Skip to main content
SpringerLink
Log in

Advances in Swallowing Neurophysiology Across Pediatric Development: Current Evidence and Insights

  • Swallowing Disorders (M Gonzalez-Fernandez, Section Editor)
  • Published:
Current Physical Medicine and Rehabilitation Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

This review article analyzes current evidence on the neurophysiology of swallowing during development and offers expert opinion on clinical implications and future research directions.

Recent Findings

In the past 5 years, basic and clinical research has offered advances in our understanding of pediatric swallowing neurophysiology. Animal models have elucidated the role of brainstem circuits and the peripheral and central nervous systems in neonatal swallowing. Recent human studies have further showcased that fetal and infant swallowing require cerebral inputs in order to develop functionally. Finally, neurophysiological and neuroimaging studies are starting to better define these cerebral inputs, as well as neuroplastic adaptations that may be needed for optimal feeding development.

Summary

The neural development of swallowing is a complex and dynamic process. Continued research is needed to better understand influences on swallowing neural development, which can be essential for improving prevention, diagnosis, and interventions for pediatric dysphagia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Amri M, Car A, Jean A. Medullary control of the pontine swallowing neurones in sheep. Exp Brain Res. 1984;55(1):105–10.

  2. Car A, Roman C. Deglutitions and oesophageal reflex contractions induced by electrical stimulation of the medulla oblongata. Exp Brain Res. 1969;11(1):75–92.

    Google Scholar 

  3. Doty RW. Influence of stimulus pattern on reflex deglutition. Am J Physiol. 1951;166(1):142–58.

    Article  CAS  PubMed  Google Scholar 

  4. Jean A, Car A, Roman C. Comparison of activity in pontine versus medullary neurones during swallowing. Exp Brain Res. 1975;22(2):211–20.

  5. Martin RE, Kemppainen P, Masuda Y, Yao D, Murray GM, Sessle BJ. Features of cortically evoked swallowing in the awake primate (Macaca fascicularis). J Neurophysiol. 1999;82(3):1529–41.

    Article  CAS  PubMed  Google Scholar 

  6. Sumi T. Reticular ascending activation of frontal cortical neurons in rabbits, with special reference to the regulation of deglutition. Brain Res. 1972;13(46):43–54.

    Article  Google Scholar 

  7. Daniels SK, Foundas AL. Lesion localization in acute stroke patients with risk of aspiration. J Neuroimaging. 1999;9(2):91–8.

    Article  CAS  PubMed  Google Scholar 

  8. Daniels SK, Pathak S, Mukhi SV, Stach CB, Morgan RO, Anderson JA. The relationship between lesion localization and dysphagia in acute stroke. Dysphagia. 2017;32(6):777–84.

    Article  PubMed  Google Scholar 

  9. Gordon C, Hewer RL, Wade DT. Dysphagia in acute stroke. Br Med J (Clin Res Ed). 1987;295(6595):411–4.

    Article  CAS  Google Scholar 

  10. Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993;8(3):195–202.

    Article  CAS  PubMed  Google Scholar 

  11. Meadows JC. Dysphagia in unilateral cerebral lesions. J Neurol Neurosurg Psychiatry. 1973;36(5):853–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Robbins J, Levine RL, Maser A, Rosenbek JC, Kempster GB. Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil. 1993;74(12):1295–300.

    Article  CAS  PubMed  Google Scholar 

  13. Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H2 15O PET activation. J Neurophysiol. 1999;81(4):1917–26.

    Article  CAS  PubMed  Google Scholar 

  14. Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C. Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp. 2009;30(10):3209–26.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Malandraki GA, Johnson S, Robbins J. Functional MRI of swallowing: from neurophysiology to neuroplasticity. Head Neck. 2011;33(S1):S14-20.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85(2):938–50.

    Article  CAS  PubMed  Google Scholar 

  17. Martin RE, MacIntosh BJ, Smith RC, Barr AM, Stevens TK, Gati JS, et al. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004;92(4):2428–43.

    Article  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  Google Scholar 

  19. Toogood JA, Barr AM, Stevens TK, Gati JS, Menon RS, Martin RE. Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study. Exp Brain Res. 2005;161(1):81–90.

    Article  PubMed  Google Scholar 

  20. Carnaby GD, LaGorio L, Silliman S, Crary M. Exercise-based swallowing intervention (McNeill Dysphagia Therapy) with adjunctive NMES to treat dysphagia post-stroke: a double-blind placebo-controlled trial. J Oral Rehabil. 2020;47(4):501–10.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Huckabee M-L, Lamvik-Gozdzikowska K. Reconsidering rehabilitation for neurogenic dysphagia: strengthening skill in swallowing. Curr Phys Med Rehabil Rep. 2018;6(3):186–91.

    Article  Google Scholar 

  22. Malandraki GA, Rajappa A, Kantarcigil C, Wagner E, Ivey C, Youse K. The intensive dysphagia rehabilitation approach applied to patients with neurogenic dysphagia: a case series design study. Arch Phys Med Rehabil. 2016;97(4):567–74.

    Article  PubMed  Google Scholar 

  23. Zimmerman E, Carnaby G, Lazarus Cathy L, Malandraki Georgia A. Motor learning, neuroplasticity, and strength and skill training: moving Ffom compensation to retraining in behavioral management of dysphagia. Am J Speech Lang Pathol. 2020;29(2S):1065–77.

    Article  PubMed  Google Scholar 

  24. Bhattacharyya N. The prevalence of pediatric voice and swallowing problems in the United States. Laryngoscope. 2015;125(3):746–50.

    Article  PubMed  Google Scholar 

  25. Borowitz KC, Borowitz SM. Feeding problems in infants and children. Pediatr Clin North Am. 2018;65(1):59–72.

    Article  PubMed  Google Scholar 

  26. Kovacic K, Rein LE, Szabo A, Kommareddy S, Bhagavatula P, Goday PS. Pediatric feeding disorder: a nationwide prevalence study. J Pediatr. 2021;1(228):126-131.e3.

    Article  Google Scholar 

  27. Linscheid TR. Behavioral treatments for pediatric feeding disorders. Behav Modif. 2006;30(1):6–23.

    Article  PubMed  Google Scholar 

  28. Lefton-Greif MA, Arvedson JC. Pediatric feeding and swallowing disorders: state of health, population trends, and application of the international classification of functioning, Disability, and Health. Semin Speech Lang. 2007;28(3):161–5.

    Article  PubMed  Google Scholar 

  29. Lefton-Greif MA, Arvedson JC. Pediatric feeding/swallowing: yesterday, today, and tomorrow. Semin Speech Lang. 2016;37(4):298–309.

    Article  PubMed  Google Scholar 

  30. Delaney AL, Arvedson JC. Development of swallowing and feeding: prenatal through first year of life. Dev Disabil Res Rev. 2008;14(2):105–17.

    Article  PubMed  Google Scholar 

  31. Miller JL, Sonies BC, Macedonia C. Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation. Early Human Dev. 2003;71(1):61–87.

    Article  Google Scholar 

  32. •• Maynard TM, Zohn IE, Moody SA, LaMantia A-S. Suckling, feeding, and swallowing: behaviors, circuits, and targets for neurodevelopmental pathology. Annu Rev Neurosci. 2020 8;43(1):315–36. This clinical review paper laid out a developmental program of feeding development and described an animal model of developmental pediatric dysphagia.

  33. Ross MG, Nijland MJM. Fetal swallowing: relation to amniotic fluid regulation. Clin Obstet Gynecol. 1997;40(2):352–65.

    Article  CAS  PubMed  Google Scholar 

  34. de Vries JI, Visser GH, Prechtl HF. The emergence of fetal behaviour. II Quantitative aspects Early Hum Dev. 1985;12(2):99–120.

    Article  PubMed  Google Scholar 

  35. Carruth BR, Ziegler PJ, Gordon A, Hendricks K. Developmental milestones and self-feeding behaviors in infants and toddlers. J Am Diet Assoc. 2004;1(104):51–6.

    Article  Google Scholar 

  36. Hennessey NW, Fisher G, Ciccone N. Developmental changes in pharyngeal swallowing acoustics: a comparison of adults and children. Logoped Phoniatr Vocol. 2018;43(2):63–72.

    Article  PubMed  Google Scholar 

  37. Hahn Arkenberg R, Mitchell S, Brown B, Goffman L, Malandraki GA. The neuromuscular development of swallowing continues into the school-age years: evidence from a preliminary cross-sectional study. Dysphagia Research Society Meeting. In Virtual; 2021.

  38. Thelen E. Dynamic systems theory and the complexity of change. Psychoanalytic Dialogues. 2005;15(2):255–83.

    Article  Google Scholar 

  39. Haddad JM, Claxton LJ, Keen R, Berthier NE, Riccio GE, Hamill J, et al. Development of the coordination between posture and manual control. J Exp Child Psychol. 2012;111(2):286–98.

    Article  Google Scholar 

  40. Jean A. Brainstem organization of the swallowing network. BBE. 1984;25(2–3):109–16.

    CAS  Google Scholar 

  41. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81(2):929–69.

    Article  CAS  PubMed  Google Scholar 

  42. Miller AJ. The search for the central swallowing pathway: the quest for clarity. Dysphagia. 1993;8(3):185–94.

    Article  CAS  PubMed  Google Scholar 

  43. Miller AJ. The neurobiology of swallowing and dysphagia. Dev Disabil Res Rev. 2008;14(2):77–86.

    Article  PubMed  Google Scholar 

  44. Pitts T, Huff A, Reed M, Iceman K, Mellen N. Evidence of intermediate reticular formation involvement in swallow pattern generation, recorded optically in the neonate rat sagittally sectioned hindbrain. J Neurophysiol. 2021;125(4):993–1005.

  45. Gould FD, Lammers AR, Mayerl CJ, German RZ. Specific vagus nerve lesion have distinctive physiologic mechanisms of dysphagia. Front Neurol. 2019;10:1301.

  46. Gould FDH, Lammers AR, Mayerl C, Ohlemacher J, German RZ. Muscle activity and kinematics show different responses to recurrent laryngeal nerve lesion in mammal swallowing. J Neurophysiol. 2020;124(6):1743–53.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Gould FDH, Yglesias B, Ohlemacher J, German RZ. Pre-pharyngeal swallow effects of recurrent laryngeal nerve lesion on bolus shape and airway protection in an infant pig Model. Dysphagia. 2017;32(3):362–73.

    Article  PubMed  Google Scholar 

  48. Ding P, Campbell-Malone R, Holman SD, Lukasik SL, Fukuhara T, Gierbolini-Norat EM, et al. Unilateral superior laryngeal nerve lesion in an animal model of dysphagia and its effect on sucking and swallowing. Dysphagia. 2013;28(3):404–12.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Stricklen BM, Bond LE, Gould FDH, German RZ, Mayerl CJ. Swallow safety in infant pigs with and without recurrent laryngeal nerve lesion. Dysphagia. 2020;35(6):978–84.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Mayerl CJ, Catchpole EA, Edmonds CE, Gould FDH, McGrattan KE, Bond LE, et al. The effect of preterm birth, recurrent laryngeal nerve lesion, and postnatal maturation on hyoid and thyroid movements, and their coordination in infant feeding. J Biomech. 2020;22(105):109786.

    Article  Google Scholar 

  51. • Mayerl CJ, Myrla AM, Gould FDH, Bond LE, Stricklen BM, German RZ. Swallow safety is determined by bolus volume during infant feeding in an animal model. Dysphagia. 2021;36(1):120–9. A study of swallow safety in preterm and full-term infant pigs, with and without RLN lesions. They found that bolus size (swallowing larger boluses) was more predictive of swallow safety than either lesion status or preterm/term status.

  52. Wong NS, Feng Z, Rappazzo C, Turk C, Randall C, Ongkasuwan J. Patterns of dysphagia and airway protection in infants with 22q11.2-Deletion syndrome. The Laryngoscope. 2020;130(11):2532–6.

    Article  CAS  PubMed  Google Scholar 

  53. LaMantia A-S, Moody SA, Maynard TM, Karpinski BA, Zohn IE, Mendelowitz D, et al. Hard to swallow: developmental biological insights into pediatric dysphagia. Dev Biol. 2016;409(2):329–42.

    Article  CAS  PubMed  Google Scholar 

  54. Welby L, Caudill H, Yitsege G, Hamad A, Bunyak F, Zohn IE, Maynard T, LaMantia AS, Mendelowitz D, Lever TE. Persistent feeding and swallowing deficits in a mouse model of 22q11. 2 deletion syndrome. Front Neurol. 2020;11:4.

  55. Maynard TM, Horvath A, P Bernot J, Karpinski BA, Tavares ALP, Shah A, et al. Transcriptional dysregulation in developing trigeminal sensory neurons in the LgDel mouse model of DiGeorge 22q11.2 deletion syndrome. Hum Mol Genet. 2020;29(6):1002–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Vijayakumar K, Rockett J, Ryan M, Harris R, Pitt M, Devile C. Experience of using electromyography of the genioglossus in the investigation of paediatric dysphagia. Dev Med Child Neurol. 2012;54(12):1127–32.

    Article  PubMed  Google Scholar 

  57. Lefton-Greif MA, Carroll JL, Loughlin GM. Long-term follow-up of oropharyngeal dysphagia in children without apparent risk factors. Pediatr Pulmonol. 2006;41(11):1040–8.

    Article  PubMed  Google Scholar 

  58. Kooi-van Es M, Erasmus CE, de Swart BJM, Voet NBM, van der Wees PJ, de Groot IJM, et al. Dysphagia and dysarthria in children with neuromuscular diseases, a prevalence study. J Neuromuscul Dis. 2020;7(3):287–95.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Sherman V, Greco E, Moharir M, Beal D, Thorpe K, Martino R. Feeding and swallowing impairment in children with stroke and unilateral cerebral palsy: a systematic review. Dev Med Child Neurol. 2019;61(7):761–9.

    Article  PubMed  Google Scholar 

  60. Sherman V, Martino R, Bhathal I, DeVeber MG, Dlamini N, MacGregor D, et al. Swallowing, oral motor, motor speech, and language impairments following acute pediatric ischemic stroke. Stroke. 2021;52(4):1309–18.

  61. Shewmon DA. Anencephaly: selected medical aspects. Hastings Cent Rep. 1988;18(5):11–9.

    Article  CAS  PubMed  Google Scholar 

  62. Peleg D, Goldman JA. Fetal deglutition: a study of the anencephalic fetus. Eur J Obstet Gynecol Reprod Biol. 1978;8(3):133–6.

    Article  CAS  PubMed  Google Scholar 

  63. • Radford K, Taylor RC, Hall JG, Gick B. Aerodigestive and communicative behaviors in anencephalic and hydranencephalic infants. Birth Defects Res. 2019;111(2):41–52. Review of published data on aerodigestive and communicative behaviors of fetuses/infants with anencephaly or hydranencephaly included in older studies.

  64. Sanchez K, Morgan AT, Slattery JM, Olsen JE, Lee KJ, Anderson PJ, et al. Neuropredictors of oromotor feeding impairment in 12month-old children. Early Human Dev. 2017;1(111):49–55.

    Article  Google Scholar 

  65. Kashou NH, Dar IA, El-Mahdy MA, Pluto C, Smith M, Gulati IK, Lo W, Jadcherla SR. Brain lesions among orally fed and gastrostomy-fed dysphagic preterm infants: can routine qualitative or volumetric quantitative magnetic resonance imaging predict feeding outcomes? Front Pediatr. 2017;5:73.

  66. •• Tamilia E, Parker MS, Rocchi M, Taffoni F, Hansen A, Grant PE, et al. Nutritive sucking abnormalities and brain microstructural abnormalities in infants with established brain injury: a pilot study. J Perinatol. 2019;39(11):1498–508. A pilot neuroimaging study of 10 infants with brain injury, which found a correlation between microstructural white matter damage and sucking deficits.

  67. Mishra A, Sheppard JJ, Kantarcigil C, Gordon AM, Malandraki GA. Novel mealtime duration measures: reliability and preliminary associations with clinical feeding and swallowing performance in self-feeding children with cerebral palsy. Am J Speech Lang Pathol. 2018;27(1):99–107.

    Article  PubMed  Google Scholar 

  68. Mishra A, Malandraki GA, Sheppard JJ, Gordon AM, Levy ES, Troche MS. Voluntary cough and clinical swallow function in children with spastic cerebral palsy and healthy controls. Dysphagia. 2019;34(2):145–54.

    Article  PubMed  Google Scholar 

  69. Kantarcigil C, Sheppard JJ, Gordon AM, Friel KM, Malandraki GA. A telehealth approach to conducting clinical swallowing evaluations in children with cerebral palsy. Res Dev Disabil. 2016;1(55):207–17.

    Article  Google Scholar 

  70. •• Mourão LF, Friel KM, Sheppard JJ, Kuo H-C, Luchesi KF, Gordon AM, et al. The role of the corpus callosum in pediatric dysphagia: preliminary findings from a diffusion tensor imaging study in children with unilateral spastic cerebral palsy. Dysphagia. 2017;32(5):703–13. A study examining the association between brain lesion characteristics and corpus callosum connectivity and clinical swallowing outcomes in 20 self-feeding children with UCP. Findings showed that type and/or side of lesion plays a role in severity of clinical dysphagia in UCP and that corpus callosum integrity correlates with feeding/swallowing performance when sensorimotor areas of the left hemisphere are affected.

  71. Malandraki GA, Mourão LF, Lu K-H, Friel KM, Luchesi KF, Sheppard JJ, et al. Functional and structural connectivity in children with unilateral cerebral palsy and clinical dysphagia: a multimodal neuroimaging study. European Society of Swallowing Disorders Congress.In Barcelona, Spain; 2017.

  72. Malandraki GA, Mitchell S, Brown B, Hahn Arkenberg R, Lundine J, Burdo-Hartman W, et al. Feeding skills and eating efficiency are reduced in self-feeding school-age children with unilateral CP: an unrecognized reality. Dysphagia Research Society Meeting. In 2021.

  73. Malandraki GA, Mitchell S, Hahn Arkenberg R, Brown B, Lundine J, Burdo-Hartman W, et al. The neuromuscular control of swallowing and speech in unilateral CP: overactivation and lack of specificity are overlapping traits. Dysphagia Research Society Meeting. In Virtual; 2021.

  74. Crary MA, Carnaby GD, LaGorio LA, Carvajal PJ. Functional and physiological outcomes from an exercise-based dysphagia therapy: a pilot investigation of the McNeill Dysphagia Therapy Program. Arch Phys Med Rehabil. 2012;93(7):1173–8.

    Article  PubMed  Google Scholar 

Download references

Funding

This work was partially supported by the National Institute on Deafness and Other Communication Disorders Early Investigator R21 Grant (Grant 1R21DC015867-01A1, PI: Malandraki) and by an American Academy of Cerebral Palsy and Developmental Medicine Pedal-with-Pete research grant (PI: Malandraki).

Author information

Authors and Affiliations

  1. Speech, Language, & Hearing Sciences, Purdue University, 715 Clinic Drive, West Lafayette, IN, 47907, USA

    Georgia A. Malandraki & Rachel Hahn Arkenberg

  2. Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA

    Georgia A. Malandraki

Authors
  1. Georgia A. Malandraki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rachel Hahn Arkenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Georgia A. Malandraki.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Human and Animal Rights

All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Swallowing Disorders

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Malandraki, G.A., Arkenberg, R.H. Advances in Swallowing Neurophysiology Across Pediatric Development: Current Evidence and Insights. Curr Phys Med Rehabil Rep 9, 267–276 (2021). https://doi.org/10.1007/s40141-021-00334-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40141-021-00334-3

Keywords

Search

Navigation