Victor M Henriquez  & Christy L Ludlow
Laryngeal and Speech Section, National Institute of Neurological Disorders and Stroke, NIH, Bethesda, Maryland, USA

https://doi.org/10.36866/pn.72.28

To produce voice for speech and song, the muscles within the vocal folds (the thyroarytenoid muscles) must contract to bring the vocal folds together in the middle of the airway. When expiratory air flow from the lungs provides adequate air pressure to induce vibration, an acoustic excitation occurs in the tract to produce the human voice. The muscle adjustments must be rapid in order to precisely control voice onset and offset for distinguishing between voiced (e.g. /b/) and voiceless consonants (/p/) during ongoing speech. In addition, the tension within the folds and the subglottal pressure are modulated to produce changes in voice pitch and loudness for both speech and song.

The laryngeal muscles are also important for airway protection; they close the vocal folds to prevent the entry of food, liquid or particles past the folds into the lungs. The laryngeal adductor response (LAR) is a brain stem reflex that produces vocal fold closure and is triggered when the mucosa covering the vocal folds and/or the laryngeal vestibule are stimulated. The superior laryngeal nerve contains the afferents whose endings innervate the laryngeal mucosa. If stimulation is intense and prolonged, a life threatening uncontrolled closure of the airway (laryngospasm) can occur.

Cortical control is involved in both the fine motor control of the voice and volitional limb movements. During purposeful arm movements, sensory input that normally produces muscle reflexes is suppressed. This suppression prevents reflex responses from interrupting or perturbing cortically controlled precise rapid arm movements (Adamovich et al. 1997). In non-human primates, reflex suppression during volitional limb movements appears to be caused by descending cortical signals that inhibit incoming afferent signals to the spinal reflex circuits (Seki et al. 2003). Similar suppression of afferent inputs from the superior laryngeal nerve to the brainstem during speech or singing, however, might be detrimental to airway protection and allow entry of saliva or foreign substances into the lungs during these activities. We studied how these two laryngeal functions —fine motor control during voice and reflexive airway protection —inter-relate.

The LAR will produce vocal fold closure when elicited either by presenting an air puff to the mucosa overlying the vocal folds (Bhabu et al. 2003) or by stimulation of the internal branch of the superior laryngeal nerve (Ludlow et al. 1992). The superior laryngeal nerve in the neck can be stimulated using hooked wire electrodes inserted along the course of the nerve deep in the neck. This will produce a LAR with two components, a short latency ipsilateral R1 and a longer latency bilateral R2. These responses can be recorded during voice and breathing from thin wires inserted into the thyroarytenoid muscles (Fig. 1).

We compared the frequency of occurrence and the amplitude of the LAR in response to electrical stimulation of the internal branch of the superior laryngeal nerve during voice production and breathing tasks: a prolonged vowel, humming, breath holding at the larynx, or breathing in. When the LAR during these tasks was compared with quiet breathing no change occurred in the R1 response frequency or amplitude in any of the tasks. We also exam-ined how the LAR affected muscle activity during task performance. During vowel production, breath holding, and prolonged inspiration muscle tone is increased or decreased in the thyroarytenoid muscle as the vocal folds are held closed or open respectively. We examined whether the LAR summated with the increased muscle activity (Fig. 2B), was reduced or masked by the muscle activity (Fig. 2C) or momentarily interrupted (suppressed) muscle activity (Fig. 2D). Because there was no difference between the size of the LAR at rest and during volitional tasks, the LAR suppressed the muscle activity for the task momentarily when it occurred (Henriquez et al. 2007).

The longer latency response, R2, was reduced in frequency of occurrence by about 50% during both humming and effort closure and, to a lesser degree, during inspiration and vowel production. Likely cortical modula-tion was able to suppress this longer pathway. On the other hand, it did not modulate the more direct R1 pathway from the afferent termina-tions in the interstitial subnucleus of the nucleus tractus solitarius, via the lateral tegmental field to the laryn-geal motor neurons in the nucleus ambiguus (Ambalavanar et al. 2004).

Previously, our group has found that volitional swallowing can transiently suppress the LAR in normal subjects (Barkmeier et al. 2000). Swallowing, however, must also incorporate parts of the protective airway reflex system as vocal fold closure occurs in the middle of the pharyngeal phase to prevent aspiration of food or liquids into the lungs. The LAR, therefore, is commensurate with airway protection during swallowing and may be suppressed by the brainstem central pattern generator when engaged during volitional swallowing.

The tenacity of airway protection over volitional laryngeal control for voice and respiration is illustrative of its importance. From a functional perspective, volitional laryngeal tasks for voice sustain the critical human activity of communication, but these are not essential for survival. The importance of preserving airway protection at the level of the brain stem overrides muscle activity for voice, breath holding and inspiration. Control of the laryngeal muscles during volitional tasks is therefore an exception to the general pattern of reflex suppression during volitional movement.

Acknowledgements

This research was supported by the Division of Intramural Research of the National Institute of Neurological Disorders and Stroke, National Institutes of Health.

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