Advertisement

Lung

pp 1–6 | Cite as

The Role of the Cerebellum in Control of Swallow: Evidence of Inspiratory Activity During Swallow

  • Mitchell D. Reed
  • Mason English
  • Connor English
  • Alyssa Huff
  • Ivan Poliacek
  • M. Nicholas Musselwhite
  • Dena R. Howland
  • Donald C. Bolser
  • Teresa PittsEmail author
RESPIRATORY PHYSIOLOGY
  • 30 Downloads

Abstract

Anatomical connections are reported between the cerebellum and brainstem nuclei involved in swallow such as the nucleus tractus solitarius, nucleus ambiguus, and Kölliker-fuse nuclei. Despite these connections, a functional role of the cerebellum during swallow has not been elucidated. Therefore, we examined the effects of cerebellectomy on swallow muscle recruitment and swallow–breathing coordination in anesthetized freely breathing cats. Electromyograms were recorded from upper airway, pharyngeal, laryngeal, diaphragm, and chest wall muscles before and after complete cerebellectomy. Removal of the cerebellum reduced the excitability of swallow (i.e., swallow number), and muscle recruitment of the geniohyoid, thyroarytenoid, parasternal (chestwall), and diaphragm muscles, but did not disrupt swallow–breathing coordination. Additionally, diaphragm and parasternal muscle activity during swallow is reduced after cerebellectomy, while no changes were observed during breathing. These findings suggest the cerebellum modulates muscle excitability during recruitment, but not pattern or coordination of swallow with breathing.

Notes

Acknowledgements

Research reported in this publication was supported by the National Institutes of Health HL111215 (TP), NS110169 (TP and DRH), HL103415 (DCB), HL1311716 (DCB), and ODO23854 (DCB). The Veterans Affairs Rehabilitation, Research and Development RCSB92495 (DRH), the Rebecca F. Hammond Endowment (DRH), the Kentucky Spinal Cord and Head Injury Research Trust, the Commonwealth of Kentucky Challenge for Excellence (TP and DRH), and the Craig F. Neilsen Foundation CNF546714 (TP and DRH).

Compliance with Ethical Standards

Conflict of interest

There are no conflicts of interest to declare.

References

  1. 1.
    Jean A (2001) Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 81(2):929–969CrossRefGoogle Scholar
  2. 2.
    Pitts T, Rose MJ, Mortensen AN, Poliacek I, Sapienza CM, Lindsey BG, Morris KF, Davenport PW, Bolser DC (2013) Coordination of cough and swallow: a meta-behavioral response to aspiration. Respir Physiol Neurobiol 189(3):543–551.  https://doi.org/10.1016/j.resp.2013.08.009 CrossRefGoogle Scholar
  3. 3.
    Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C (2009) Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp 30(10):3209–3226.  https://doi.org/10.1002/hbm.20743 CrossRefGoogle Scholar
  4. 4.
    Rangarathnam B, Kamarunas E, McCullough GH (2014) Role of cerebellum in deglutition and deglutition disorders. Cerebellum 13(6):767–776.  https://doi.org/10.1007/s12311-014-0584-1 CrossRefGoogle Scholar
  5. 5.
    Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H (2003) Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia 18(2):71–77.  https://doi.org/10.1007/s00455-002-0088-x CrossRefGoogle Scholar
  6. 6.
    Reis DJ, Doba N, Nathan MA (1973) Predatory attack, grooming, and consummatory behaviors evoked by electrical stimulation of cat cerebellar nuclei. Science 182(4114):845–847CrossRefGoogle Scholar
  7. 7.
    Berntson GG, Potolicchio SJ Jr, Miller NE (1973) Evidence for higher functions of the cerebellum: eating and grooming elicited by cerebellar stimulation in cats. Proc Natl Acad Sci USA 70(9):2497–2499CrossRefGoogle Scholar
  8. 8.
    Lutherer LO, Lutherer BC, Dormer KJ, Janssen HF, Barnes CD (1983) Bilateral lesions of the fastigial nucleus prevent the recovery of blood pressure following hypotension induced by hemorrhage or administration of endotoxin. Brain Res 269(2):251–257CrossRefGoogle Scholar
  9. 9.
    Xu F, Frazier DT (2000) Modulation of respiratory motor output by cerebellar deep nuclei in the rat. J Appl Physiol (1985) 89(3):996–1004.  https://doi.org/10.1152/jappl.2000.89.3.996 CrossRefGoogle Scholar
  10. 10.
    Xu F, Frazier DT, Zhang Z, Baekey DM, Shannon R (1997) Cerebellar modulation of cough motor pattern in cats. J Appl Physiol (1985) 83(2):391–397.  https://doi.org/10.1152/jappl.1997.83.2.391 CrossRefGoogle Scholar
  11. 11.
    Pitts T, Poliacek I, Rose MJ, Reed MD, Condrey JA, Tsai HW, Zhou G, Davenport PW, Bolser DC (2018) Neurons in the dorsomedial medulla contribute to swallow pattern generation: evidence of inspiratory activity during swallow. PLoS ONE 13(7):e0199903.  https://doi.org/10.1371/journal.pone.0199903 CrossRefGoogle Scholar
  12. 12.
    Xu F, Frazier DT (2002) Role of the cerebellar deep nuclei in respiratory modulation. Cerebellum 1(1):35–40.  https://doi.org/10.1080/147342202753203078 CrossRefGoogle Scholar
  13. 13.
    Bonis JM, Neumueller SE, Krause KL, Pan LG, Hodges MR, Forster HV (2013) Contributions of the Kolliker–Fuse nucleus to coordination of breathing and swallowing. Respir Physiol Neurobiol 189(1):10–21.  https://doi.org/10.1016/j.resp.2013.06.003 CrossRefGoogle Scholar
  14. 14.
    Basmajian J, Stecko G (1962) A new bipolar electrode for electromyography. J Appl Physiol 17(5):849–849CrossRefGoogle Scholar
  15. 15.
    Thexton AJ, Crompton AW, Owerkowicz T, German RZ (2009) Impact of rhythmic oral activity on the timing of muscle activation in the swallow of the decerebrate pig. J Neurophysiol 101(3):1386–1393.  https://doi.org/10.1152/jn.90847.2008 CrossRefGoogle Scholar
  16. 16.
    Hårdemark Cedborg AI, Sundman E, Bodén K, Hedström HW, Kuylenstierna R, Ekberg O, Eriksson LI (2009) Co-ordination of spontaneous swallowing with respiratory airflow and diaphragmatic and abdominal muscle activity in healthy adult humans. Exp Physiol 94(4):459–468.  https://doi.org/10.1113/expphysiol.2008.045724 CrossRefGoogle Scholar
  17. 17.
    McConnel FM, Hood D, Jackson K, O’Connor A (1994) Analysis of intrabolus forces in patients with Zenker’s diverticulum. Laryngoscope 104(5 Pt 1):571–581CrossRefGoogle Scholar
  18. 18.
    Pitts T, Gayagoy A, Rose M, Poliacek I, Condrey J, Musslewhite M, Shen T, Davenport P, Bolser D (2015) Suppression of abdominal motor activity during swallowing in cats and humans. PLoS ONE 10(5):e0128245–e0128245CrossRefGoogle Scholar
  19. 19.
    Rikard-Bell GC, Bystrzycka EK, Nail BS (1984) Brainstem projections to the phrenic nucleus: a HRP study in the cat. Brain Res Bull 12(5):469–477CrossRefGoogle Scholar
  20. 20.
    Vogel AP, Brown SE, Folker JE, Corben LA, Delatycki MB (2014) Dysphagia and swallowing-related quality of life in Friedreich ataxia. J Neurol 261(2):392–399.  https://doi.org/10.1007/s00415-013-7208-4 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Mitchell D. Reed
    • 1
  • Mason English
    • 1
  • Connor English
    • 1
  • Alyssa Huff
    • 1
    • 2
  • Ivan Poliacek
    • 3
    • 4
  • M. Nicholas Musselwhite
    • 3
  • Dena R. Howland
    • 1
    • 5
  • Donald C. Bolser
    • 3
  • Teresa Pitts
    • 1
    Email author
  1. 1.Department of Neurological Surgery and Kentucky Spinal Cord Injury Research Center, College of MedicineUniversity of LouisvilleLouisvilleUSA
  2. 2.Department of Physiology, College of MedicineUniversity of LouisvilleLouisvilleUSA
  3. 3.Department of Physiological Sciences, College of Veterinary MedicineUniversity of FloridaGainesvilleUSA
  4. 4.Institute of Medical Biophysics, Jessenius Faculty of Medicine in MartinComenius University in BratislavaMartinSlovakia
  5. 5.Research ServiceRobley Rex Veterans Affairs Medical CenterLouisvilleUSA

Personalised recommendations