New directions for understanding neural control in swallowing: The potential and promise of motor learning

Dysphagia

Volumn 28, Issue 1, 2013, Pages 1-10

  Humbert, Ianessa A ^a   German, Rebecca Z ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adaptation; Deglutition; Deglutition disorders; Motor control; Motor learning; Muscle memory; Neuroscience

Indexed keywords

ADAPTATION; BRAIN FUNCTION; DIGESTIVE FUNCTION; ELECTROENCEPHALOGRAM; HUMAN; LEARNING; LIMB MOVEMENT; MOTOR CONTROL; NERVOUS SYSTEM PARAMETERS; NEUROFEEDBACK; OROPHARYNX; POSITIVE FEEDBACK; PREDICTION; PRIORITY JOURNAL; REVIEW; SENSORY FEEDBACK; SWALLOWING;

ADAPTATION, PHYSIOLOGICAL; CENTRAL NERVOUS SYSTEM; DEGLUTITION; DEGLUTITION DISORDERS; FEEDBACK, SENSORY; HUMANS; LEARNING; MODELS, BIOLOGICAL; MOTOR SKILLS; VOLITION;

EID: 84874191948     PISSN: 0179051X     EISSN: 14320460     Source Type: Journal    
DOI: 10.1007/s00455-012-9432-y     Document Type: Review

References (78)

1. Marshall-Hall E. On the reflex function of the medulla oblongata and medulla spinalis. Philos Trans. 1833;26:635-65.
2. Miller RF, Sherrington CS. Some observations on the bucco-pharyngeal stage of reflex deglutition in the cat. Q J Exp Physiol. 1916;9:147-86.
3. Negus VE. The mechanism of swallowing. Proc R Soc Med. 1942;36:85-92.
4. Wise S, Shadmehr R. Motor control. In: Ramachandran VS, editor. Encyclopedia of the Human Brain. San Diego: Academic Press; 2002. p. 137-57.
5. Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89-108.
6. Steele CM, Miller AJ. Sensory input pathways and mechanisms in swallowing: a review. Dysphagia. 2010;25(4):323-33.
7. Humbert IA, Lokhande A, Christopherson H, German R, Stone A. Adaptation of swallowing hyo-laryngeal kinematics is distinct in oral versus pharyngeal sensory processing. J Appl Physiol. 2012;112(10):1698-705.
8. Kandel R, Schwartz J, Jessell T. Principles of neuroscience. 4th ed. New York: McGraw-Hill; 2002.
9. Turvey MT, Fonseca S. Nature of motor control: perspectives and issues. Adv Exp Med Biol. 2009;629:93-123.
10. Turvey M, Shaw R, Mace W. Issues in the theory of action: degrees of freedom, coordinative structures and coalitions. Hillsdale: Lawrence Erlbaum Associates; 1978.
11. Han DS, et al. Comparison of disordered swallowing patterns in patients with recurrent cortical/subcortical stroke and first-time brainstem stroke. J Rehabil Med. 2005;37(3):189-91.
12. Michou E, Hamdy S. Cortical input in control of swallowing. Curr Opin Otolaryngol Head Neck Surg. 2009;17(3):166-71.
13. Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140(3):280-9.
14. Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003;18(2):71-7.
15. Martin BJ, Logemann JA, Shaker R, Dodds WJ. Normal laryngeal valving patterns during three breath-hold maneuvers: a pilot investigation. Dysphagia. 1993;8(1):11-20.
16. Boden K, Hallgren A, Witt Hedstrom H. Effects of three different swallow maneuvers analyzed by videomanometry. Acta Radiol. 2006;47(7):628-33.
17. Kern MK, Jaradeh S, Arndorfer RC, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001;280(3):G354-60.
18. Babaei A, Kern M, Antonik S, Mepani R, Ward BD, Li SJ, Hyde J, Shaker R. Enhancing effects of flavored nutritive stimuli on cortical swallowing network activity. Am J Physiol Gastrointest Liver Physiol. 2010;299(2):G422-9.
19. Humbert IA, Joel S. Tactile, gustatory, and visual biofeed-back stimuli modulate neural substrates of deglutition. Neuroimage. 2012;59(2):1485-90.
20. Prochazka A, Clarac F, Loeb GE, Rothwell JC, Wolpaw JR. What do reflex and voluntary mean? Modern views on an ancient debate. Exp Brain Res. 2000;130(4):417-32.
21. Ertekin C. Voluntary versus spontaneous swallowing in man. Dysphagia. 2011;26(2):183-92.
22. Jean A. Brainstem organization of the swallowing network. Brain Behav Evol. 1984;25(2-3):109-16.
23. Gibbs CH, Suit SR. Movements of the jaw after unexpected contact with a hard object. J Dent Res. 1973;52(4):810-4.
24. Miller AJ. The Neuroscientific principles of swallowing and dysphagia (dysphagia series). San Diego: Singular Publishing Group; 1999. p. 284.
25. Miller AJ. The neurobiology of swallowing and dysphagia. Dev Disabil Res Rev. 2008;14(2):77-86.
26. Martin RE. Neuroplasticity and swallowing. Dysphagia. 2009;24(2):218-29.
27. Humbert IA, Robbins J. Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia. 2007;22(3):266-75.
28. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;114(12):2226-44.
29. Lang IM. Brain stem control of the phases of swallowing. Dysphagia. 2009;24(3):333-48.
30. Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol. 2007;102(2):587-600.
31. German RZ, Crompton AW, Thexton AJ. Integration of the reflex pharyngeal swallow into rhythmic oral activity in a neurologically intact pig model. J Neurophysiol. 2009;102(2):1017-25.
32. Bastian AJ. Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol. 2008;21(6):628-33.
33. Krakauer JW, Mazzoni P. Human sensorimotor learning: adaptation, skill, and beyond. Curr Opin Neurobiol. 2011;21(4):636-44.
34. Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci. 2011;12(12):739-51.
35. Shadmehr R, Krakauer JW. A computational neuroanatomy for motor control. Exp Brain Res. 2008;185(3):359-81.
36. 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.
37. Gritsenko V, Kalaska JF. Rapid online correction is selectively suppressed during movement with a visuomotor transformation. J Neurophysiol. 2010;104(6):3084-104.
38. 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.
39. 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.
40. 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.
41. 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.
42. Latash M. Neurophysiological basis of movement. 2nd ed. Champaign: Human Kinetics; 2008.
43. Krakauer JW, Shadmehr R. Towards a computational neuropsychology of action. Prog Brain Res. 2007;165:383-94.
44. Shadmehr R, Mussa-Ivaldi FA. Adaptive representation of dynamics during learning of a motor task. J Neurosci. 1994;14(5 Pt 2):3208-24.
45. Franklin DW, Wolpert DM. Computational mechanisms of sensorimotor control. Neuron. 2011;72(3):425-42.
46. Shmuelof L, Krakauer JW. Are we ready for a natural history of motor learning? Neuron. 2011;72(3):469-76.
47. Donner MW, Bosma JF, Robertson DL. Anatomy and physiology of the pharynx. Gastrointest Radiol. 1985;10(3):196-212.
48. Smith KK. The evolution of the mammalian pharynx. Zool J Linn Soc. 1992;104:313-49.
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.
50. Komuro A, Masuda Y, Iwata K, Kobayashi M, Kato T, Hidaka O, Morimoto T. Influence of food thickness and hardness on possible feed-forward control of the masseteric muscle activity in the anesthetized rabbit. Neurosci Res. 2001;39(1):21-9.
51. Komuro A, Morimoto T, Iwata K, Inoue T, Masuda Y, Kato T, Hidaka O. Putative feed-forward control of jaw-closing muscle activity during rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol. 2001;86(6):2834-44.
52. Ross CF, Baden AL, Georgi J, Herrel A, Metzger KA, Reed DA, Schaerlaeken V, Wolff MS. Chewing variation in lepidosaurs and primates. J Exp Biol. 2010;213(4):572-84.
53. Ross CF, Dharia R, Herring SW, Hylander WL, Liu ZJ, Rafferty KL, Ravosa MJ, Williams SH. Modulation of mandibular loading and bite force in mammals during mastication. J Exp Biol. 2007;210:1046-63.
54. Hidaka O, Morimoto T, Kato T, Masuda Y, Inoue T, Takada K. Behavior of jaw muscle spindle afferents during cortically induced rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol. 1999;82(5):2633-40.
55. Ottenhoff FA, van der Bilt A, van der Glas HW, Bosman F. Control of human jaw elevator muscle activity during simulated chewing with varying bolus size. Exp Brain Res. 1993;96(3):501-12.
56. van der Bilt A, Ottenhoff FA, van der Glas HW, Bosman F, Abbink JH. Modulation of the mandibular stretch reflex sensitivity during various phases of rhythmic open-close movements in humans. J Dent Res. 1997;76(4):839-47.
57. Lund JP. Chew before you swallow (chap 15). Prog Brain Res. 2011;188:219-28.
58. Hidaka O, Iwasaki M, Saito M, Morimoto T. Influence of clenching intensity on bite force balance, occlusal contact area, and average bite pressure. J Dent Res. 1999;78(7):1336-44.
59. Hidaka O, Morimoto T, Masuda Y, Kato T, Matsuo R, Inoue T, Kobayashi M, Takada K. Regulation of masticatory force during cortically induced rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol. 1997;77(6):3168-79.
60. Nasir SM, Ostry DJ. Auditory plasticity and speech motor learning. Proc Natl Acad Sci USA. 2009;106(48):20470-5.
61. Houde JF, Jordan MI. Sensorimotor adaptation in speech production. Science. 1998;279(5354):1213-6.
62. Houde JF, Jordan MI. Sensorimotor adaptation of speech I: Compensation and adaptation. J Speech Lang Hear Res. 2002;45(2):295-310.
63. Shiller DM, Sato M, Gracco VL, Baum SR. Perceptual recalibration of speech sounds following speech motor learning. J Acoust Soc Am. 2009;125(2):1103-13.
64. Nasir SM, Ostry DJ. Speech motor learning in profoundly deaf adults. Nat Neurosci. 2008;11(10):1217-22.
65. Avivi-Arber L, Lee JC, Sessle BJ. Face sensorimotor cortex neuroplasticity associated with intraoral alterations (chap 9). Prog Brain Res. 2011;188:135-50.
66. Adachi K, Lee JC, Hu JW, Yao D, Sessle BJ. Motor cortex neuroplasticity associated with lingual nerve injury in rats. Somatosens Mot Res. 2007;24(3):97-109.
67. Avivi-Arber L, Lee JC, Sessle BJ. Cortical orofacial motor representation: effect of diet consistency. J Dent Res. 2010;89(10):1142-7.
68. Sessle BJ, Hannam AG. Mastication and swallowing: biological and chemical correlates. Toronto: University of Toronto Press; 1976. 194 pp.
69. German RZ, Crompton AW, Owerkowicz T, Thexton AJ. Volume and rate of milk delivery as determinants of swallowing in an infant model (Sus scrofia). Dysphagia. 2004;19:147-54.
70. Chee C, Arshad S, Singh S, Mistry S, Hamdy S. The influence of chemical gustatory stimuli and oral anaesthesia on healthy human pharyngeal swallowing. Chem Senses. 2005;30(5):393-400.
71. Ding R, Logemann JA, Larson CR, Rademaker AW. The effects of taste and consistency on swallow physiology in younger and older healthy individuals: a surface electromyographic study. J Speech Lang Hear Res. 2003;46(4):977-89.
72. Leow LP, Huckabee ML, Sharma S, Tooley TP. The influence of taste on swallowing apnea, oral preparation time, and duration and amplitude of submental muscle contraction. Chem Senses. 2007;32(2):119-28.
73. Palmer PM, McCulloch TM, Jaffe D, Neel AT. Effects of a sour bolus on the intramuscular electromyographic (EMG) activity of muscles in the submental region. Dysphagia. 2005;20(3):210-7.
74. Pelletier CA, Dhanaraj GE. The effect of taste and palatability on lingual swallowing pressure. Dysphagia. 2006;21(2):121-8.
75. German RZ, Campbell-Malone R, Crompton AW, Ding P, Holman S, Konow N, Thexton AJ. The concept of hyoid posture. Dysphagia. 2011;26(2):97-8.
76. Luo P, Zhang J, Yang R, Pendlebury W. Neuronal circuitry and synaptic organization of trigeminal proprioceptive afferents mediating tongue movement and jaw-tongue coordination via hypoglossal premotor neurons. Eur J Neurosci. 2006;23(12):3269-83.
77. Krakauer JW, Carmichael ST, Corbett D, Wittenberg GF. Getting neurorehabilitation right: what can be learned from animal models? Neurorehabil Neural Repair. 2012;26(8):923-31.
78. Krakauer JW. Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr Opin Neurol. 2006;19(1):84-90.