Abstract
The hyoid bone and larynx elevate to protect the airway during swallowing. However, it is unknown whether hyolaryngeal movements during swallowing can adjust and adapt to predict the presence of a persistent perturbation in a feed-forward manner (adaptive motor learning). We investigated adaptive motor learning in nine healthy adults. Electrical stimulation was administered to the anterior neck to reduce hyolaryngeal elevation, requiring more strength to swallow during the perturbation period of this study. We assessed peak hyoid bone and laryngeal movements using videofluoroscopy across thirty-five 5-ml water swallows. Evidence of adaptive motor learning of hyolaryngeal movements was found when (1) participants showed systematic gradual increases in elevation against the force of electrical stimulation and (2) hyolaryngeal elevation overshot the baseline (preperturbation) range of motion, showing behavioral aftereffects, when the perturbation was unexpectedly removed. Hyolaryngeal kinematics demonstrates adaptive, error-reducing movements in the presence of changing and unexpected demands. This is significant because individuals with dysphagia often aspirate due to disordered hyolaryngeal movements. Thus, if rapid motor learning is accessible during swallowing in healthy adults, patients may be taught to predict the presence of perturbations and reduce errors in swallowing before they occur.
This is a preview of subscription content, access via your institution.



Similar content being viewed by others
References
Kendall KA, Leonard RJ, McKenzie SW. Accommodation to changes in bolus viscosity in normal deglutition: a videofluoroscopic study. Ann Otol Rhinol Laryngol. 2001;110(11):1059–65.
Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25(4):323–33.
Bastian AJ. Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol. 2008;21(6):628–33.
Aasland WA, Baum SR, McFarland DH. Electropalatographic, acoustic, and perceptual data on adaptation to a palatal perturbation. J Acoust Soc Am. 2006;119(4):2372–81.
Gritsenko V, Kalaska JF. Rapid online correction is selectively suppressed during movement with a visuomotor transformation. J Neurophysiol. 2010;104(6):3084–104.
Noguchi K, Fujii H, Yamabe Y, Tanaka M, Shimada A, Torisu T, Suenaga H. Anticipation and motor control on repetitive tooth tapping produced by open-close jaw movements. J Oral Rehabil. 2008;35(1):20–6.
Vasudevan EV, Bastian AJ. Split-belt treadmill adaptation shows different functional networks for fast and slow human walking. J Neurophysiol. 2010;103(1):183–91.
Jayaram G, Galea JM, Bastian AJ, Celnik P. Human locomotor adaptive learning is proportional to depression of cerebellar excitability. Cereb Cortex. 2011;21(8):1901–9.
Humbert IA, Poletto CJ, Saxon KG, Kearney PR, Crujido L, Wright-Harp W, Payne J, Jeffries N, Sonies BC, Ludlow CL. The effect of surface electrical stimulation on hyolaryngeal movement in normal individuals at rest and during swallowing. J Appl Physiol. 2006;101(6):1657–63.
Ludlow CL, Humbert I, Saxon K, Poletto C, Sonies B, Crujido L. Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal dysphagia. Dysphagia. 2007;22(1):1–10.
Morton SM, Bastian AJ. Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci. 2006;26(36):9107–16.
Krakauer JW. Motor learning and consolidation: the case of visuomotor rotation. Adv Exp Med Biol. 2009;629:405–21.
Galea JM, Vazquez A, Pasricha N, de Xivry JJ, Celnik P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb Cortex. 2011;21(8):1761–70.
Fernandez-Ruiz J, Hall C, Vergara P, DÃiaz R. Prism adaptation in normal aging: slower adaptation rate and larger aftereffect. Brain Res Cogn Brain Res. 2000;9(3):223–6.
Lackner JR, Dizio P. Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol. 1994;72(1):299–313.
Lang CE, Bastian AJ. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol. 1999;82(5):2108–19.
Lang CE, Bastian AJ. Additional somatosensory information does not improve cerebellar adaptation during catching. Clin Neurophysiol. 2001;112(5):895–907.
Morton SM, Bastian AJ. Prism adaptation during walking generalizes to reaching and requires the cerebellum. J Neurophysiol. 2004;92(4):2497–509.
Bunday KL, Reynolds RF, Kaski D, Rao M, Salman S, Bronstein AM. The effect of trial number on the emergence of the ‘broken escalator’ locomotor aftereffect. Exp Brain Res. 2006;174(2):270–8.
Burnett TA, Mann EA, Stoklosa JB, Ludlow CL. Self-triggered functional electrical stimulation during swallowing. J Neurophysiol. 2005;94(6):4011–8.
Searl J, Evitts P, Davis WJ. Perceptual and acoustic evidence of speaker adaptation to a thin pseudopalate. Logoped Phoniatr Vocol. 2006;31(3):107–16.
Donner MW, Bosma JF, Robertson DL. Anatomy and physiology of the pharynx. Gastrointest Radiol. 1985;10(3):196–212.
Smith KK. The evolution of the mammalian pharynx. Zool J Linn Soc. 1992;104:313–49.
Ludlow CL. Recent advances in laryngeal sensorimotor control for voice, speech and swallowing. Curr Opin Otolaryngol Head Neck Surg. 2004;12(3):160–5.
Acknowledgments
This study was funded by The National Institutes of Health (NIDCD 1K23DC010776-01 to IH, NIDCD DC009980 to RZG, and R01 HD053793 to PC) and The National Institute of Child, Health and Development (NICHD) (PC).
Conflict of interest
There are no financial or other conflicts of interest related to this study by any author.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Humbert, I.A., Christopherson, H., Lokhande, A. et al. Human Hyolaryngeal Movements Show Adaptive Motor Learning During Swallowing. Dysphagia 28, 139–145 (2013). https://doi.org/10.1007/s00455-012-9422-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00455-012-9422-0