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. 1979 Nov;296:291–314. doi: 10.1113/jphysiol.1979.sp013006

The effect of carbon dioxide on the tonic and the rhythmic discharges of expiratory bulbospinal neurones.

C R Bainton, P A Kirkwood
PMCID: PMC1279079  PMID: 529096

Abstract

1. Extracellular micro-electrodes were used to measure the responses of expiratory bulbospinal neurones to CO2 in anaesthetized, paralyzed cats, ventilated with O2. Simultaneous measurements were made of phrenic nerve and intercostal nerve filament discharges. 2. Hypocapnia produced tonic activity in some of the expiratory neurones and in expiratory filaments but rendered the phrenic and inspiratory filaments silent. 3. A graded excitatory effect of CO2 on tonic activity of both the neurones and the filaments was seen which progressed smoothly and continuously to rhythmic activity as CO2 was increased and to zero as CO2 was decreased. 4. Increases in blood pressure produced effects which were opposite to those produced by CO2, and which had a faster time course. 5. The CO2 response curves of those units showing tonic activity were indistinguishable from the CO2 response curves of those which did not. 6. A mid line lesion in the medulla interrupted inspiratory activity, converting activity of expiratory bulbospinal neurones from periodic to ionic firing patterns. 7. Following such lesions the CO2 threshold for rhythmic excitation of medullary neurones was elevated and the slopes of their CO2 response curves were reduced. 8. These findings fully confirm the hypothesis put forward by Bainton, Kirkwood & Sears (1978b) that bulbospinal respiratory neurones convey both tonic and rhythmic excitation to spinal respiratory motoneurones and that the rhythmic excitation of expiratory muscles derives from a period inhibition of expiratory bulbospinal neurones which are subjected to a tonic CO2 dependent excitation which is continuously variable over the physiological range.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aminoff M. J., Sears T. A. Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones. J Physiol. 1971 Jun;215(2):557–575. doi: 10.1113/jphysiol.1971.sp009485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bainton C. R., Kirkwood P. A., Sears T. A. On the transmission of the stimulating effects of carbon dioxide to the muscles of respiration. J Physiol. 1978 Jul;280:249–272. doi: 10.1113/jphysiol.1978.sp012383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Band D. M., Cameron I. R., Semple S. J. The effect on respiration of abrupt changes in carotid artery pH and PCO2 in the cat. J Physiol. 1970 Dec;211(2):479–494. doi: 10.1113/jphysiol.1970.sp009288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Batsel H. L. Activity of bulbar respiratory neurons during passive hyperventilation. Exp Neurol. 1967 Nov;19(3):357–374. doi: 10.1016/0014-4886(67)90032-5. [DOI] [PubMed] [Google Scholar]
  5. Berger A. J. Dorsal respiratory group neurons in the medulla of cat: spinal projections, responses to lung inflation and superior laryngeal nerve stimulation. Brain Res. 1977 Oct 28;135(2):231–254. doi: 10.1016/0006-8993(77)91028-9. [DOI] [PubMed] [Google Scholar]
  6. Berger A. J., Krasney J. A., Dutton R. E. Respiratory recovery from CO 2 breathing in intact and chemodenervated awake dogs. J Appl Physiol. 1973 Jul;35(1):35–41. doi: 10.1152/jappl.1973.35.1.35. [DOI] [PubMed] [Google Scholar]
  7. Bianchi A. L. Localisation et étude des neurones respiratoires bulbaires. Mise en jeu antidromique par stimulation spinale ou vagale. J Physiol (Paris) 1971 Jan-Feb;63(1):5–40. [PubMed] [Google Scholar]
  8. Bishop B. Carotid baroreceptor modulation of diaphragm and abdominal muscle activity in the cat. J Appl Physiol. 1974 Jan;36(1):12–19. doi: 10.1152/jappl.1974.36.1.12. [DOI] [PubMed] [Google Scholar]
  9. Camerer H., Meesmann M., Richter D. W., Röhrig N. Reciprocal inhibition of bulbar respiratory neurones in the cat [proceedings]. J Physiol. 1978 Nov;284:80P–80P. [PubMed] [Google Scholar]
  10. Cohen M. I. Discharge patterns of brain-stem respiratory neurons in relation to carbon dioxide tension. J Neurophysiol. 1968 Mar;31(2):142–165. doi: 10.1152/jn.1968.31.2.142. [DOI] [PubMed] [Google Scholar]
  11. Da Silva K. M., Sayers B. M., Sears T. A., Stagg D. T. The changes in configuration of the rib cage and abdomen during breathing in the anaesthetized cat. J Physiol. 1977 Apr;266(2):499–521. doi: 10.1113/jphysiol.1977.sp011779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dutton R. E., Davies D. G., Ghatak P. K., Fitzgerald R. S. Respiration during transient perfusion of vertebral arteries with hypocapnic blood. Am J Physiol. 1969 Oct;217(4):1178–1182. doi: 10.1152/ajplegacy.1969.217.4.1178. [DOI] [PubMed] [Google Scholar]
  13. Dutton R. E., Hodson W. A., Davies D. G., Chernick V. Ventilatory adaptation to a step change in PCO2 at the caotid bodies. J Appl Physiol. 1967 Aug;23(2):195–202. doi: 10.1152/jappl.1967.23.2.195. [DOI] [PubMed] [Google Scholar]
  14. EKLUND G., VON EULER, RUTKOWSKI S. SPONTANEOUS AND REFLEX ACTIVITY OF INTERCOSTAL GAMMA MOTONEURONES. J Physiol. 1964 May;171:139–163. doi: 10.1113/jphysiol.1964.sp007368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GILL P. K. THE EFFECTS OF END-TIDAL CO2 ON THE DISCHARGE OF INDIVIDUAL PHRENIC MOTONEURONES. J Physiol. 1963 Sep;168:239–257. doi: 10.1113/jphysiol.1963.sp007190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gabriel M., Seller H. Excitation of expiratory neurones adjacent to the nucleus ambiguus by carotid sinus baroreceptor and trigeminal afferents. Pflugers Arch. 1969;313(1):1–10. doi: 10.1007/BF00586323. [DOI] [PubMed] [Google Scholar]
  17. Gelfand R., Lambertsen C. J. Dynamic respiratory response to abrupt change of inspired CO2 at normal and high PO2. J Appl Physiol. 1973 Dec;35(6):903–913. doi: 10.1152/jappl.1973.35.6.903. [DOI] [PubMed] [Google Scholar]
  18. Granit R., Kernell D., Lamarre Y. Algebraical summation in synaptic activation of motoneurones firing within the 'primary range' to injected currents. J Physiol. 1966 Nov;187(2):379–399. doi: 10.1113/jphysiol.1966.sp008097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Heymans C., Bouckaert J. J. Sinus caroticus and respiratory reflexes: I. Cerebral blood flow and respiration. Adrenaline apnoea. J Physiol. 1930 Apr 14;69(2):254–266. doi: 10.1113/jphysiol.1930.sp002648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kirkwood P. A., Sears T. A. Interaction between the monosynaptic EPSP and the central respiratory drive potential of expiratory motoneurones in the cat. J Physiol. 1973 Jul;232(1):38P–40P. [PubMed] [Google Scholar]
  21. Kirkwood P. A., Sears T. A. The synaptic connexions to intercostal motoneurones as revealed by the average common excitation potential. J Physiol. 1978 Feb;275:103–134. doi: 10.1113/jphysiol.1978.sp012180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Koepchen H. P., Klüssendorf D., Philipp U. Mechanisms of central transmission of respiratory reflexes. Acta Neurobiol Exp (Wars) 1973;33(1):287–299. [PubMed] [Google Scholar]
  23. Lipscomb W. T., Boyarsky L. L. Neurophysiological investigations of medullary chemosensitive areas of respiration. Respir Physiol. 1972 Dec;16(3):362–376. doi: 10.1016/0034-5687(72)90065-5. [DOI] [PubMed] [Google Scholar]
  24. Lipski J., McAllen R. M., Spyer K. M. The carotid chemoreceptor input to the respiratory neurones of the nucleus of tractus solitarus. J Physiol. 1977 Aug;269(3):797–810. doi: 10.1113/jphysiol.1977.sp011930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Loeschcke H. H., De Lattre J., Schläfke M. E., Trouth C. O. Effects on respiration and circulation of electrically stimulating the ventral surface of the medulla oblongata. Respir Physiol. 1970 Sep;10(2):184–197. doi: 10.1016/0034-5687(70)90082-4. [DOI] [PubMed] [Google Scholar]
  26. Merrill E. G. The lateral respiratory neurones of the medulla: their associations with nucleus ambiguus, nucleus retroambigualis, the spinal accessory nucleus and the spinal cord. Brain Res. 1970 Nov 11;24(1):11–28. doi: 10.1016/0006-8993(70)90271-4. [DOI] [PubMed] [Google Scholar]
  27. Mitchell R. A., Herbert D. A. Synchronized high frequency synaptic potentials in medullary respiratory neurons. Brain Res. 1974 Jul 26;75(2):350–355. doi: 10.1016/0006-8993(74)90760-4. [DOI] [PubMed] [Google Scholar]
  28. Mitchell R. A., Herbert D. A. The effect of carbon dioxide on the membrane potential of medullary respiratory neurons. Brain Res. 1974 Jul 26;75(2):345–349. doi: 10.1016/0006-8993(74)90759-8. [DOI] [PubMed] [Google Scholar]
  29. NAKAYAMA S., VON BAUMGARTEN LOKALISIERUNG ABSTEIGENDER ATMUNGSBAHNEN IM RUECKENMARK DER KATZE MITTELS ANTIDROMER REIZUNG. Pflugers Arch Gesamte Physiol Menschen Tiere. 1964 Oct 22;281:231–244. doi: 10.1007/BF00412424. [DOI] [PubMed] [Google Scholar]
  30. PAPPENHEIMER J. R., FENCL V., HEISEY S. R., HELD D. ROLE OF CEREBRAL FLUIDS IN CONTROL OF RESPIRATION AS STUDIED IN UNANESTHETIZED GOATS. Am J Physiol. 1965 Mar;208:436–450. doi: 10.1152/ajplegacy.1965.208.3.436. [DOI] [PubMed] [Google Scholar]
  31. Rapoport S., Susswein A., Uchino Y., Wilson V. J. Synaptic actions of individual vestibular neurones on cat neck motoneurones. J Physiol. 1977 Nov;272(2):367–382. doi: 10.1113/jphysiol.1977.sp012049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Richter D. W., Camerer H., Sonnhof U. Changes in extracellular potassium during the spontaneous activity of medullary respiratory neurones. Pflugers Arch. 1978 Sep 6;376(2):139–149. doi: 10.1007/BF00581577. [DOI] [PubMed] [Google Scholar]
  33. SEARS T. A. Activity of fusimotor fibres innervating muscle spindles in the intercostal muscles of the cat. Nature. 1963 Mar 9;197:1013–1014. doi: 10.1038/1971013a0. [DOI] [PubMed] [Google Scholar]
  34. SEARS T. A. EFFERENT DISCHARGES IN ALPHA AND FUSIMOTOR FIBRES OF INTERCOSTAL NERVES OF THE CAT. J Physiol. 1964 Nov;174:295–315. doi: 10.1113/jphysiol.1964.sp007488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. SEARS T. A. THE SLOW POTENTIALS OF THORACIC RESPIRATORY MOTONEURONES AND THEIR RELATION TO BREATHING. J Physiol. 1964 Dec;175:404–424. doi: 10.1113/jphysiol.1964.sp007524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sears T. A., Stagg D. Short-term synchronization of intercostal motoneurone activity. J Physiol. 1976 Dec;263(3):357–381. doi: 10.1113/jphysiol.1976.sp011635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sears T. A. The respiratory motoneuron and apneusis. Fed Proc. 1977 Sep;36(10):2412–2420. [PubMed] [Google Scholar]
  38. St John W. M. Integration of peripheral and central chemoreceptor stimuli by pontine and medullary respiratory centers. Fed Proc. 1977 Sep;36(10):2421–2427. [PubMed] [Google Scholar]

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