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Pflügers Archiv

, Volume 365, Issue 1, pp 49–59 | Cite as

Metabolic control of respiratory neuronal activity and the accompanying changes in breathing movements of the rabbit

I. Manipulation of inspiratory and experiatory-inspiratory neurons
  • R. A. Chaplain
  • H. R. O. Dinse
  • M. Fallert
Article

Summary

The property of the neuronal membrane to be permeable to metabolic modifiers of two regulatory enzymes has been utilized to manipulate the spike activity of inspiratory (I) and expiratory-inspiratory (EI) neurons of the bulbar respiratory centre. The neurons have been classified according to their response to lung distension or collapse (α- or β-type) and to hyperventilation (tonic firing denoted by “+”, cessation of activity by “−”). Using extracellular microelectrodes for single unit recording, the medulla oblongata was superfused with a metabolite-containing CSF. The various neuronal sub-types exhibited a differential activating or inhibitory response to one or several metabolic effectors. For example I α + units were activated by 5 mM glucose-6-phosphate (G-6-P) and 3.5 mM 3-phosphoglycerate (3-PGA), which both inhibited I β + neurons, while 5 mM AMP inhibited I α + much more strongly than I β + cells. The spike density of I α and I β neurons was increased in the presence of 2.5 mM fructose-6-phosphate and 3.5–5 mM AMP, but became reduced by G-6-P. In contrast, 3 mM fructose-1,6-diphosphate and 5 mM 3-PGA activated the I α but inhibited the I β neurons. The EIβ units were characteristically activated by 10 mM citrate, which inhibited all I-type neurons. Activations of the Iα and Iβ neurons led to an accelerated respiratory rate and a higher tidal volume, while the opposite was true for EIβ neurons. Intravenous injection of metabolites could not duplicate the striking effects under local applications.

Key words

Bulbar respiratory centre Inspiratory neurons Respiratory movements Neuronal classification Metabolic modifiers of neuronal activity 

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References

  1. Baumgarten, R. von: Zur Technik der Mikroableitung am pulsierenden Gehirn. Naturwissenschaften44 22–23 (1957)Google Scholar
  2. Baumgarten, R. von, Kanzow, E.: The interaction of two types of inspiratory neurons in the region of the tractus solitarius of the cat. Arch. ital. Biol.96, 361–373, (1958)Google Scholar
  3. Betz, A.: Oscillatory control of glycolysis as a model for biological timing processes. In: Quantitative biology of metabolism. A. Locker, ed. Berlin-Heidelberg-New York: Springer 1968Google Scholar
  4. Böhmer, G., Chaplain, R. A., Fallert, M.: Metabolic control of respiratory neuronal activity and the accompanying changes in breathing movements of the rabbit. II. Manipulation of expiratory and inspiratory-expiratory neurons. Pflügers Arch.365, 61–68 (1976)Google Scholar
  5. Broman, T., Steinwall, O.: Model of the blood-brain barrier system. In: Brain edema (I. Klatzo and F. Seitelberger, eds.) Berlin-Heidelberg-New York: Springer 1967Google Scholar
  6. Burns, B. D., Salmoriraghi, G. C.: Repetitive firing of respiratory neurons during their burst activity. J. Neurophysiol.23, 27–46 (1960)Google Scholar
  7. Chaplain, R. A.: Metabolic regulations of the rhythmic activity in pacemaker neurons. II. Metabolically induced conversion of beating to bursting pacemaker activity in Aplysia neurons. Brain Research106, 307–319 (1976)Google Scholar
  8. Chaplain, R. A., Baumgarten, R. von: Metabolic aspects of neuronal learning. Pflügers Arch.355 (Suppl.) R 87 (1975)Google Scholar
  9. Chaplain, R. A., Krämer, G.: Metabolic regulations of the rhythmic activity in pacemaker neurons. I. Frequency-setting of beating Aplysia pacemakers by modifiers of phosphofructokinase and fructose-1,6-diphosphatase. Pflügers Arch.359 (Suppl.) R 83 (1975)Google Scholar
  10. Cohen, M. I.: Discharge patterns of brain stem respiratory neurons in relation to carbon dioxide tension. J. Neurophysiol.31, 142–165 (1968)Google Scholar
  11. Cohen, M. I.: The genesis of respiratory rhythmicity. In: Central rhythmic and regulation, circulation, respiration, extrapyramidal motor system (W. Umbach and H. P. Koepchen, eds.), pp. 15–35. Stuttgart: Hippokrates-Verlag 1974Google Scholar
  12. Crone, C.: The permeability of brain capillaries to non-electrolytes. Acta physiol. scand.64, 407–417 (1965)Google Scholar
  13. Dinse, H. R. O., Fallert, M., Böhmer, G., Chaplain, R. A.: Metabolic control of respiratory neuronal activity and the accompanying changes in breathing movements of the rabbit. III. Phase shifts in respiratory neurons induced by inflation and collapse of the lung, hyperventilation or metabolic modifiers. Pflügers Arch.365, 69–75 (1976)Google Scholar
  14. Euler, C. von, Hayward, J. N., Marttila, I., Wyman, R.: Vagal and spinal connections of the inspiratory neurons of the ventrolateral nucleus of the tractus solitarius of the cat. Arch. Fisiol.68, 327–328 (1972)Google Scholar
  15. Fallert, M.: Der Hering-Breuer Reflex bei künstlicher Beatmung des Kaninchens. III. Die Wirkung von intermittierender, durch den Respirator selbst gesteuerter, afferenter Vagusreizung. Pflügers Arch.333, 166–181 (1972)Google Scholar
  16. Fallert, M., Corinth, G.: A device to trigger automatically electrical stimulation at different states of in- or expiration on the back-ground of variable lung inflation in the rabbit. Pflügers Arch.357, 139–143 (1975)Google Scholar
  17. Fujita, U.: Elektromyographisches Studium des Zwerchfelltonus. Pflügers Arch. ges. Physiol.203, 472–479 (1924)Google Scholar
  18. Kirk, J. E., Laursen, T. J. S.: Diffusion coefficients of various solutes for human aortic tissue with special reference to variation in tissue permeability with age. J. Geront.10, 288–302 (1955)Google Scholar
  19. Lipscomb, W. T., Boyarsky, L. L.: Neurophysiological investigations of medullary chemosensitive areas of respiration. Respir. Physiol.16, 362–376 (1972)Google Scholar
  20. Loeschcke, H. H.: Intracranielle Chemoreceptoren mit Wirkung auf die Atmung. Helv. physiol. pharmacol. Acta15, C25-C26 (1957)Google Scholar
  21. Loeschcke, H. H., Koepchen, H. P.: Über das Verhalten der Atmung und des arteriellen Drucks bei Einbringen von Veratridin, Lobelin und Cynanid in den Liquor cerebrospinalis. Pflügers Arch. ges. Physiol.266, 586–610 (1958)Google Scholar
  22. 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.10, 184–197 (1970)Google Scholar
  23. Mitchell, R. A., Loeschcke, H. H., Massion, W. H., Severinghaus, J. W.: Respiratory responses mediated through superficial chemosensitive areas on the medulla. J. appl. Physiol.18, 523–533 (1963)Google Scholar
  24. Mitchell, R. A., Loeschcke, H. H., Severinghaus, J. W., Richardson, B. W., Massion, W. H.: Regions of respiratory chemosensitivity on the surface of the medulla. Ann. N. Y. Acad. Sci.109, 661–681 (1963)Google Scholar
  25. Mitchell, R. A., Massion, W. H., Carman, C. S., Severinghaus, J. W.: 4th ventricle respiratory chemosensitivity and the area postrema. Fed. Proc.19, 374 (1960)Google Scholar
  26. Pappenheimer, J. R., Fencl, V., Heisey, S. R., Held, D.: Role of cerebral fluids in control of respiration as studied in unanesthetized goats. Amer. J. Physiol.208, 436–450 (1965)Google Scholar
  27. Salmoiraghi, G. C., Baumgarten, R. von: Intracellular potentials from respiratory neurons in brain stem of cat and mechanism of rhythmic respiration. J. Neurophysiol.24, 203–218 (1961)Google Scholar
  28. Salmoiraghi, G. C., Burns, B. D.: Localisation and patterns of discharge of respiratory neurons in brain-stem of cat. J. Neurophysiol.23, 2–13 (1960)Google Scholar
  29. Schläfke, M. E., Loeschcke, H. H.: Lokalisation eines an der Regulation von Atmung und Kreislauf beteiligten Gebietes an der ventralen Oberfläche der Medulla oblongata durch Kälteblokkade. Pflügers Arch. ges. Physiol.297, 201–220 (1967)Google Scholar
  30. Schläfke, M. E., See, W. R., Loeschcke, H. H.: Ventilatory response to alterations of H+ ion concentration in small areas of the ventral medullary surface. Respir. Physiol.10, 198–212 (1970)Google Scholar
  31. Wyss, O. A. M.: Die tonische Innervation des Zwerchfells. Pflügers Arch. ges. Physiol.244, 712–735 (1941)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • R. A. Chaplain
    • 1
  • H. R. O. Dinse
    • 1
  • M. Fallert
    • 1
  1. 1.Physiologisches Institut der Universität MainzMainzGermany

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