Pflügers Archiv

, Volume 407, Issue 2, pp 190–198 | Cite as

Reflex prolongation of stage I of expiration

  • J. E. Remmers
  • D. W. Richter
  • D. Ballantyne
  • C. R. Bainton
  • J. P. Klein
Excitable Tissues and Central Nervous Physiology


Experiments were performed on anesthetized cats to test the theory that the interval between phrenic bursts is comprised of two phases, stage I and stage II of expiration. Evidence that these represent two separate neural phases of the central respiratory rhythm was provided by the extent to which stage duration is controlled individually when tested by superior laryngeal, vagus and carotid sinus nerve stimulation. Membrane potential trajectories of bulbar postinspiratory neurons were used to identify the timing of respiratory phases.

Stimulation of the superior laryngeal, vagus and carotid sinus nerves during stage I of expiration prolonged the period of depolarization in postinspiratory neurons without significantly changing the durations of either stage II expiratory or inspiratory inhibition, indicating a fairly selective prolongation of the first stage of expiration. Changes in subglottic pressure, insufflation of smoke into the upper airway, application of water to the larynx or rapid inflation of the lungs produced similar effects. Sustained tetanic stimulation of superior laryngeal and vagus nerves arrested the respiratory rhythm in stage I of expiration. Membrane potentials in postinspiratory, inspiratory and expiratory neurons were indicative of a prolonged postinspiratory period. Thus, such an arrhythmia can be described as a postinspiratory apneic state of the central oscillator. The effects of carotid sinus nerve stimulation reversed when the stimulus was applied during stage II expiration. This was accompanied by corresponding changes in the membrane potential trajectories in postinspiratory neurons.

The results manifest a ternary central respiratory cycle with two individually controlled phases occurring between inspiratory bursts.

Key words

Respiratory rhythm Postinspiratory phase Apneic states Tachypneic states Medullary respiratory neurons Laryngeal afferents Pulmonary afferents Carotid sinus afferents 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ballantyne D, Richter DW (1984) Postsynaptic inhibition of bulbar inspiratory neurones in cat. J Physiol (Lond) 348:67–87Google Scholar
  2. Bartlett D Jr (1979) Effects of hypercapnia and hypoxia on laryngeal resistance to airflow. Respir Physiol 37:293–302Google Scholar
  3. Bartlett D Jr (1980) Effects of vagal afferents on laryngeal responses to hypercapnia and hypoxia. Respir Physiol 42:189–198Google Scholar
  4. Bartlett D Jr, Knuth SL, Knuth KV (1981) Effects of pulmonary stretch receptor blockade on laryngeal responses to hypercapnia and hypoxia. Respir Physiol 45:67–77Google Scholar
  5. Baumgarten R v, Kanzow E (1958) The interaction of two types of inspiratory neurones in the region of the tractus solitarius of the cat. Archs Ital Biol 96:361–373Google Scholar
  6. Berger AJ (1977) Dorsal respiratory group neurons in the medulla of the cat: spinal projections, responses to lung inflation and superior laryngeal nerve stimulation. Brain Res 135:231–254Google Scholar
  7. Bianchi AL, Barillot JC (1975) Activity of medullary respiratory neurones during reflexes from the lungs in cats. Respir Physiol 25:335–352Google Scholar
  8. Black AMS, Torrance RW (1971) Respiratory oscillation in chemoreceptor discharge in control of breathing. Respir Physiol 13:229–237Google Scholar
  9. Breuer J (1968) Die Selbststeuerung der Athmung durch den Nervus vagus. S-B Akad Wiss Wien (II) 58:909–937Google Scholar
  10. Brooks JG (1982) Apnea of infancy and sudden infant death syndrome. Am J Dis Child 136:1012–1023Google Scholar
  11. Cohen MI (1969) discharge patterns of brainstem respiratory neurons during Hering-Breuer reflex evoked by lung inflation. J Neurophysiol 32:356–374Google Scholar
  12. Eldridge FL (1972a) The importance of timing on the respiratory effects of intermittent carotid sinus nerve stimulation. J Physiol (Lond) 222:297–318Google Scholar
  13. Eldridge FL (1972b) The importance of timing on the respiratory effects of intermittent carotid body chemoreceptor stimulation. J Physiol (Lond) 222:319–333Google Scholar
  14. Eldridge FL (1976) Expiratory effects of brief carotid sinus nerve and carotid body stimulation. Respir Physiol 26:395–410Google Scholar
  15. Euler C v (1983) On the central pattern generator for the basic breathing rhythmicity. J Appl Physiol Environ Exerc Physiol 55:1647–1659Google Scholar
  16. Gesell R, White F (1938) Recruitment of muscular activity and the central neurone after-discharge of hyperpnea. Am J Physiol 122:48–56Google Scholar
  17. Harding R (1984) Function of the larynx in the fetus and newborn. Ann Rev Physiol 46:645–659Google Scholar
  18. Harding R, Johnson P, McClelland ME (1979) The expiratory role of the larynx during development and the influence of behavioural state. In: Euler C v, Lagercrantz H (eds) Central nervous control mechanisms in breathing. Pergamon Press, Oxford, pp 353–359Google Scholar
  19. Hering E (1968) Die Selbststeuerung der Athmung durch den Nervus vagus. S-B Akad Wiss Wien (II) 57:672–677Google Scholar
  20. Iscoe S, Feldman JL, Cohen MI (1979) Properties of inspiratory termination by superior laryngeal and vagal stimulation. Respir Physiol 36:353–366Google Scholar
  21. Johnson P, Robinson JS, Salisbury D (1972) The onset and control of breathing after birth. In: Sir Joseph Bancroft Symposium on Fetal and Neonatal Physiology. Cambridge University Press, London, pp 217–221Google Scholar
  22. Koepchen H-P, Klussenforf D, Philipp U (1973) Mechanisms of central transmission of respiratory reflexes. Acta Neurobiol Exp 33:287–299Google Scholar
  23. Larrabee MG, Knowlton GC (1946) Excitation and inhibition of phrenic motoneurons by inflation of the lungs. Am J Physiol 147:90–99Google Scholar
  24. Lawson EE (1981) Prolonged central respiratory inhibition following reflex-induced apnea. J Appl Physiol 50:874–879Google Scholar
  25. Lipski J, McAllen M, Spyer KM (1977) The carotid chemoreceptor input to the respiratory neurones of the nucleus of tractus solitarius. Physiol (Lond) 269:797–810Google Scholar
  26. Menon AP, Schefft GL, Thach BT (1984) Frequency and significance of swallowing during prolonged apnea in infants. Am Rev Respir Dis 130:969–973Google Scholar
  27. Paintal AS (1973) Vagal sensory receptors and their reflex effects. Physiol Rev 53:159–227Google Scholar
  28. Remmers JE, Bartlett D Jr (1977) Reflex control of expiratory airflow and duration. J Appl Physiol Respir Environ Exerc Physiol 42:80–87Google Scholar
  29. Remmers JE, Richter DW, Ballantyne D (1986) Synaptic inputs to bulbar postinspiratory neurons from respiratory afferents and rostral pons. Brain Res (submitted)Google Scholar
  30. Richter DW (1982) Generation and maintenance of the respiratory rhythm. J Exp Biol 100:93–107Google Scholar
  31. Richter DW, Ballantyne D (1983) A three phase theory about the basic respiratory pattern generator. In: Schlafke ME, Koepchen HP, See WR (eds) Central neurone environment. Springer, Berlin Heidelberg New York Tokyo, pp 164–174Google Scholar
  32. Richter DW, Camerer H, Meesmann M, Rohrig N (1979) Studies on the synaptic interconnection between bulbar respiratory neurons of cats. Pflügers Arch 380:245–257Google Scholar
  33. Richter DW, Heyde F, Gabriel M (1975a) Intracellular recordings from different types of medullary respiratory neurons of the cat. J Neurophysiol 38:1162–1171Google Scholar
  34. Richter DW, Heyde F (1975b) Accommodative reactions of medullary respiratory neurons of the cat. J Neurophysiol 38: 1172–1180Google Scholar
  35. Richter DW, Remmers JE, Ballantyne D (1985a) On the inhibitory function of bulbar postinspiratory neurons. J Neuroscience (submitted)Google Scholar
  36. Sant'Ambrogio G (1982) Information arising from the tracheobronchial tree of mammals. Physiol Rev 62:531–569Google Scholar
  37. Trippenbach T (1981) Laryngeal, vagal and intercostal reflexes during the early postnatal period. J Develop Physiol 3:133–159Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • J. E. Remmers
    • 1
  • D. W. Richter
    • 1
  • D. Ballantyne
    • 1
  • C. R. Bainton
    • 1
  • J. P. Klein
    • 1
  1. 1.I. Physiologisches InstitutUniversität HeidelbergFederal Republic of Germany

Personalised recommendations