Christopher J. Poletto

Effects of Surface Electrical Stimulation Both at Rest and During Swallowing in Chronic Pharyngeal Dysphagia

We tested two hypotheses using surface electrical stimulation in chronic pharyngeal dysphagia: that stimulation (1) lowered the hyoid bone and/or larynx when applied at rest, and (2) increased aspiration, penetration, or pharyngeal pooling during swallowing. Bipolar surface electrodes were placed on the skin overlying the submandibular and laryngeal regions. Maximum tolerated levels of stimulation were applied while patients held their mouth closed at rest. Videofluoroscopic recordings were used to measure hyoid movements in the superior-inferior and anterior-posterior dimensions and the subglottic air column position while stimulation was on or off. Patients swallowed 5 ml liquid when stimulation was off, at low sensory stimulation levels, and at maximum tolerated levels (motor). Speech pathologists, blinded to condition, tallied the frequency of aspiration, penetration, pooling, and esophageal entry from videofluorographic recordings of swallows. Only significant (p = 0.0175) hyoid depression occurred during stimulation at rest. Aspiration and pooling were significantly reduced only with low sensory threshold levels of stimulation (p = 0.025) and not during maximum levels of surface electrical stimulation. Those patients who had reduced aspiration and penetration during swallowing with stimulation had greater hyoid depression during stimulation at rest (p = 0.006). Stimulation may have acted to resist patients’ hyoid elevation during swallowing.

Sensory stimulation activates both motor and sensory components of the swallowing system

Volitional swallowing in humans involves the coordination of both brainstem and cerebral swallowing control regions. Peripheral sensory inputs are necessary for safe and efficient swallowing, and their importance to the patterned components of swallowing has been demonstrated. However, the role of sensory inputs to the cerebral system during volitional swallowing is less clear. We used four conditions applied during functional magnetic resonance imaging to differentiate between sensory, motor planning, and motor execution components for cerebral control of swallowing. Oral air pulse stimulation was used to examine the effect of sensory input, covert swallowing was used to engage motor planning for swallowing, and overt swallowing was used to activate the volitional swallowing system. Breath-holding was also included to determine whether its effects could account for the activation seen during overt swallowing. Oral air pulse stimulation, covert swallowing and overt swallowing all produced activation in the primary motor cortex, cingulate cortex, putamen and insula. Additional regions of the swallowing cerebral system that were activated by the oral air pulse stimulation condition included the primary and secondary somatosensory cortex and thalamus. Although air pulse stimulation was on the right side only, bilateral cerebral activation occurred. On the other hand, covert swallowing minimally activated sensory regions, but did activate the supplementary motor area and other motor regions. Breath-holding did not account for the activation during overt swallowing. The effectiveness of oral-sensory stimulation for engaging both sensory and motor components of the cerebral swallowing system demonstrates the importance of sensory input in cerebral swallowing control.

Human Brain Activation during Phonation and Exhalation: Common Volitional Control for Two Upper Airway Functions

Phonation is defined as a laryngeal motor behavior used for speech production, which involves a highly specialized coordination of laryngeal and respiratory neuromuscular control. During speech, brief periods of vocal fold vibration for vowels are interspersed by voiced and unvoiced consonants, glottal stops and glottal fricatives (/h/). It remains unknown whether laryngeal/respiratory coordination of phonation for speech relies on separate neural systems from respiratory control or whether a common system controls both behaviors. To identify the central control system for human phonation, we used event-related fMRI to contrast brain activity during phonation with activity during prolonged exhalation in healthy adults. Both whole-brain analyses and region of interest comparisons were conducted. Production of syllables containing glottal stops and vowels was accompanied by activity in left sensorimotor, bilateral temporoparietal and medial motor areas. Prolonged exhalation similarly involved activity in left sensorimotor and temporoparietal areas but not medial motor areas. Significant differences between phonation and exhalation were found primarily in the bilateral auditory cortices with whole-brain analysis. The ROI analysis similarly indicated task differences in the auditory cortex with differences also detected in the inferolateral motor cortex and dentate nucleus of the cerebellum. A second experiment confirmed that activity in the auditory cortex only occurred during phonation for speech and did not depend upon sound production. Overall, a similar central neural system was identified for both speech phonation and voluntary exhalation that primarily differed in auditory monitoring.

Functional neuroanatomy of human voluntary cough and sniff production

Cough and sniff are both spontaneous respiratory behaviors that can be initiated voluntarily in humans. Disturbances of cough may be life threatening, while inability to sniff impairs the sense of smell in neurological patients. Cortical mechanisms of voluntary cough and sniff production have been predicted to exist; however, the localization and function of supramedullary areas responsible for these behaviors are poorly understood. We used functional magnetic resonance imaging to identify the central control of voluntary cough and sniff compared with breathing. We determined that both voluntary cough and sniff require a widespread pattern of sensorimotor activation along the Sylvian fissure convergent with voluntary breathing. Task-specific activation occurred in a pontomesencephalic region during voluntary coughing and in the hippocampus and piriform cortex during voluntary sniffing. Identification of the localization of cortical activation for cough control in humans may help potential drug development to target these regions in patients with chronic cough. Understanding the sensorimotor sniff control mechanisms may provide a new view on the cerebral functional reorganization of olfactory control in patients with neurological disorders.

The Effect of Surface Electrical Stimulation on Vocal Fold Position

Objectives/Hypothesis: Closure of the true and false vocal folds is a normal part of airway protection during swallowing. Individuals with reduced or delayed true vocal fold closure can be at risk for aspiration and may benefit from intervention to ameliorate the problem. Surface electrical stimulation is currently used during therapy for dysphagia, despite limited knowledge of its physiological effects.

Suppression of Thyroarytenoid Muscle Responses during Repeated Air Pressure Stimulation of the Laryngeal Mucosa in Awake Humans

Repeated stimulation of the laryngeal mucosa occurs during speech. Single stimuli, however, can elicit the laryngeal adductor response (LAR). Our hypothesis was that the LAR to repeated rapid air pressure stimuli is centrally suppressed in humans. Hookedwire electrodes were inserted into the thyroarytenoid and cricothyroid muscles on both sides and into the posterior cricoarytenoid muscle on one side. Pairs of air puff stimuli were presented to the mucosa over the arytenoids at pressure levels three times threshold with interstimulus intervals from 250 to 5,000 ms. Bilateral thyroarytenoid responses occurred at around 150 ms to more than 70% of the initial stimuli. With repeated presentation at intervals of 2 seconds or less, the percent occurrence decreased to less than 40% and response amplitudes were reduced by 50%. Central suppression of adductor responses to repeated air puff stimuli may allow speakers to produce voice without eliciting reflexive spasms that could disrupt speech.

Coordinating Voicing Onset with Articulation: A Potential Role for Sensory Cues in Shaping Phonological Distinctions

In the typical speech of any language, voicing onset and offset are effortlessly coordinated with articulation as part of the intrinsic coordination of sound production. In this paper, we argue that voicing-articulatory coordination patterns could be shaped by sensory feedback during early speech learning and these patterns persist in mature syllable productions. Our experimental results show that voicing onset is closely associated with the peak velocity and peak amplitude of jaw and upper lip movements for VC syllables in adults. This robust coordination in the onset position may function to increase the salience of VC syllables and provide a phonetically natural explanation for vowels to undergo phonological lengthening and to avoid phonological reduction in word-initial onset position.

Influences of laryngeal afferent blockade on laryngeal muscle activity during speech

Problem: A previous study determined that sensory blockade reduced symptoms in spasmodic dysphonia. The purpose of this study was to determine how laryngeal afferent feedback blockade alters laryngeal muscle activity during speech, to explain this benefit in patients with spasmodic dysphonia. Methods: We used hooked wire electrodes to record from intrinsic laryngeal muscles (thyroarytenoid, cricothyroid, and posterior cricoarytenoid) during sentence production in subjects with either adductor and abductor spasmodic dysphonia before and after bilateral superior laryngeal nerve blockade with lidocaine. Prior to the block, sensory thresholds were determined for air puff stimuli presented to the mucosa overlying the arytenoid cartilages. Following the block, laryngeal muscle activity during production of the same sentences was recorded again and sensory testing confirmed blockade on both sides. Measures included the mean muscle activity during the first syllable of each sentence, syllable duration, and the pre-phonatory interval between muscle activity onset and voice onset for the first syllable of each sentence. Results: No changes occurred in mean muscle activity level following afferent blockade in all 3 muscles. Significant within-subject reductions were found in the duration of the first syllable of the sentence and in the pre-phonatory interval between thyroarytenoid muscle activity onset and vocalization onset for speech. The pre-phonatory interval decreased in 7 of the 8 subjects. No significant changes in pre-phonatory interval were found in the posterior cricoarytenoid or cricothyroid muscles. Conclusion: Symptom benefits following a reduction in afferent feedback are not a result of reduced muscle activity level but may reflect changes in central patterning of muscle activity in patients with spasmodic dysphonia. Significance: These results provide further understanding of the pathophysiology of symptom generation in spasmodic dysphonia. Support: The research was supported by the National Institute of Neurological Disorders and Stroke, 1 Z01 NS002980-05.