Skip to main content

Human Hyolaryngeal Movements Show Adaptive Motor Learning During Swallowing

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. 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.

    PubMed  CAS  Google Scholar 

  2. Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25(4):323–33.

    Article  PubMed  Google Scholar 

  3. Bastian AJ. Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol. 2008;21(6):628–33.

    Article  PubMed  Google Scholar 

  4. 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.

    Article  PubMed  Google Scholar 

  5. Gritsenko V, Kalaska JF. Rapid online correction is selectively suppressed during movement with a visuomotor transformation. J Neurophysiol. 2010;104(6):3084–104.

    Article  PubMed  CAS  Google Scholar 

  6. 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.

    Article  PubMed  CAS  Google Scholar 

  7. 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.

    Article  PubMed  Google Scholar 

  8. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  10. 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.

    Article  PubMed  Google Scholar 

  11. Morton SM, Bastian AJ. Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci. 2006;26(36):9107–16.

    Article  PubMed  CAS  Google Scholar 

  12. Krakauer JW. Motor learning and consolidation: the case of visuomotor rotation. Adv Exp Med Biol. 2009;629:405–21.

    Article  PubMed  Google Scholar 

  13. 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.

    Article  PubMed  Google Scholar 

  14. Fernandez-Ruiz J, Hall C, Vergara P, Díiaz R. Prism adaptation in normal aging: slower adaptation rate and larger aftereffect. Brain Res Cogn Brain Res. 2000;9(3):223–6.

    Article  PubMed  CAS  Google Scholar 

  15. Lackner JR, Dizio P. Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol. 1994;72(1):299–313.

    PubMed  CAS  Google Scholar 

  16. Lang CE, Bastian AJ. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol. 1999;82(5):2108–19.

    PubMed  CAS  Google Scholar 

  17. Lang CE, Bastian AJ. Additional somatosensory information does not improve cerebellar adaptation during catching. Clin Neurophysiol. 2001;112(5):895–907.

    Article  PubMed  CAS  Google Scholar 

  18. Morton SM, Bastian AJ. Prism adaptation during walking generalizes to reaching and requires the cerebellum. J Neurophysiol. 2004;92(4):2497–509.

    Article  PubMed  Google Scholar 

  19. 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.

    Article  PubMed  CAS  Google Scholar 

  20. Burnett TA, Mann EA, Stoklosa JB, Ludlow CL. Self-triggered functional electrical stimulation during swallowing. J Neurophysiol. 2005;94(6):4011–8.

    Article  PubMed  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. Donner MW, Bosma JF, Robertson DL. Anatomy and physiology of the pharynx. Gastrointest Radiol. 1985;10(3):196–212.

    PubMed  CAS  Google Scholar 

  23. Smith KK. The evolution of the mammalian pharynx. Zool J Linn Soc. 1992;104:313–49.

    Article  Google Scholar 

  24. Ludlow CL. Recent advances in laryngeal sensorimotor control for voice, speech and swallowing. Curr Opin Otolaryngol Head Neck Surg. 2004;12(3):160–5.

    Article  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Ianessa A. Humbert.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-012-9422-0

Keywords