Decrementing expiratory neurons of the Bötzinger complex

II. Direct inhibitory synaptic linkage with ventral respiratory group neurons
  • K. Ezure
  • M. Manabe


In Nembutal-anesthetized, immobilized and artificially ventilated cats, decrementing expiratory (E-DEC) neurons which were excited by lung inflation were isolated in the vicinity of the Bötzinger complex. Then intracellular recordings were made from the respiratory neurons in the contralateral ventral respiratory group (VRG). The intracellular membrane potentials were averaged using extracellular spikes of the E-DEC neurons as triggers (spike-triggered averaging method). Hyperpolarizing potentials locked to the triggering spikes were obtained and they were shown to be unitary IPSPs since their polarity was reversed when averaged during passage of hyperpolarizing current. The latencies of antidromic activation of the E-DEC-neurons from the area of intracellular recordings were shorter by about 0.2 ms than those of unitary IPSPs. This showed that the connections were monosynaptic. A total of 47 pairs were analyzed and unitary IPSPs were found in 12 pairs. The E-DEC neurons inhibited both inspiratory and expiratory neurons, including bulbospinal inspiratory neurons, propriobulbar inspiratory neurons, and vagal motoneurons with expiratory activity. These inhibitory E-DEC neurons, receiving excitatory inputs from the stretch receptors of the lungs, presumably intervene in reflex loops such as the Hering-Breuer reflex and may make some contribution to normal breathing.

Key words

Spike-triggered averaging Decrementing E neurons VRG neurons Monosynaptic IPSP 


  1. Bak MJ, Schmidt EM (1977) An improved time-amplitude window discriminator. IEEE Trans Biomed Eng 24: 486–489CrossRefPubMedGoogle Scholar
  2. Ballantyne D, Richter DW (1984) Post-synaptic inhibition of bulbar inspiratory neurones in the cat. J Physiol (Lond) 348: 67–87Google Scholar
  3. Ballantyne D, Richter DW (1986) The non-uniform character of expiratory synaptic activity in expiratory bulbospinal neurones of the cat. J Physiol (Lond) 370: 433–456Google Scholar
  4. Barillot JC, Bianchi AL (1971) Activité des motoneurones laryngés pendant les réflexes de Hering-Breuer. J Physiol (Paris) 63: 783–792Google Scholar
  5. Baumgarten R von, Baumgarten A von, Schaefer KP (1957) Beitrag zur Lokalisationsfrage bulboreticulärer respiratorischer Neurone der Katze. Pflügers Arch 264: 217–227CrossRefGoogle Scholar
  6. Bianchi AL (1971) Localisation et étude des neurones respiratoires bulbaires. Mise en jeu antidromique par stimulation spinal ou vagale. J Physiol (Paris) 63: 5–40Google Scholar
  7. Bianchi AL, Barillot JC (1975) Activity of medullary respiratory neurones during reflexes from the lungs in cats. Respir Physiol 25: 335–352CrossRefPubMedGoogle Scholar
  8. Bianchi AL, Barillot JC (1982) Respiratory neurons in the region of the retrofacial nucleus: pontile, medullary, spinal and vagal projections. Neurosci Lett 31: 277–282CrossRefPubMedGoogle Scholar
  9. Burns BD, Salmoiraghi GC (1960) Repetitive firing of respiratory neurones during their burst activity. J Neurophysiol 23: 27–46PubMedGoogle Scholar
  10. Cohen MI (1969) Discharge patterns of brain-stem respiratory neurons during Hering-Breuer reflex evoked by lung inflation. J Neurophysiol 32: 356–374PubMedGoogle Scholar
  11. Cohen MI (1979) Neurogenesis of respiratory rhythm in the mammal. Physiol Rev 59: 1105–1173PubMedGoogle Scholar
  12. Cohen MI, Feldman JL, Sommer D (1985) Caudal medullary expiratory neurone and internal intercostal nerve discharges in the cat: effects of lung inflation. J Physiol (Lond) 368: 147–178Google Scholar
  13. Eyzaguirre C, Taylor JR (1963) Respiratory discharge of some vagal motoneurons. J Neurophysiol 26: 61–78Google Scholar
  14. Fedorko L, Merrill EG (1984) Axonal projections from the rostral expiratory neurones of the Bötzinger complex to medulla and spinal cord in the cat. J Physiol (Lond) 350: 487–496Google Scholar
  15. Feldman JL, Cohen MI (1978) Relation between expiratory duration and rostral medullary expiratory neuronal discharge. Brain Res 141: 172–178CrossRefPubMedGoogle Scholar
  16. Harber E, Kohn KW, Ngai SH, Holaday DA, Wang SC (1957) Localization of spontaneous respiratory neuronal activities in the medulla oblongata of the cat: a new location of the expiratory center. Am J Physiol 190: 350–355Google Scholar
  17. Hikosaka O, Igusa Y, Nakao S, Shimazu H (1978) Direct inhibitory synaptic linkage of pontomedullary reticular burst neurons with abducens motoneurons in the cat. Exp Brain Res 33: 337–352CrossRefPubMedGoogle Scholar
  18. Jankowska E, Roberts WJ (1972) Synaptic actions of single interneurones mediating reciprocal Ia inhibition of motoneurones. J Physiol (Lond) 222: 623–642Google Scholar
  19. Kalia MP (1981) Anatomical organization of central respiratory neurons. Ann Rev Physiol 43: 105–120CrossRefGoogle Scholar
  20. Kubin L, Lipski J (1980) Properties of the rostral NRA expiratory neurones projecting to the contralateral NTS group. Neurosci Lett Suppl 5: S141Google Scholar
  21. Lindsey BG, Segers LS, Shannon R (1987) Functional association among simultaneously monitored lateral medullary respiratory neurons in the cat. II. Evidence for inhibitory actions of expiratory neurons. J Neurophysiol 57: 1101–1117PubMedGoogle Scholar
  22. Lipski J, Merrill EG (1980) Electrophysiological demonstration of the projection from expiratory neurons in the rostral medulla to contralateral dorsal respiratory group. Brain Res 197: 521–524CrossRefPubMedGoogle Scholar
  23. Manabe M, Ezure K (1987) Inhibition of inspiratory neurons by decrementing expiratory neurons around the Bötzinger complex. J Physiol Soc Jpn 49: 537Google Scholar
  24. Manabe M, Ezure K (1988) Decrementing expiratory neurons of the Bötzinger complex. I. Response to lung inflation and axonal projection. Exp Brain Res 72: 150–158CrossRefPubMedGoogle Scholar
  25. Merrill EG (1974) Finding a respiratory function for the medullary respiratory neurons. In: Bellairs R, Gray EG (eds) Essays on the nervous system. Clarendon Press, Oxford, pp 451–486Google Scholar
  26. Merrill EG, Fedorko L (1984) Monosynaptic inhibition of phrenic motoneurons: a long descending projection from Bötzinger neurons. J Neurosci 4: 2350–2353PubMedGoogle Scholar
  27. Merrill EG, Lipski J, Kubin L, Fedorko L (1983) Origin of the expiratory inhibition of nucleus tractus solitarius inspiratory neurones. Brain Res 263: 43–50CrossRefPubMedGoogle Scholar
  28. Nesland R, Plum F (1965) Subtypes of medullary respiratory neurons. Exp Neurol 12: 337–348CrossRefGoogle Scholar
  29. Otake K, Sasaki H, Mannen H, Ezure K (1987a) Morphology of expiratory neurons of the Bötzinger complex: an HRP study in the cat. J Comp Neurol 258: 565–579CrossRefPubMedGoogle Scholar
  30. Otake K, Sasaki H, Mannen H, Ezure K, Manabe M (1987b) Morphological characteristics of augmenting expiratory neurons of the Bötzinger complex. Neurosci Res Suppl 5: S20CrossRefGoogle Scholar
  31. Rapoport S, Susswein A, Uchino Y, Wilson VJ (1977) Synaptic actions of individual vestibular neurones on cat neck motoneurones. J Physiol (Lond) 272: 367–382Google Scholar
  32. Remmers JE, Richter DW, Ballantyne D, Bainton CR, Klein JP (1986) Reflex prolongation of stage I of expiration. Pflügers Arch 407: 190–198CrossRefPubMedGoogle Scholar
  33. Richter DW (1982) Generation and maintenance of the respiratory rhythm. J Exp Biol 100: 93–107PubMedGoogle Scholar
  34. Richter DW, Camerer H, Meesmann M, Röhrig N (1979) Studies on the synaptic interconnection between bulbar respiratory neurones of cats. Pflügers Arch 380: 245–257CrossRefPubMedGoogle Scholar
  35. Segers LS, Shannon R, Saporta S, Lindsey BG (1987) Functional associations among simultaneously monitored lateral medullary respiratory neurons in the cat. I. Evidence for excitatory and inhibitory action of inspiratory neurons. J Neurophysiol 57: 1078–1100PubMedGoogle Scholar
  36. Sica AL, Cohen MI, Donnelly DF, Zhang H (1985) Responses of recurrent laryngeal motoneurons to changes of pulmonary afferent inputs. Respir Physiol 62: 153–168CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • K. Ezure
    • 1
  • M. Manabe
    • 1
  1. 1.Department of NeurobiologyTokyo Metropolitan Institute for NeurosciencesTokyoJapan

Personalised recommendations