic neck piece. The neck piece is attached with soft adjustable ties and is connected to a controller unit. The device was supplied by Passy Muir.

Fig. 2.

A: results of the fast Fourier transform (FFT) used in LabChart 7 to analyze the spectrum and identify the lowest frequency component from the microphone signal recorded during phonation of the vowel /i/ for ~8 s with the motor turned off. The lowest peak frequency was identified at the arrow which was 195 Hz in this female subject. B: FFT of the accelerometer signal when recorded with the motor turned on while the participant was not phonating. The lowest motor frequency at the arrow was 66 Hz. C: FFT was computed from signal from the microphone recording of the same female subject when the motor was turned on and the peak frequency of the lowest frequency component at the arrow was 97 Hz. The y-axis is the dB down of the power spectrum and the x-axis is the frequency from 0 to 2 kHz.

Fig. 3.

An example of marking a swallow in LabChart. A large initial spike in the piezoelectric accelerometer signal (A) indicates hyolaryngeal elevation at swallowing onset. The first derivative of the sum Inductotrace channel (B), which flattens around zero on the y-axis at ~217.4 s, with arrows indicating the onset and offset of the apneic period. A square wave in the pulse generator (C) indicates a button press when a swallow was observed by a trained assistant.

Fig. 4.

A 3-dimensional MRI in Brainsight 2.0 software showing the location of the regions of interest in Montreal Neurological Institute standardized space in the right and left hemispheres, including motor (anterior) and sensory (posterior) areas.

Fig. 5.

An example of the plot of the event-related average of Z score changes in one location in one hemisphere in one participant showing oxygenated hemoglobin (solid line) and deoxygenated hemoglobin (dotted line) changes over time from 5 s before the onset of the swallows (−5s) to 22 s after the onset of swallows. All events are time-locked averages based on the time of onset of laryngeal elevation (at 0 s) for the onset of the pharyngeal phase of swallowing. This average is for swallows occurring between stimulations. The period of potential motion artifact for swallowing is from 0 to 2 s, the time of the early peak is between 4 and 7 s from the swallow onset and for the late peak is from 14 to 17 s from the swallow onset.

Fig. 6.

A line graph showing the peak frequency in Hz of the lowest frequency component during 8 s of phonation with the motor turned off (Phonation) and the peak frequency in Hz of the lowest frequency component during 8 s of phonation with the motor turned on (Phonation + Vibration). The solid lines are the results of the 3 male participants; the dashed lines are the results of the 3 female participants.

Fig. 7.

Line graphs depict the percent change from the sham condition in the rate of swallowing for 70-Hz stimulation (A), 150-Hz stimulation (B), and 70/110-Hz hybrid (C) stimulation. Each line is a single participant.

Fig. 8.

Mean Z scores with 95% confidence intervals (CI) of difference in oxygenated hemoglobin during vibratory stimulation and sham (no stimulation) from baseline mean and SD between −5 and 0 s before stimulation onset for different vibratory conditions 30, 70, 110, 150, 70 + 110 Hz (Hybrid), and sham (no vibration) in the left hemisphere (squares) and the right hemisphere (circles).

Fig. 9.

Mean peak Z scores with 95% confidence intervals (CI) of early and late responses combined showing difference in oxygenated hemoglobin to swallowing in the sham condition (Sham), swallowing between stimulation periods (Swallow stim off), and swallowing during stimulation periods (Swallow stim on) from baseline mean and SD between −5 and 0 s before swallow onset. The data is divided by motor (M1; diamonds) and sensory (S1; circles) regions and by right (RIGHT) and left (LEFT) hemispheres.

Fig. 10.

Mean peak Z scores with 95% confidence intervals (CI) of responses in oxygenated hemoglobin to swallowing in the motor (M1) and sensory (S1) regions for early responses between 4 and 7 s (diamonds) and late responses between 14 and 17 s (circles) after swallowing onset.

Fig. 11.

Mean peak Z scores with 95% confidence intervals (CI) of responses in oxygenated hemoglobin to swallowing are shown on the y-axis, with the following conditions on the x-axis: Sham, swallowing between stimulation periods (Swallow stim off), and swallowing during stimulation periods (Swallow stim on). The timing of responses occurred 4–7 s (diamonds) and 14–17 s (circles) after swallowing onset. The data were divided into separate graphs for the right (RIGHT) and left (LEFT) hemispheres.