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Experimental Brain Research

, Volume 95, Issue 3, pp 477–487 | Cite as

Upper cervical inspiratory neurons in the rat: an electrophysiological and morphological study

  • J. Lipski
  • J. Duffin
  • B. Kruszewska
  • X. Zhang
Article

Abstract

Upper cervical inspiratory neurons form a distinct neuronal column located near the lateral edge of the intermediate grey matter in the rostral spinal segments. Previous studies conducted in cats have demonstrated synaptic inputs to these neurons from several respiratory related regions of the medulla, and long descending axonal projections mainly towards the motoneurons supplying the intercostal muscles. The aim of this study was to examine the electrophysiological and morphological properties of this propriospinal system in the rat. Extracellular recordings were made from 127 cervical inspiratory units, mainly in the C1 and C2 segments. Eighty-two percent could be antidromically activated from the C7/C8 border. No evidence of monosynaptic connection was obtained by cross-correlating the activity of some of these units with the discharge of the phrenic nerve. Intracellular recordings were made from seven neurons, three of which were labelled with biotinamide (neurobiotin). Long “survival times” after intracellular injections (up to 23 h) resulted in staining of axons for long distances, at least to the C5 segment. Each of the three labelled axons issued only one short collateral which arborized in the region of the phrenic nucleus. These results demonstrate that upper cervical inspiratory neurons in the rat have features similar to those previously described in the cat, including only a limited projection to the phrenic nucleus. In addition, this study provides the first morphological identification of these neurons.

Key words

Electrophysiology Medulla oblongata Spinal cord Interneurons Respiratory control Intracellular labelling Rat 

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References

  1. Aoki M, Mori S, Kawahara K, Watanabe H, Ebata N (1980) Generation of spontaneous respiratory rhythm in high spinal cats. Brain Res 202:51–63Google 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, Ohtsuka K, Satomi H (1984) The projection of cervical respiratory neurons to the phrenic nucleus in the cat. Neurosci Lett Suppl 17:S49Google 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. Liss, New York, pp 73–82Google Scholar
  5. Aoki M, Kosaka I, Fujito Y, Kobayashi N (1988) Distribution pattern of the cervical respiratory neurons in the cat, rat and monkey. Neurosci Res [Suppl] 7: S89Google Scholar
  6. Bellingham MC, Lipski J (1990) Respiratory interneurons in the C5 segment of the spinal cord of the cat. Brain Res 533:141–146Google Scholar
  7. Bryant TH, Yoshida S, DeCastro D, Lipski J (1993) Expiratory neurons of the Bötzinger complex in the rat: a morphological study following intracellular labelling with biocytin.J Comp Neurol (in press)Google Scholar
  8. Cameron WE, Averill DB, Berger AJ (1983) Morphology of cat phrenic motoneurons as revealed by intracellular injection of horseradish peroxidase. J Comp Neurol 219:70–80Google Scholar
  9. Cohen MI, Piercey MF, Gootman PM, Wolotsky P (1974) Synaptic connections between medullary inspiratory neurons and phrenic motoneurons as revealed by cross-correlation. Brain Res 81:319–324Google Scholar
  10. Dawkins MA, Foreman RD, Farber JP (1992) Short latency excitation of upper cervical respiratory neurons by vagal stimulation in the rat. Brain Res 594:319–322Google Scholar
  11. Dick TE, Berger AJ (1985) Axonal projections of single bulbospinal inspiratory neurons revealed by spike-triggered averaging and antidromic activation. J Neurophysiol 53:1590–1603Google Scholar
  12. Douse MA, Duffin J (1993) Axonal projections and synaptic connexions of C5 segment expiratory neurons in the cat. J Physiol (Lond) (in press)Google Scholar
  13. Douse MA, Duffin J, Brooks D, Fedorko L (1992) Role of upper cervical inspiratory neurons studied by cross-correlation in the cat. Exp Brain Res 90:153–162Google Scholar
  14. Duffin J, Hoskin RW (1987) Intracellular recordings from upper cervical inspiratory neurons in the cat. Brain Res 435:351–354Google Scholar
  15. Duffin J, Lipski J (1987) Monosynaptic excitation of thoracic motoneurons by inspiratory neurons of the nucleus tractus solitarius in the cat. J Physiol (London) 390:415–431Google Scholar
  16. Ezure K, Manabe M, Yamada H (1988) Distribution of medullary respiratory neurons in the rat. Brain Res 455:262–270Google Scholar
  17. Furicchia JV, Goshgarian HG (1987) Dendritic organization of phrenic motoneurons in the adult rat. Exp Neurol 96:621–634Google Scholar
  18. Goshgarian HG, Rafols JA (1981) The phrenic nucleus of the albino rat: a correlative HRP and Golgi study. J Comp Neurol 201:441–456Google Scholar
  19. Hilaire G, Monteau R, Gauthier P, Rega P, Morin D (1990) Functional significance of the dorsal respiratory group in adult and newborn rats: in vivo and in vitro studies. Neurosci Lett 111:133–138Google 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. Keswani NH, Groat RA, Hollinshead W (1954) Localization of the phrenic nucleus in the spinal cord of the cat. J Anat Soc India 3:82–89Google Scholar
  24. Kirkwood PA, Munson JB, Sears TA, Westgaard RH (1988) Respiratory interneurons in the thoracic spinal cord of the cat. J Physiol (Lond) 395:161–192Google Scholar
  25. Kita H, Armstrong W (1991) A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labelling and neuronal tracing studies: comparison with biocytin. J Neurosci Methods 37:141–150Google Scholar
  26. Kubin L, Romaniuk JR (1988) Propriospinal inspiratory neurons in the upper cervical spinal cord of the rabbit; location and efferent spinal projections. In: Karczewski WA, Grieb P, Kulesza J, Bonsignore G (eds) Control of breathing during sleep and anesthesia. Plenum, New York, pp 197–201Google Scholar
  27. Lindsay AD, Greer JJ, Feldman JL (1991) Phrenic motoneuron morphology in the neonatal rat. J Comp Neurol 308:169–179Google Scholar
  28. Lipski J (1981) Antidromic activation of neurones as an analytic tool in the study of the central nervous system. J Neurosci Methods 4:1–32Google Scholar
  29. 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
  30. Lipski J, Fyffe REW, Jodkowski J (1985) Recurrent inhibition of cat phrenic motoneurons. J Neurosci 5:1545–1555Google Scholar
  31. Lipski J, Kubin L, Jodkowski J (1983) Synaptic action of Rβ neurons on phrenic motoneurons studied with spike-triggered averaging. Brain Res 288:105–118Google Scholar
  32. Lipski J, Zhang X, Kruszewska B, Kanjhan R (1993) Tracing long axonal projections of intracellularly-labeled neurons “in vivo”. Proc Aust Neurosci Soc 4:94Google Scholar
  33. Lundberg A (1979) Integration in a propriospinal motor centre controlling the forelimb of the cat. In: Integration in the nervous system. Asanuma H, Wilson VJ (eds) Igaku-Shoin, Tokyo, pp 47–64Google Scholar
  34. Mateika JH, Duffin J (1989) The connections from Bötzinger expiratory neurons to upper cervical inspiratory neurons in the cat. Exp Neurol 104:138–146Google Scholar
  35. Merrill EG, Lipski J (1987) Inputs to intercostal motoneurons from ventrolateral medullary respiratory neurons in the cat. J Neurophysiol 57:1837–1853Google Scholar
  36. Miller AD, Ezure K, Suzuki I (1985) Control of abdominal muscles by brainstem respiratory neurons in the cat. J Neurophysiol 54:155–167Google Scholar
  37. NakazonoY, Aoki M (dy1991) Monosynaptic excitatory connections between propriospinal respiratory neurons and phrenic motoneurons in cat. Third IBRO Congress, Abstracts, p18.10Google Scholar
  38. Nonaka S, Miller AD (1991) Behaviour of upper cervical inspiratory propriospinal neurons during fictive vomiting. J Neurophysiol 65:1492–1500Google Scholar
  39. Pilowsky PM, Jiang C, Lipski J (1990) An intracellular study of respiratory neurons in the rostral ventolateral medulla and their relationship to catecholamine-containing neurons. J Comp Neurol 301:604–617Google Scholar
  40. Pilowsky P, Llewellyn-Smith IJ, Lipski J, Chalmers J (1992) Substance P immunoreactive boutons form synapses with feline sympathetic preganglionic neurons. J Comp Neurol 320:121–135Google Scholar
  41. Saether K, Hilaire G, Monteau R (1987) Dorsal and ventral respiratory groups of neurons in the medulla of the rat. Brian Res 419:87–96Google Scholar
  42. Schwarzacher SW, Wilhelm Z, Anders K, Richter DW (1991) The medullary respiratory network in the rat. J Physiol (Lond) 435:631–644Google Scholar
  43. Waibl H (1973) Zur Topographie der Medulla spinalis der Albinoratte (Rattus norvegicus). Adv Anat Embryol Cell Biol 47:6–42Google Scholar
  44. Webber ChL Jr, Wurster RD, Chung JM (1979) Cat phrenic nucleus architecture as revealed by horseradish peroxidase mapping. Exp Brain Res 35:395–406Google Scholar
  45. Zheng Y, Barillot JC, Bianchi AL (1992) Medullary expiratory neurons in the decerebrate rat: an intracellular study. Brain Res 576:245–253Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • J. Lipski
    • 1
  • J. Duffin
    • 2
  • B. Kruszewska
    • 1
  • X. Zhang
    • 1
  1. 1.Department of PhysiologySchool of Medicine University of AucklandAucklandNew Zealand
  2. 2.Departments of Physiology and AnaesthesiaUniversity of TorontoTorontoCanada

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