The Generation of Post-Inspiratory Activity in Laryngeal Motoneurons: A Review

  • Tara G. Bautista
  • Peter G.R. Burke
  • Qi-Jian Sun
  • Robert G. Berkowitz
  • Paul M. Pilowsky
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 669)

Abstract

Breathing is a vegetative function that is altered during more complex behaviours such as exercise, vocalisation and respiratory protective reflexes. Recent years have seen recognition of the importance of respiratory pattern generation in addition to rhythm generation. Respiratory-modulated cranial motoneurons (laryngeal, pharyngeal, hypoglossal, facial) offer a unique insight into the control of respiration since: (1) they receive rhythmic respiratory inputs but; (2) their respiratory-modulated firing pattern differs to that of phrenic neurons to suit their function, (for example, hypoglossal motoneurons begin firing and thus the tongue depresses before the onset of phrenic nerve discharge and diaphragmatic during inspiration) and; (3) their activity is often altered in parallel with changes in respiration during stereotypical non-respiratory behaviours such as coughing, swallowing and sneeze. Here we review some mechanisms that modulate the respiratory-related activity of laryngeal motoneurons with an emphasis on the generation of post-inspiratory activity.

Keywords

Glycine Respiration Adduct Dick Cough 

Notes

Acknowledgements

Supported by the Garnett Passe and Rodney Williams Memorial Foundation, NHMRC (457069, 457080) and MQRES scholarship.

References

  1. Alheid, G.F., Milsom, W.K., and McCrimmon, D.R. (2004) Pontine influences on breathing: An overview. Respir. Physiol. Neurobiol. 143, 105–114.CrossRefPubMedGoogle Scholar
  2. Arita, H., Ichikawa, K., and Sakamoto, M. (1995) Serotonergic cells in nucleus raphe pallidus provide tonic drive to posterior cricoarytenoid motoneurons via 5-hydroxytryptamine2 receptors in cats. Neurosci. Lett. 197, 113–116.CrossRefPubMedGoogle Scholar
  3. Arnold, G.E. (1961) Physiology and pathology of the cricothyroid muscle. Laryngoscope 71, 687–753.CrossRefPubMedGoogle Scholar
  4. Baekey, D.M., Morris, K.F., Gestreau, C., Li, Z., Lindsey, B.G., and Shannon, R. (2001) Medullary respiratory neurones and control of laryngeal motoneurones during fictive eupnoea and cough in the cat. J. Physiol. 534, 565–581.CrossRefPubMedGoogle Scholar
  5. Barillot, J.C., Grélot, L., Reddad, S., and Bianchi, A.L. (1990) Discharge patterns of laryngeal motoneurones in the cat: An intracellular study. Brain Res. 509, 99–106.CrossRefPubMedGoogle Scholar
  6. Bartlett, D.J. (1986) Upper airway motor systems. In N.S. Cherniack and J.G. Widdicombe (Eds.), Handbook for physiology (pp. 223–245). Bethesda, MD: The American Physiological Society.Google Scholar
  7. Berkowitz, R.G., Sun, Q.-J., and Pilowsky, P.M. (2005) Congenital bilateral vocal cord paralysis and the role of glycine. In Annals of otology, rhinology and laryngology (pp. 494–498). Annals Publishing Company.Google Scholar
  8. Bieger, D. and Hopkins, D.A. (1987) Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: The nucleus ambiguus. J. Comp. Neurol. 262, 546–562.CrossRefPubMedGoogle Scholar
  9. Dean, J.B., Czyzyk-Krzeska, M., and Millhorn, D.E. (1989) Experimentally induced postinhibitory rebound in rat nucleus ambiguus is dependent on hyperpolarization parameters and membrane potential. Neurosci. Res. 6, 487–493.CrossRefPubMedGoogle Scholar
  10. Dick, T.E., Baekey, D.M., Paton, J.F.R., Lindsey, B.G., and Morris, K.F. (2009) Cardio-respiratory coupling depends on the pons. Respir. Phys. Neurobiol. 168, 76–85.CrossRefGoogle Scholar
  11. Dick, T.E., Bellingham, M.C., and Richter, D.W. (1994) Pontine respiratory neurons in anesthetized cats. Brain Res. 636, 259–269.CrossRefPubMedGoogle Scholar
  12. Dutschmann, M. and Paton, J.F.R. (2002) Glycinergic inhibition is essential for co-ordinating cranial and spinal respiratory motor outputs in the neonatal rat. J. Physiol. 543, 643–653.CrossRefPubMedGoogle Scholar
  13. Dutschmann, M. and Herbert, H. (2006) The Kolliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur. J. Neurosci. 24, 1071–1084.CrossRefPubMedGoogle Scholar
  14. Ezure, K. and Manabe, M. (1988) Decrementing expiratory neurons of the Botzinger complex. II. Direct inhibitory synaptic linkage with ventral respiratory group neurons. Exp. Brain Res. 72, 159–166.CrossRefPubMedGoogle Scholar
  15. Ezure, K. and Tanaka, I. (2006) Distribution and medullary projection of respiratory neurons in the dorsolateral pons of the rat. Neuroscience 141, 1011–1023.CrossRefPubMedGoogle Scholar
  16. Gauthier, P., Hilaire, G., and Monteau, R. (1983) Onset and control of expiratory laryngeal discharge: Cross-correlation analysis. Respir. Physiol. 54, 67–77.CrossRefPubMedGoogle Scholar
  17. Haji, A., Takeda, R., and Remmers, J.E. (1992) Evidence that glycine and GABA mediate postsynaptic inhibition of bulbar respiratory neurons in the cat. J. Appl. Physiol. 73, 2333–2342.PubMedGoogle Scholar
  18. Hayakawa, T., Takanaga, A., Maeda, S., Ito, H., and Seki, M. (2000) Monosynaptic inputs from the nucleus tractus solitarii to the laryngeal motoneurons in the nucleus ambiguus of the rat. Anat. Embryol. (Berl.) 202, 411–420.CrossRefGoogle Scholar
  19. Hilaire, G. and Gauthier, P. (1983) Central respiratory drive and recruitment order of phrenic and inspiratory laryngeal motoneurons. Respir. Physiol. 51, 341–359.CrossRefPubMedGoogle Scholar
  20. Horner, R.L., Kozar, L.F., and Phillipson, E.A. (1994) Tonic respiratory drive in the absence of rhythm generation in the conscious dog. J. Appl. Physiol. 76, 671–680.CrossRefPubMedGoogle Scholar
  21. Milligan, C.J., Edwards, I.J., and Deuchars, J. (2006) HCN1 ion channel immunoreactivity in spinal cord and medulla oblongata. Brain Res. 1081, 79–91.CrossRefPubMedGoogle Scholar
  22. Nunez-Abades, P.A., Portillo, F., and Pasaro, R. (1990) Characterisation of afferent projections to the nucleus ambiguus of the rat by means of fluorescent double labelling. J. Anat. 172, 1–15.PubMedGoogle Scholar
  23. Onimaru, H., Ikeda, K., and Kawakami, K. (2009) Phox2b, RTN/pFRG neurons and respiratory rhythmogenesis. Respir. Physiol. & Neurobiol. 168, 13–18.CrossRefGoogle Scholar
  24. Ono, K., Shiba, K., Nakazawa, K., and Shimoyama, I. (2006) Synaptic origin of the respiratory-modulated activity of laryngeal motoneurons. Neuroscience 140, 1079–1088.CrossRefPubMedGoogle Scholar
  25. Pierrefiche, O., Haji, A., Bischoff, A., and Richter, D.W. (1999) Calcium currents in respiratory neurons of the cat in vivo. Pflugers Arch. Eur. J. Physiol. 438, 817.CrossRefGoogle Scholar
  26. Richardson, M.A. and Adams, J. (2005) Fatal apnea in piglets by way of laryngeal chemoreflex: Postmortem findings as anatomic correlates of sudden infant death syndrome in the human infant. Laryngoscope 115, 1163–1169.CrossRefPubMedGoogle Scholar
  27. Shiba, K., Nakazawa, K., Ono, K., and Umezaki, T. (2007) Multifunctional laryngeal premotor neurons: Their activities during breathing, coughing, sneezing, and swallowing. J. Neurosci. 27, 5156–5162.CrossRefPubMedGoogle Scholar
  28. Smith, J.C., Abdala, A.P.L., Koizumi, H., Rybak, I.A., and Paton, J.F.R. (2007) Spatial and functional architecture of the mammalian brain stem respiratory network: A hierarchy of three oscillatory mechanisms. J. Neurophysiol. 98, 3370–3387.CrossRefPubMedGoogle Scholar
  29. Sun, Q.-J., Berkowitz, R.G., and Pilowsky, P.M. (2005) Response of laryngeal motoneurons to hyperventilation induced apnea in the rat. Respir. Physiol. Neurobiol. 146, 155–163.CrossRefPubMedGoogle Scholar
  30. Sun, Q.-J., Berkowitz, R.G., and Pilowsky, P.M. (2008) GABA a mediated inhibition and post-inspiratory pattern of laryngeal constrictor motoneurons in rat. Respir. Physiol. Neurobiol. 162, 41–47.CrossRefPubMedGoogle Scholar
  31. Surges, R., Sarvari, M., Steffens, M., and Els, T. (2006) Characterization of rebound depolarization in hippocampal neurons. Biochem. Biophys. Res. Comm. 348, 1343–1349.CrossRefPubMedGoogle Scholar
  32. Waldbaum, S., Hadziefendic, S., Erokwu, B., Zaidi, S.I.A., and Haxhiu, M.A. (2001) CNS innervation of posterior cricoarytenoid muscles: A transneuronal labeling study. Respir. Physiol. 126, 113–125.CrossRefPubMedGoogle Scholar
  33. Yajima, Y., Hayakawa, T., and Hayashi, Y. (1997) Evidence for GABAA receptor-mediated inhibition in ambiguous motoneurons. Acta Otolaryngol. (Suppl.) 532, 132–134.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Tara G. Bautista
    • 1
  • Peter G.R. Burke
    • 1
  • Qi-Jian Sun
    • 1
  • Robert G. Berkowitz
    • 2
  • Paul M. Pilowsky
    • 1
  1. 1.Australian School of Advanced MedicineMacquarie UniversitySydneyAustralia
  2. 2.Departments of Otolaryngology and PaediatricsRoyal Children’s HospitalMelbourneAustralia

Personalised recommendations