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An electrophysiological investigation of propriospinal inspiratory neurons in the upper cervical cord of the cat

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Summary

This study was performed in order to describe the location, axonal projection and possible synaptic action of the inspiratory neurons recently described in the upper cervical cord. In 26 cats anaesthetized with Nembutal, extracellular recordings were made from 224 cervical inspiratory units which were found near the lateral border of lamina VII and formed a column extending from the caudal end of the nucleus retroambigualis at the C1 segment to the rostral half of the C3 segment. Most of the units (approximately 85%) could be excited antidromically from the thoracic cord. Antidromic mapping showed collateral branches to the C5 segment in the vicinity of the phrenic nucleus, occasionally crossing the midline. No synaptic connections with phrenic motoneurones could be revealed either by cross-correlation of the activity of the cervical units with the discharge of C5 phrenic root, or by spike-triggered averaging (STA) of the post-synaptic noise recorded intracellularly from phrenic motoneurons. Extensive branching was found in the examined T3–T5 segments with arborizations near the ipsilateral intercostal motor nuclei and often extending across the midline. Cross-correlation experiments did not show clear monosynaptic connections to the inspiratory intercostal motoneurons. Intracellular recording from intercostal motoneurons and STA resulted in a few (2 out of 37) small, probably disynaptic, e.p.s.p.s. It is concluded that the upper cervical neurons are involved in the control of phrenic and intercostal motoneurons, probably through a disynaptic pathway involving segmental interneurons.

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References

  • Aminoff MJ, Sears TA (1971) Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones. J Physiol (London) 215: 557–575

    Google Scholar 

  • Aoki M (1982) Respiratory-related neuron activities in the cervical cord of the cat. In: Feldman JL, Berger AJ (eds.) Proceedings International Symposium. Central neural production of periodic respiratory movements. Lake Bluff, Illinois, pp 155–156

  • Aoki M, Kasaba T, Kurosawa Y (1983) Properties of respiratory neurons in the upper cervical cord of the cat. Neurosci Lett Suppl 13: S9

    Google Scholar 

  • 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 177, S49

  • Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: Handbook of physiology, nervous system II, Part 1. American Physiological Society, Bethesda, MD, pp 509–595

    Google Scholar 

  • Baumgarten R von, Schmiedt H, Dodich N (1963) Microelectrode studies of phrenic motoneurons. Ann N Y Acad Sci 109: 536–544

    Google Scholar 

  • Cameron WE, Averill DB, Berger AJ (1983) Morphology of cat phrenic motoneurons as revealed by intracellular injection of horseradish peroxidase. J Comp Neurol 219: 70–80

    Google Scholar 

  • 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: 319–324

    Google Scholar 

  • Dick TE, Berger AJ (1985) Axonal projections of single bulbospinal inspiratory neurons revealed by spike-triggered averaging and antidromic activation. J Neurophysiol 53: 1590–1603

    Google Scholar 

  • Duffin J, Lipski J (1986) Stabilization of intracellular recordings in the cat spinal cord using high frequency ventilation. Can J Physiol (in press)

  • Duron B, Le Bars P (1985) 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 209–215

    Google Scholar 

  • Fedorko L, Merrill EG, Lipski J (1983) Two descending medullary inspiratory pathways to phrenic motoneurons. Neurosci Lett 43: 285–291

    Google Scholar 

  • Feldman JL (1985) Neurophysiology of breathing in mammals. In: Handbook of Physiology. The Nervous System, V.B. Mountcastle (ed.) Section I, vol IV. American Physiological Society, Bethesda MD (in press)

    CAS  PubMed  Google Scholar 

  • Feldman JL, Loewy AD, Speck DF (1985) Projections from the ventral respiratory group to phrenic and intercostal motoneurons in the cat: an autoradiographic study. J Neurosci (in press)

  • Feldman JL, McCrimon DR, Speck DF (1984) Effects of synchronous activation of medullary inspiratory bulbo-spinal neurones on phrenic nerve discharge in the cat. J Physiol 347: 241–254

    Google Scholar 

  • Graham K, Duffin J (1982) Cross-correlation of medullary dorsomedial inspiratory neurons in the cat. Exp Neurol 75: 627–643

    Google Scholar 

  • Haber 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: 350–355

    Google Scholar 

  • Hilaire G, Monteau R (1976) Connexions entre les neurones inspiratoires bulbaires et les motoneurones phréniques et intercostaux. J Physiol (Paris) 72: 987–1000

    Google Scholar 

  • Illert M, Lundberg A, Padel Y, Tanaka R (1978) Integration in descending motor pathways controlling the forelimb in the cat. 5. Properties of and monosynaptic excitatory convergence on C3–C4 propriospinal neurons. Exp Brain Res 33: 101–130

    Google Scholar 

  • Jankowska E, Roberts WJ (1972a) An electrophysiological demonstration of the axonal projections of single spinal interneurons in the cat. J Physiol (London) 222: 597–622

    Google Scholar 

  • Jankowska E, Roberts WJ (1972b) Synaptic actions of single interneurons mediating reciprocal Ia inhibition of motoneurons. J Physiol (London) 222: 623–642

    Google Scholar 

  • Kirkwood PA, Sears TA (1973) Monosynaptic excitation of thoracic expiratory motoneurones from lateral respiratory neurones in the medulla of the cat. J Physiol (London) 234: 87–89

    Google Scholar 

  • Larnicol N, Rose D, Marlot D, Duron B (1982) Anatomical organization of cat intercostal motor nuclei as demonstrated by HRP retrograde labelling. J Physiol (Paris) 78: 198–206

    Google Scholar 

  • Lipski J (1981) Antidromic activation of neurones as an analytic tool in the study of the central nervous system. J Neurosci Meth 4: 1–32

    Google Scholar 

  • Lipski J, Fyffe REW, Jodkowski J (1985) Recurrent inhibition of cat phrenic motoneurons. J Neurosci 5: 1545–1555

    Google Scholar 

  • Lipski J, Kubin L, Jodkowski J (1983) Synaptic action of Rβ neurons on phrenic motoneurons studied with spike-triggered averaging. Brain Res 288: 105–118

    Google Scholar 

  • Lipski J, Merrill EG (1983) Inputs to intercostal motoneurones from ventrolateral medullary respiratory neurons in nembutal-anaesthetized cat. J Physiol 339: 25–26

    Google Scholar 

  • Lipski J, Trzebski A, Kubin L (1979) Excitability changes of dorsal inspiratory neurons during lung inflations as studied by measurement of antidromic invasion latencies. Brain Res 161: 25–38

    Google Scholar 

  • Long SE, Duffin J (1984a) The medullary respiratory neurons: a review. Can J Physiol 62: 161–182

    Google Scholar 

  • Long SE, Duffin J (1984b) Cross-correlation of ventrolateral inspiratory neurons in the cat. Exp Neurol 83: 233–253

    Google Scholar 

  • 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, Tokyo New York, pp 47–64

    Google Scholar 

  • Mendell LL, Henneman E (1971) Terminals of single Ia fibres: location, density and distribution within a pool of 300 homonymous motoneurons. J Neurophysiol 34: 171–187

    Google Scholar 

  • Merrill EG (1970) The lateral respiratory neurones of the medulla: their association with nucleus ambiguus, nucleus retroambigualis, the spinal accessory nucleus and the spinal cord. Brain Res 24: 11–28

    Google Scholar 

  • Merrill EG (1974a) Preliminary studies on nucleus retroambigualis-nucleus of the solitary tract interactions in cats. J Physiol (London) 244: 54–55

    Google Scholar 

  • Merrill EG (1974b) Finding a respiratory function for the medullary respiratory neurones. In: Bellairs R, Gray EG (eds.) Essays on the Nervous System. Oxford, Clarendon, pp 451–486

    Google Scholar 

  • Merrill EG, Lipski J, Kubin L, Fedorko L (1983) Origin of the expiratory inhibition of nucleus tractus solitarius inspiratory neurones. Brain Res 263: 43–50

    Google Scholar 

  • Monteau R, Khatib M, Hilaire G (1985) Central determination of recruitment order: intracellular study of phrenic motoneurons. Neurosci Lett 56: 341–346

    Google Scholar 

  • Munson JB, Sypert GW (1979) Properties of single central Ia afferent fibres projecting to motoneurons. J Physiol (London) 296: 315–327

    Google Scholar 

  • Nelson JR (1959) Single unit activity in medullary respiratory centers of cat. J Neurophysiol 22: 590–598

    Google Scholar 

  • Peterson BW, Mauntz RA, Pitts NG, Mackel RG (1975) Patterns of projection and branching of reticulospinal neurons. Exp Brain Res 23: 333–351

    Google Scholar 

  • Rexed B (1954) A cytoarchitectonic atlas of the spinal cord in the cat. J Comp Neurol 100: 297–379

    Google Scholar 

  • Rikard-Bell G, Bystrzycka EK (1980) Localization of phrenic motor nucleus in the cat and rabbit studied with horseradish peroxidase. Brain Res 194: 479–483

    Google Scholar 

  • Rikard-Bell G, Bystrzycka EK, Nail BS (1985) The identification of brainstem neurones projecting to thoracic respiratory motoneurones in the cat as demonstrated by retrograde transport of HRP. Brain Res Bull 14: 25–37

    Google Scholar 

  • Rose PK, Richmond FJR (1981) White-matter dendrites in the upper cervical spinal cord of the adult cat: a light and electron microscopic study. J Comp Neurol 199: 191–203

    CAS  PubMed  Google Scholar 

  • Satomi H, Takahaski K, Aoki M, Kasaba T, Kurosawa Y, Otsuka K (1985) Localization of the spinal accessory motoneurons in the cervical cord in connection with the phrenic nucleus: an HRP study in cats. Brain Res (in press)

  • Sears TA (1966) The respiratory motoneurone: integration at spinal segmental level. In: Howell JBL, Campbell EJM (eds) Breathlessness. Oxford, pp 33–47

  • Sears TA, Kirkwood PA, Davies JGMcF (1985) Cross-correlation analysis of the connections between bulbospinal neurones and respiratory motoneurones. In: Bianchi AL, Denavit-Saubie M (eds.) Neurogenesis of central respiratory rhythm. MTP Press Ltd, Cambridge MA London, pp 216–222

    Google Scholar 

  • Sears TA, Stagg D (1976) Short-term synchronization of intercostal motoneurone activity. J Physiol (London) 263: 357–387

    Google Scholar 

  • Shinoda Y, Arnold AP, Asanuma H (1976) Spinal branching of corticospinal axons in the cat. Exp Brain Res 26: 215–234

    Google Scholar 

  • Shinoda Y, Ghez C, Arnold A (1977) Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30: 203–218

    Google Scholar 

  • Taylor A, Watt DGD, Stauffer EK, Reinking RM, Stuart DG (1976) Use of afferent triggered averaging to study the central connections of muscle spindle afferents. In: Homma S (ed.) Understanding the stretch reflex: Progress in brain research, Vol 44. Elsevier, Amsterdam, pp 171–183

    Google Scholar 

  • Viala D, Freton E (1983) Evidence for respiratory and locomotor pattern generators in the rabbit cervico-thoracic cord and for their interactions. Exp Brain Res 49: 247–256

    Google Scholar 

  • Webber CHL Jr, Wurster RD, Chung YJ (1979) Cat phrenic nucleus architecture as revealed by horseradish peroxidase mapping. Exp Brain Res 35: 395–406

    Google Scholar 

  • Winkler C, Potter A (1914) An anatomical guide to experimental researches on the cat's brain. Versluys, Amsterdam

    Google Scholar 

Download references

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Lipski, J., Duffin, J. An electrophysiological investigation of propriospinal inspiratory neurons in the upper cervical cord of the cat. Exp Brain Res 61, 625–637 (1986). https://doi.org/10.1007/BF00237589

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  • DOI: https://doi.org/10.1007/BF00237589

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