Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Aug 1;502(Pt 3):623–639. doi: 10.1111/j.1469-7793.1997.623bj.x

Rhythmic bursting of pre- and post-inspiratory neurones during central apnoea in mature mice.

J F Paton 1
PMCID: PMC1159533  PMID: 9279813

Abstract

1. Stimulation of pulmonary vagal C fibres (PCFs) inhibits inspiration but the response pattern of respiratory rhythm-generating neurones is unknown. This study provides the first description of the effects of PCF stimulation on six different types of respiratory neurones located in the ventrolateral medulla of the mature mouse. 2. Studies were performed in both urethane-anaesthetized (1.5 g kg-1 I.P.) mature mice and in an arterially perfused working heart-brainstem preparation (WHBP). In both preparations the respiratory motor pattern of phrenic and recurrent laryngeal nerves were comparable. Stimulation of PCFs, using phenylbiguanide (2-5 micrograms) injected into the right atrium, evoked a similar respiratory and cardiac response pattern in both anaesthetized and perfused mice, which included: (i) a significant prolongation of the inter-inspiratory interval; (ii) an increase in the duration and amplitude of post-inspiratory (PI) activity; and (iii) an atropine-sensitive bradycardia (50-260 beats min-1). 3. In the WHBP, PCF stimulation evoked a depolarization (11 +/- 1 mV) and high frequency tonic discharge (up to 64 Hz) in ten out of twenty-one PI neurones. During the PCF-induced prolongation of PI activity all other PI neurones (n = 11), as well as pre-inspiratory neurones (PreI; n = 11), displayed oscillations in membrane potential and/or rhythmic bursting at a similar frequency of 0.7-1.0 Hz. Other respiratory neurones recorded, including stage II expiratory neurones (n = 7), early- (n = 6), ramp- (n = 16) and late-inspiratory neurones (n = 4), ceased firing rhythmically during PCF stimulation. 4. The firing behaviour of PI and PreI neurones was assessed after switching to a low Ca2+ (0.2 mM)-high Mg2+ (5.25 mM) perfusate to block synaptic transmission in the WHBP. In the absence of synaptic transmission, PreI neurones (n = 7/8) continued to discharge rhythmically, whereas all other respiratory cell types (including PI neurones, n = 5) fired tonically. 5. In conclusion, stimulation of PCFs elicits a reflex-evoked prolongation of the PI phase of the respiratory cycle and excitation of PI neurones including rhythmic discharging. It is suggested that this rhythmic bursting depends on inhibitory connections from PreI neurones. The functional significance of these central 'apnoeic rhythms' are discussed.

Full text

PDF
623

Selected References

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

  1. Cohen M. I. Discharge patterns of brain-stem respiratory neurons during Hering-Breuer reflex evoked by lung inflation. J Neurophysiol. 1969 May;32(3):356–374. doi: 10.1152/jn.1969.32.3.356. [DOI] [PubMed] [Google Scholar]
  2. Coleridge H. M., Coleridge J. C., Luck J. C. Pulmonary afferent fibres of small diameter stimulated by capsaicin and by hyperinflation of the lungs. J Physiol. 1965 Jul;179(2):248–262. doi: 10.1113/jphysiol.1965.sp007660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Daly M. D. Some reflex cardioinhibitory responses in the cat and their modulation by central inspiratory neuronal activity. J Physiol. 1991 Aug;439:559–577. doi: 10.1113/jphysiol.1991.sp018682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eglen R. M., Lee C. H., Khabbaz M., Fontana D. J., Daniels S., Kilfoil T., Wong E. H. Comparison of potencies of 5-HT3 receptor antagonists at inhibiting aversive behavior to illumination and the von Bezold-Jarisch reflex in the mouse. Neuropharmacology. 1994 Feb;33(2):227–234. doi: 10.1016/0028-3908(94)90013-2. [DOI] [PubMed] [Google Scholar]
  5. Haji A., Takeda R. Variations in membrane potential trajectory of post-inspiratory neurons in the ventrolateral medulla of the cat. Neurosci Lett. 1993 Jan 12;149(2):233–236. doi: 10.1016/0304-3940(93)90779-k. [DOI] [PubMed] [Google Scholar]
  6. Johnson S. M., Smith J. C., Funk G. D., Feldman J. L. Pacemaker behavior of respiratory neurons in medullary slices from neonatal rat. J Neurophysiol. 1994 Dec;72(6):2598–2608. doi: 10.1152/jn.1994.72.6.2598. [DOI] [PubMed] [Google Scholar]
  7. Klages S., Bellingham M. C., Richter D. W. Late expiratory inhibition of stage 2 expiratory neurons in the cat--a correlate of expiratory termination. J Neurophysiol. 1993 Oct;70(4):1307–1315. doi: 10.1152/jn.1993.70.4.1307. [DOI] [PubMed] [Google Scholar]
  8. Onimaru H., Arata A., Homma I. Firing properties of respiratory rhythm generating neurons in the absence of synaptic transmission in rat medulla in vitro. Exp Brain Res. 1989;76(3):530–536. doi: 10.1007/BF00248909. [DOI] [PubMed] [Google Scholar]
  9. Onimaru H., Ballanyi K., Richter D. W. Calcium-dependent responses in neurons of the isolated respiratory network of newborn rats. J Physiol. 1996 Mar 15;491(Pt 3):677–695. doi: 10.1113/jphysiol.1996.sp021249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. PAINTAL B. A. Impulses in vagal afferent fibres from specific pulmonary deflation receptors: the response of these receptors to phenyl diguanide, potato starch, 5-hydroxytryptamine and nicotine, and their rôle in respiratory and cardiovascular reflexes. Q J Exp Physiol Cogn Med Sci. 1955 Apr;40(2):89–111. doi: 10.1113/expphysiol.1955.sp001116. [DOI] [PubMed] [Google Scholar]
  11. Paintal A. S. Mechanism of stimulation of type J pulmonary receptors. J Physiol. 1969 Aug;203(3):511–532. doi: 10.1113/jphysiol.1969.sp008877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Paton J. F. A working heart-brainstem preparation of the mouse. J Neurosci Methods. 1996 Mar;65(1):63–68. doi: 10.1016/0165-0270(95)00147-6. [DOI] [PubMed] [Google Scholar]
  13. Paton J. F., Richter D. W. Maturational changes in the respiratory rhythm generator of the mouse. Pflugers Arch. 1995 May;430(1):115–124. doi: 10.1007/BF00373846. [DOI] [PubMed] [Google Scholar]
  14. Paton J. F., Richter D. W. Role of fast inhibitory synaptic mechanisms in respiratory rhythm generation in the maturing mouse. J Physiol. 1995 Apr 15;484(Pt 2):505–521. doi: 10.1113/jphysiol.1995.sp020682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Paton J. F. The ventral medullary respiratory network of the mature mouse studied in a working heart-brainstem preparation. J Physiol. 1996 Jun 15;493(Pt 3):819–831. doi: 10.1113/jphysiol.1996.sp021425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Remmers J. E., Richter D. W., Ballantyne D., Bainton C. R., Klein J. P. Reflex prolongation of stage I of expiration. Pflugers Arch. 1986 Aug;407(2):190–198. doi: 10.1007/BF00580675. [DOI] [PubMed] [Google Scholar]
  17. Richter D. W., Ballantyne D., Remmers J. E. The differential organization of medullary post-inspiratory activities. Pflugers Arch. 1987 Nov;410(4-5):420–427. doi: 10.1007/BF00586520. [DOI] [PubMed] [Google Scholar]
  18. Richter D. W., Ballanyi K., Schwarzacher S. Mechanisms of respiratory rhythm generation. Curr Opin Neurobiol. 1992 Dec;2(6):788–793. doi: 10.1016/0959-4388(92)90135-8. [DOI] [PubMed] [Google Scholar]
  19. Richter D. W. Generation and maintenance of the respiratory rhythm. J Exp Biol. 1982 Oct;100:93–107. doi: 10.1242/jeb.100.1.93. [DOI] [PubMed] [Google Scholar]
  20. Schwarzacher S. W., Smith J. C., Richter D. W. Pre-Bötzinger complex in the cat. J Neurophysiol. 1995 Apr;73(4):1452–1461. doi: 10.1152/jn.1995.73.4.1452. [DOI] [PubMed] [Google Scholar]
  21. Smith J. C., Ellenberger H. H., Ballanyi K., Richter D. W., Feldman J. L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science. 1991 Nov 1;254(5032):726–729. doi: 10.1126/science.1683005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wilson C. G., Zhang Z., Bonham A. C. Non-NMDA receptors transmit cardiopulmonary C fibre input in nucleus tractus solitarii in rats. J Physiol. 1996 Nov 1;496(Pt 3):773–785. doi: 10.1113/jphysiol.1996.sp021726. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES