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Experimental Brain Research

, Volume 90, Issue 1, pp 153–162 | Cite as

Role of upper cervical inspiratory neurons studied by cross-correlation in the cat

  • M. A. Douse
  • J. Duffin
  • D. Brooks
  • L. Fedorko
Article

Summary

Axonal projections and synaptic connectivity of upper cervical inspiratory neurons (UCINs) were investigated in anaesthetised cats to clarify their role as propriospinal respiratory interneurons. Antidromic mapping showed axonal collaterals near phrenic and intercostal motonuclei. Of the UCINs tested, 37% had collaterals at T3-4; 55% had ipsilateral projections and 45% had contralateral projections. Ipsilateral or contralateral cross-correlations of the activity of pairs of UCINs (one on each side of the spinal cord) with the discharge of internal intercostal, external intercostal (T3-4) or phrenic nerves revealed similar features. Those with the internal intercostal and phrenic nerves were interpreted as evidence for shared or oligosynaptic excitation, those with the external intercostal nerve as shared excitation and inhibition. No evidence for monosynaptic connections was found. Monosynaptic connections could also not be demonstrated between inspiratory intercostal neurons located near (< 0.5 mm) the UCINs collateral arborizations in T3-4, examined by cross-correlation. Afferent feedback from internal intercostal nerves (T3-4) was investigated by cross-correlating nerve stimulation with UCINs activity. Ipsilateral and contralateral cross-correlograms had similar features, providing evidence for excitation in some cases and inhibition in others. Finally, cross-correlations between ipsilateral UCINs and cervical sympathetic nerves were featureless. The results suggest that the role of UCINs as part of a respiratory propriospinal control system analagous to forelimb motor control is untenable, although they may be part of an intercostal afferent feedback loop.

Key words

Respiration Neurons Axonal projections Spinal cord Cat 

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References

  1. Anderson KE, Duffin J (1976) An instrument for cross-correlating neurophysiological data in real time. In: Digest of the 11th International Conference on Medical and Biological Engineering. National Research Council, Ottawa, pp 234–235Google Scholar
  2. Aoki M, Kasaba T, Kurosawa Y (1983) Properties of respiratory neurons in the upper cervical cord of the cat. Neurosci Lett Suppl 13:S59Google Scholar
  3. Aoki M, Kasaba T, Kurosawa Y, Ohutsuka K, Satomi H (1984) The projection of cervical respiratory neurons to the phrenic nucleus in the cat. Neurosci Lett Suppl 17:849Google Scholar
  4. Aoki M, Fujito Y, Kurosawa Y, Kawasaki H, Kosaka I (1987) Descending inputs to the upper cervical inspiratory neurons from the medullary respiratory neurons and the raphe nuclei in the cat. In: Sieck G, Gandevia SC, Cameron WE (eds) Respiratory muscles and their neuromotor control. Alan R Liss, New York, pp 73–82Google Scholar
  5. Bainton CR, Richter DW, Seller H, Ballentyne D, Klein JP (1985) Respiratory modulation of sympathetic activity. J Auto Nerv Syst 12:77–90Google Scholar
  6. Bak MJ, Schmidt EM (1977) An improved time-amplitude window discriminator. IEEE Trans Biomed Eng, BME-24:486–489Google Scholar
  7. Bellingham M (1989) Synaptic inhibition of phrenic motoneurons by intercostal nerve stimulation. Neurosci Lett Suppl 34:S59Google Scholar
  8. Bellingham M, Lipski J (1990) Respiratory interneurones in the C5 segment of the spinal cord of the cat. Brain Res 533:141–146Google Scholar
  9. Bianchi AL, Grelot L (1989) Converse motor output of inspiratory bulbospinal premotor neurons during vomiting. Neurosci Lett 104:298–302Google Scholar
  10. Connelly CA, Wurster RD (1985) Spinal pathways mediating respiratory influences on sympathetic nerves. Am J Physiol 249:R91-R99Google Scholar
  11. Davies JG McF, Kirkwood PA, Sears TA (1985) The detection of monosynaptic connexions from inspiratory bulbospinal neurones to inspiratory motoneurones in the cat. J Physiol 368:33–62Google Scholar
  12. Decima EE, von Euler C (1969) Intercostal and cerebellar influences on afferent phrenic activity in the decerebrate cat. Acta Physiol Scand 76:148–158Google Scholar
  13. Duffin J, Hoskin RW (1987) Intracellular recordings from upper cervical inspiratory neurons in the cat. Brain Res 435:351–354Google Scholar
  14. Duron B, LeBars P (1984) Respiratory motor units in the lateral intercostal muscle nerves. In: Bianchi AL, Denavit-Saubie M (eds) Neurogenesis of central respiratory rhythm. MTP Press Ltd, Cambridge MA London, pp 209–215Google Scholar
  15. Fedorko LM, Merrill EG, Lipski J (1983) Two descending medullary inspiratory pathways to phrenic motoneurons. Neurosci Lett 43:285–291Google Scholar
  16. Fedorko L, Hoskin RW, Duffin J (1989) Projections from inspiratory neurons of the nucleus retroambigualis to phrenic motoneurons in the cat. Exp Neurol 105:306–310Google Scholar
  17. Fetz EE, Gustafsson B (1983) Relation between shapes of postsynaptic potentials and changes in firing probability of cat motoneurons. J Physiol 341:387–410Google Scholar
  18. Graham K, Duffin J (1981) Cross-correlation of medullary expiratory neurons in the cat. Exp Neurol 73:451–464Google Scholar
  19. Hilaire G, Monteau R (1976) Connexions entre les neurones inspiratoire bulbaires et les motoneurones phreniques et intercosteaux. J Physiol (Paris) 72:987–1000Google Scholar
  20. Hoskin RW, Duffin J (1987a) Excitation of upper cervical inspiratory neurons by inspiratory neurons of the nucleus tractus solitarius in the cat. Exp Neurol 95:126–141Google Scholar
  21. Hoskin RW, Duffin J (1987b) Excitation of upper cervical inspiratory neurons by inspiratory neurons of the nucleus retroambigualis in the cat. Exp Neurol 98:404–417Google Scholar
  22. Hoskin RW, Fedorko LM, Duffin J (1988) Projections from upper cervical inspiratory neurons to thoracic and lumbar expiratory motornuclei in the cat. Exp Neurol 99:544–555Google Scholar
  23. Iscoe S, Grelot L, Bianchi AL (1990) Responses of inspiratory neurons of the dorsal respiratory group to stimulation of expiratory muscle and vagal afferents. Brain Res 507:281–288Google Scholar
  24. Jankowska E, Roberts WJ (1972) An electrophysiological demonstration of the axonal projections of single spinal interneurons in the cat. J Physiol 222:597–622Google Scholar
  25. Kirkwood PA (1979) On the use and interpretation of cross-correlation measurements in the mammalian central nervous system. J Neurosci Meth 1:107–132Google Scholar
  26. Kirkwood PA, Munson JB, Sears TA, Westgaard RH (1988) Respiratory interneurones in the thoracic spinal cord of the cat. J Physiol 395:161–192Google Scholar
  27. Lipski J (1981) Antidromic activation of neurones as an analytic tool in the study of the central nervous system. J Neurosci Meth 4:1–32Google Scholar
  28. Lipski J, Duffin J (1986) An electrophysiological investigation of propriospinal inspiratory neurons in the upper cervical cord of the cat. Exp Brain Res 61:625–637Google Scholar
  29. Long SE, Duffin J (1986) The neuronal determinants of respiratory rhythm. Prog Neurobiol 27:101–182Google Scholar
  30. Lundberg A (1979) Integration in a propriospinal motor centre controlling the forelimb of the cat. In: Asanuma H, Wilson VJ (ed) Integration in the nervous system. Jgaku-Shoin, Tokoyo New York, pp 47–64Google Scholar
  31. Mateika JH, Duffin J (1989) The connections from Botzinger expiratory neurons to upper cervical inspiratory neurons in the cat. Exp Neurol 104:138–146Google Scholar
  32. Merrill EG, Lipski J (1987) Inputs to intercostal motoneurons from ventrolateral medullary respiratory neurons in the cat. J Neurophysiol 57:1837–1853Google Scholar
  33. Miller AD, Ezure K, Suzuki I (1985) Control of abdominal muscles by brainstem respiratory neurons in the cat. J Neurophysiol 54:155–167Google Scholar
  34. Miller AD, Nonaka S, Lakos SF, Tan LK (1990) Diaphragmatic and external intercostal muscle control during vomiting: behavior of inspiratory bulbospinal neurons. J Neurophysiol 63:31–36Google Scholar
  35. Nelson JR (1959) Single unit activity in medullary respiratory centers of cat. J Neurophysiol 22:590–598Google Scholar
  36. Nonaka S, Miller AD (1991) Behavior of upper cervical inspiratory propriospinal neurons during fictive vomiting. J Neurophysiol 65:1492–1500Google Scholar
  37. Preiss G, Kirchner F, Polosa C (1975) Patterning of sympathetic preganglionic neuron firing by the central respiratory drive. Brain Res 87:363–374Google Scholar
  38. Shannon R (1980) Intercostal and abdominal muscle afferent influence on medullary dorsal respiratory group neurons. Respir Physiol 39:73–94Google Scholar
  39. Shannon R (1986) Reflexes from respiratory muscles and costovertebral joints. In: Cherniak NS, Widdicombe JG (eds) The respiratory system. Handbook of physiology, Section 3, Vol 2. American Physiological Society, Bethesda MD, pp 431–447Google Scholar
  40. Sears TA, Stagg D (1976) Short term synchronization of intercostal motoneurone activity. J Physiol 263:357–381Google Scholar
  41. 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 actions of inspiratory neurons. J Neurophysiol 57:1078–1100Google Scholar
  42. Wallenstein S, Zucker CL, Fleiss JL (1980) Some statistical methods useful in circulation research. Circ Res 47:1–9Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • M. A. Douse
    • 1
  • J. Duffin
    • 1
  • D. Brooks
    • 1
  • L. Fedorko
    • 2
  1. 1.Departments of Physiology and AnaesthesiaUniversity of TorontoTorontoCanada
  2. 2.Mt. Sinai Hospital Research InstituteTorontoCanada

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