Advertisement

Dysrhythmias of The Respiratory Oscillator

  • David Paydarfar
  • Daniel M. Buerkel

Abstract

Breathing is regulated by a central neural oscillator that produces rhythmic output to the respiratory muscles. Pathological disturbances in the rhythm of breathing can lead to prolonged apnea and severe hypoxemia. Respiratory recordings[1] of these potentially fatal episodes have shown that in some cases, most commonly in sleeping infants, the first sign of apnea is cessation of rhythmic contraction of the diaphragm without airway obstruction, suggesting that the disturbance is due to loss of rhythmicity of the brainstem respiratory oscillator. These dysrhythmias often arise unexpectedly, i.e., they are immediately preceded by a normal respiratory pattern and a normal metabolic profile. In some instances prolonged apneic pauses are associated with or triggered by brief physiological stimuli such as exposure to sound[2],[3], stimulation of the face [4],[5], oropharynx or larynx[6], and swallowing[7]. All infants are frequently exposed to these brief physiological stimuli, so the mechanism by which generally benign perturbations could on rare occasion cause prolonged apnea has remained a mystery.

Keywords

Singular Point Respiratory Rhythm Stimulus Strength Superior Laryngeal Nerve Phase Reset 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Southall, D. P., and D. G. Talbert. Mechanisms for abnormal apnea of possible relevance to the sudden infant death syndrome. Ann. NY Acad. Sci. 533: 329–349, 1988.PubMedCrossRefGoogle Scholar
  2. 2.
    Gerhart, H.-J., H. Wagner, I. Thomschke, and B. Pasch. Zur Beeinflussbarkeit der Atmung durch rhythmische akustische Reize. Z. Laryngol. Rhinol. Otol. 46: 235–247, 1967.Google Scholar
  3. 3.
    Heron, T. G., and R. Jacobs. A physiological response of the neonate to auditory stimulation. Int. Aud. 7: 41–47, 1968.Google Scholar
  4. 4.
    Wolf, S. Sudden death and the oxygen conserving reflex. Am. Heart J. 71: 840–841, 1966.PubMedCrossRefGoogle Scholar
  5. 5.
    French, J. W., B. C. Morgan, and W. G. Guntheroth. Infant monkeys-A model for crib death. Amer. J. Dis. Child. 123: 480–484, 1972.PubMedGoogle Scholar
  6. 6.
    Downing, S. E., and J. C. Lee. Laryngeal chemosensitivity: a possible mechanism for sudden infant death. Pediatrics 55: 640–649, 1975.PubMedGoogle Scholar
  7. 7.
    Wilson, S. L., B. T. Thach, R. T. Brouillette, and Y. K. Abu-Osba. Coordination of breathing and swallowing in human infants. J. Appl. Physiol. 50: 851–858, 1981, See p. 856.PubMedGoogle Scholar
  8. 8.
    Winfree, A. T. The Geometry of Biological Time. New York: Springer-Verlag, 1980.Google Scholar
  9. 9.
    Paydarfar, D., F. L. Eldridge and J. P. Kiley. Resetting of mammalian respiratory rhythm: existence of a phase singularity. Am. J. Physiol. 250: R721–R727, 1986. (See also Kitano, S. and A. Komatsu. Central respiratory oscillator: phase-response analysis. Brain Res. 439: 19–30, 1988; Lewis, J., Bachoo, M., Polosa, C., and L. Glass. The effects of superior laryngeal nerve stimulation on the respiratory rhythm: phase-resetting and aftereffects. Brain Res. 517: 44–50, 1989.)PubMedGoogle Scholar
  10. 10.
    Paydarfar, D., and F. L. Eldridge. Phase resetting and dysrhythmic responses of the respiratory oscillator. Am. J. Physiol. 252: R55–R62, 1987.PubMedGoogle Scholar
  11. 11.
    Eldridge, F. L., D. Paydarfar, P. G. Wagner, and R. T. Dowell. Phase resetting of respiratory rhythm: effect of changing respiratory drive. Am. J. Physiol. 257: R271–R277, 1989.PubMedGoogle Scholar
  12. 12.
    Paydarfar, D., R. J. Gilbert, C. Poppel, and P. Nassab. Respiratory phase resetting and airflow changes induced by swallowing in humans. J. Physiol. 483. 1: 273–288, 1995.PubMedGoogle Scholar
  13. 13.
    Smith, D. M., R. R. Mercer, and F. L. Eldridge. Servo control of end-tidal CO2 in paralyzed animals. J. Appl. Physiol. 45: 133–136, 1978.PubMedGoogle Scholar
  14. 14.
    Eldridge, F. L. Relationship between respiratory nerve and muscle activity and muscle force output. J. Appl. Physiol. 39: 567–574, 1975.PubMedGoogle Scholar
  15. 15.
    Fitzhugh, R. Impulses and physiological states in theoretical models of nerve membrane. Biophys. J. 1: 445–466, 1961.CrossRefPubMedGoogle Scholar
  16. 16.
    Also called the Fitzhugh-Nagumo equations. See Nagumo, J. S., S. Arimoto, and S. Yoshizawa. An active pulse transmission line simulating nerve axon. Proc. IRE. 50: 2061–2070, 1962.CrossRefGoogle Scholar
  17. 17.
    Bifurcation analysis has led to the same conclusion (see Hadeler, K. P., U. Van Der Heiden, and K. Schumacher. Generation of nervous impulse and periodic oscillations. Biol. Cybernet. 23:211–218, 1976; Baer, S. M., T. Erneux, and J. Rinzel. The slow passage through a Hopf bifurcation: delay, memory effects, and resonance. SIAM J. Appl. Math. 49: 55–71, 1989.Google Scholar
  18. 18.
    Eldridge, F. L. (personal correspondence to D. Paydarfar, 1990). See also reference 11 for similar scaling factor for the van der Pol equation.Google Scholar
  19. 19.
    Remmers, J.E., DeGroot, W.J., Sauerland, E.K., and Anch, A. Pathogenesis of upper airway occlusion during sleep. J. Appl. Physiol. 44: 931–938, 1978.PubMedGoogle Scholar
  20. 20.
    Southall, D. P., V. Stebbens, and N. Abraham. Prolonged apnoea with severe arterial hypoxaemia resulting from complex partial seizures. Dev. Med. Child Neurol. 29: 784–804, 1987.PubMedCrossRefGoogle Scholar
  21. 21.
    Brazy, J. E., H. C. Kinney, and W. J. Oakes. Central nervous system lesions causing apnea at birth. J. Pediatr. 111: 163–175, 1987.PubMedCrossRefGoogle Scholar
  22. 22.
    Kinney, H. C., J. J. Filiano, and R. M. Harper. The Neuropathology of the Sudden Infant Death Syndrome. A Review. J. Neuropathol Exp Neurol 51: 115–126, 1992.PubMedCrossRefGoogle Scholar
  23. 23.
    Dwyer, T., A.-L. B. Ponsonby, N.M. Newman, L. E. Gibbons. Prospective cohort study of prone sleeping position and sudden infant death syndrome. Lancet 337: 1244–1247, 1991.PubMedCrossRefGoogle Scholar
  24. 24.
    Feldman, J. L., and J. D. Cowan. Large-scale activity in neural nets II: A model for the brainstem respiratory oscillator. Biol. Cybern. 17:39–51, 1975.PubMedCrossRefGoogle Scholar
  25. 25.
    Botros, S. M., and E. N. Bruce. Neural network implementation of a three-phase model of respiratory rhythm generation. Biol. Cybern 63: 143–153, 1990.PubMedCrossRefGoogle Scholar
  26. 26.
    Lewis. J., L. Glass, M. Bachoo, and C. Polosa. Phase resetting and fixed-delay stimulation of a simple model of respiratory rhythm generation. J. Theor. Biol. 159: 491–506, 1992.PubMedCrossRefGoogle Scholar
  27. 27.
    Lumsden, T. Observations on the respiratory centers. J. Physiol. Lond. 57: 354–367, 1923.PubMedGoogle Scholar
  28. 28.
    Lumsden, T. Observations on the respiratory centers in the cat. J. Physiol. Lond. 57: 153–160, 1923.PubMedGoogle Scholar
  29. 29.
    Lumsden, T. The regulation of respiration. Part 1. J. Physiol. Lond. 58: 81–91, 1923.PubMedGoogle Scholar
  30. 30.
    von Euler, C. Brain stem mechanisms for generation and control of breathing pattern. In: Handbook of Physiology. The Respiratory System II, edited by N. S. Cherniack and J. G. Widdicombe. Bthesda. MD: American Physiological Society, 1986, p. 43, fig. 33.Google Scholar
  31. 31.
    Eldridge, F. L., and D. Paydarfar. Phase resetting of respiratory rhythm studied in a model of a limit-cycle oscillator: influence of stochastic processes. In: Respiratory Control, edited by G. D. Swanson, F. S. Grodins, and R. L. Hughson. New York: Plenum Publishing Corporation, 1989, p. 379–388.Google Scholar
  32. 32.
    Glass, L., and A._T. Winfree. Discontinuities in phase-resetting experiments. Am. J. Physiol. 246: R251–R258, 1984.PubMedGoogle Scholar
  33. 33.
    Lewis, J., M. Bachoo, C. Polosa, and L. Glass. The effects of superior laryngeal nerve stimulation on the respiratory rhythm: phase-resetting and aftereffects. Brain Res. 517: 44–50, 1989.CrossRefGoogle Scholar
  34. 34.
    Moore, G. P., D. H. Perkel, and J. P. Segundo. Statistical analysis and functional interpretation of neuronal spike data. Annu. Rev. Physiol. 28: 493–522, 1966.PubMedCrossRefGoogle Scholar
  35. 35.
    Croner, L. J., K. Purpura, and E. Kaplan. Response variability in retinal ganglion cells of primates. Proc. Natl. Acad. Sci. (USA) 90:8128–8130, 1993.CrossRefGoogle Scholar
  36. 36.
    Douglass, J. K., L. Wilkens, E. Pantazelou, and F. Moss. Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365: 337–340, 1993.PubMedCrossRefGoogle Scholar
  37. 37.
    Glass, L. C. C. Graves, G. A. Petrillo, and M. C. Mackey. Unstable dysnamics of a periodically driven oscillator in the presence of noise. J. Theor. Biol. 86: 455–475, 1980.PubMedCrossRefGoogle Scholar
  38. 38.
    Kurrer, C., and K. Schulten. Effect of noise and perturbations on limit cycle systems. Physica D 50: 311–320, 1991.CrossRefGoogle Scholar
  39. 39.
    Shannon, R. Reflexes from respiratory muscles and costovertebral joints. In: Handbook of Physiology The Respiratory System II, edited by N.S. Cherniack and J.G. Widdicombe. Bethesda MD: American Physiological Society, 1986, p. 431–447.Google Scholar
  40. 40.
    Bradford, L. J. Respiratory Audiometry. In: Physiological Measures of the Audio-Vestibular System, edited by L. J. Bradford. New York: Academic Press, 1975, p. 249–317.Google Scholar

Copyright information

© Plenum Press 1996

Authors and Affiliations

  • David Paydarfar
    • 1
  • Daniel M. Buerkel
    • 1
  1. 1.Departments of Medicine and Biomedical ResearchSt. Elizabeth’s Medical Center of Boston and Tufts University School of Medicine Boston

Personalised recommendations