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Influence of the Noradrenergic Coeruleospinal System on Recurrent Inhibition in the Spinal Cord and its Role During Postural Reflexes

  • O. Pompeiano

Abstract

Renshaw (R)-cells and recurrent inhibition of α-motoneurons can be influenced in the cat by a variety of excitatory and inhibitory inputs arising from supraspinal structures, such as the cerebral cortex (MacLean and Leffman 1967), the internal capsule (Koehler et al. 1978), the thalamus (MacLean and Leffman 1967), the red nucleus (Henatsch et al. 1986), the reticular formation (Koizumi et al. 1959; Haase and Van der Meulen 1961; MacLean and Leffman 1967; Haase and Vogel 1971) and the cerebellum (Granit et al. 1960; Haase and Van der Meulen 1961; see for ref. Pompeiano 1984). These excitatory or inhibitory volleys are of physiological importance, as they serve to increase or decrease the functional coupling between R-cells and their input motoneurons, thus modifying the input-output relation of α-motoneurons to a given excitatory input (Hultborn et al. 1979).

Keywords

Locus Coeruleus Locus Coeruleus Neuron Recurrent Inhibition Response Gain Renshaw Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aghajanian GK, Cedarbaum JM, Wang RY (1977) Evidence for norepinephrine-mediated collateral inhibition of locus coeruleus neurons. Brain Res 136: 570–577PubMedCrossRefGoogle Scholar
  2. Aston-Jones G, Ennis M, Pieribone VA, Nickell WT, Shipley MT (1986) The brain nucleus locus coeruleus: restricted afferent control of a broad efferent network. Science 234: 734–737PubMedCrossRefGoogle Scholar
  3. Barnes CD, D’Ascanio P, Manzoni D, Pompeiano O, Stampacchia G (1985) Responses of locus coeruleus neurons to sinusoidal stimulation of vestibular receptors. Atti Soc Ital Biol, Soc Ital Fisiol, Soc Ital Nutr Um, Pisa, Abstr n 164Google Scholar
  4. Belcher G, Ryall RW (1977) Substance P and Renshaw cells: a new concept of inhibitory synaptic interactions. J Physiol (Lond) 272: 105–119Google Scholar
  5. Bergmans J, Burkes R, Lundberg A (1969) Inhibition of transmission in the recurrent inhibitory pathway to motoneurones. Brain Res 13: 600–602PubMedCrossRefGoogle Scholar
  6. Biscoe TJ, Curtis DR (1966) Noradrenaline and inhibition of Renshaw cells. Science 151: 1230–1231PubMedCrossRefGoogle Scholar
  7. Boyle R, Pompeiano O (1980) Reciprocal responses to sinusoidal tilt of neurons in Deiters’ nucleus and their dynamic characteristics. Arch Ital Biol 118: 1–32PubMedGoogle Scholar
  8. Boyle R, Pompeiano O (1984) Discharge activity of spindle afferents from the gastrocnemiussoleus muscle during head rotation in the decerebrate cat. Pflügers Arch 400: 140–150PubMedCrossRefGoogle Scholar
  9. Cedarbaum JM, Aghajanian GK (1976) Noradrenergic neurons of the locus coeruleus: inhibition by epinephrine and activation by the alpha-antagonist piperoxane. Brain Res 112: 413–419PubMedCrossRefGoogle Scholar
  10. Cedarbaum JM, Aghajanian GK (1978 a) Activation of locus coeruleus neurons by peripheral stimuli: modulation by a collateral inhibitory mechanism. Life Sci 23: 1383–1392Google Scholar
  11. Cedarbaum JM, Aghajanian GK (1978 b) Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique. J Comp Neurol 178: 1–16Google Scholar
  12. Chan JYH, Fung SJ, Chan SHH, Barnes CD (1986) Facilitation of lumbar monosynaptic reflexes by locus coeruleus in the rat. Brain Res 369: 103–109PubMedCrossRefGoogle Scholar
  13. Chu NS, Bloom FE (1974) Activity patterns of catecholamine-containing pontine neurons in the dorsolateral tegmentum of unrestrained cats. J Neurobiol 5: 527–544PubMedCrossRefGoogle Scholar
  14. d’Ascanio P, Bettini E, Pompeiano O (1985) Tonic inhibitory influences of locus coeruleus on the response gain of limb extensors to sinusoidal labyrinth and neck stimulations. Arch Ital Biol 123: 69–100PubMedGoogle Scholar
  15. d’Ascanio P, Pompeiano O, Stampacchia G (1988) Noradrenergic and cholinergic mechanisms responsible for the gain regulation of vestibulospinal reflexes. In: Pompeiano O, Allum JHJ (eds) Vestibulospinal control of posture and locomotion. Elsevier, Amsterdam, pp 361–374 (Progress in Brain Research, vol 76 )CrossRefGoogle Scholar
  16. Eccles JC, Fatt P, Koketsu K (1954) Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol (Lond) 126: 524–562Google Scholar
  17. Engberg I, Ryall RW (1966) The inhibitory action of noradrenaline and other monoamines on spinal neurones. J Physiol (Lond) 185: 298–322Google Scholar
  18. Ennis M, Aston-Jones G (1986) A potent excitatory input to the nucleus locus coeruleus from the ventrolateral medulla. Neurosci Lett 71: 299–305PubMedCrossRefGoogle Scholar
  19. Foote SL, Bloom FE, Aston-Jones G (1983) Nucleus locus coeruleus: new evidence of anatomical and physiological specificity. Physiol Rev 63: 844–914PubMedGoogle Scholar
  20. Fung SJ, Barnes CD (1981) Evidence of facilitatory coerulospinal action in lumbar motoneurons of cats. Brain Res 216: 299–311PubMedCrossRefGoogle Scholar
  21. Fung SJ, Barnes CD (1984) Locus coeruleus control of spinal cord activity. In: Barnes CD (ed) Brainstem control of spinal cord function. Academic Press, London, pp 215–255 (Research Topics in Physiology, vol 6 )Google Scholar
  22. Fung SJ, Barnes CD (1986) Increased efficacy of antidromic and orthodromic activation of cat alpha motoneurons upon arrival of coerulospinal volleys. Arch Ital Biol 124: 229–243PubMedGoogle Scholar
  23. Fung SJ, Barnes CD (1987) Membrane excitability changes in hindlimb motoneurons induced by stimulation of the locus coeruleus in cats. Brain Res 402: 230–242PubMedCrossRefGoogle Scholar
  24. Fung SJ, Pompeiano O, Barnes CD (1987) Suppression of the recurrent inhibitory pathway in lumbar cord segments during locus coeruleus stimulation in cats. Brain Res 402: 351–354PubMedCrossRefGoogle Scholar
  25. Fung SJ, Pompeiano O, Barnes CD (1988) Coeruleospinal influence on recurrent inhibition of spinal motonuclei innervating antagonistic hindleg muscles. Pflügers Arch (in press)Google Scholar
  26. Granit R, Haase J, Rutledge LT (1960) Recurrent inhibition in relation to frequency of firing and limitation of discharge rate of extensor motoneurones. J Physiol (Lond) 154: 308–328Google Scholar
  27. Haase J, Meulen JD van der (1961) Effects of supraspinal stimulation on Renshaw cells belonging to extensor motoneurones. J Neurophysiol 24: 510–520PubMedGoogle Scholar
  28. Haase J, Vogel B (1971) Direkte und indirekte Wirkungen supraspinaler Reizungen auf Renshaw-Zellen. Pflügers Arch 325: 334–346PubMedCrossRefGoogle Scholar
  29. Henatsch H-D, Meyer-Lohmann J, Windhorst U, Schmidt J (1986) Differential effects of stimulation of the cat’s red nucleus on lumbar alpha motoneurones and their Renshaw cells. Exp Brain Res 62: 161–174PubMedCrossRefGoogle Scholar
  30. Hobson J A, Steriade M (1986) Neuronal basis of behavioral state control. In: Bloom FE (ed) Intrinsic regulatory systems of the brain. American Physiological Society, Bethesda, Maryland, pp 701–823 (Handbook of physiology, section 1, The nervous system, vol IV )Google Scholar
  31. Hultborn H, Lindstrom S, Wigstrom H (1979) On the function of recurrent inhibition in the spinal cord. Exp Brain Res 37: 399–403PubMedCrossRefGoogle Scholar
  32. Jones BE, Friedman L (1983) Atlas of catecholamine perikarya, varicosities and pathways in the brainstem of the cat. J Comp Neurol 215: 382–396PubMedCrossRefGoogle Scholar
  33. Koehler W, Windhorst U, Schmidt J, Meyer-Lohmann J, Henatsch H-D (1978) Diverging influences on Renshaw cell responses and monosynaptic reflexes from stimulation of capsula interna. Neurosci Lett 8: 35–39PubMedCrossRefGoogle Scholar
  34. Koizumi K, Ushiyama J, Brooks C McC (1959) A study of reticular formation action on spinal interneurons and motoneurons. Jpn J Physiol 9: 282–303Google Scholar
  35. Krnjevic K, Lekic D (1977) Substance P selectively blocks excitation of Renshaw cell by acetylcholine. Can J Physiol Pharmacol 55: 958–961PubMedCrossRefGoogle Scholar
  36. Leger L, Hernandez-Nicaise M-L (1980) The cat locus coeruleus: light and electron microscopic study of the neural somata. Anat Embryol 159: 181–198PubMedCrossRefGoogle Scholar
  37. MacLean JB, Leffman H (1967) Supraspinal control of Renshaw cells. Exp Neurol 18: 94–104PubMedCrossRefGoogle Scholar
  38. Manzoni D, Pompeiano O, Srivastava UC, Stampacchia G (1983 a) Responses of forelimb ex-tensors to sinusoidal stimulation of macular labyrinth and neck receptors. Arch Ital Biol 121: 205–214Google Scholar
  39. Manzoni D, Pompeiano O, Stampacchia G, Srivastava UC (1983 b) Responses of medullary reticulospinal neurons to sinusoidal stimulation of labyrinth receptors in decerebrate cat. J Neurophysiol 50: 1059–1079Google Scholar
  40. Manzoni D, Pompeiano O, Srivastava UC, Stampacchia G (1984) Gain regulation of vestibular reflexes in fore- and hindlimb muscles evoked by roll tilt. Bull Soc Ital Biol Sper 60, Suppl 3: 9–10Google Scholar
  41. Marchand AR, Manzoni D, Pompeiano O, Stampacchia G (1987) Effects of stimulation of vestibular and neck receptors on Deiters neurons projecting to the lumbosacral cord. Pflügers Arch 409: 13–23PubMedCrossRefGoogle Scholar
  42. Miachon S, Berod A, Leger L, Chat M, Hartman B, Pujol JF (1984) Identification of catechol-amine cell bodies in the pons and pons-mesencephalon junction of the cat brain, using tyrosine hydroxylase and dopamines-hydroxylase immunohistochemistry. Brain Res 305: 369–374PubMedCrossRefGoogle Scholar
  43. Mizukawa K (1980) The segmental detailed topographical distribution of monoaminergic terminals and their pathways in the spinal cord of the cat. Anat Anz 147: 125–144PubMedGoogle Scholar
  44. Pompeiano O (1967) The neurophysiological mechanisms of the postural and motor events during desynchronized sleep. Proc Assoc Res Nerv Ment Dis 45: 351–423Google Scholar
  45. Pompeiano O (1975) Vestibulo-spinal relationships. In: Naunton RF (ed) The vestibular system. Academic Press, London, pp 147–180Google Scholar
  46. Pompeiano (1984) Recurrent inhibition. In: Davidoff RA (ed) Handbook of the spinal cord, vol 2 and 3. Dekker, New York, pp 461–557Google Scholar
  47. Pompeiano O, Hoshino K (1976 a) Tonic inhibition of dorsal pontine neurons during the postural atonia produced by an anticholinesterase in the decerebrate cat. Arch Ital Biol 114: 310–340Google Scholar
  48. Pompeiano O, Hoshino K (1976 b) Central control of posture: reciprocal discharge by two pontine neuronal groups leading to suppression of decerebrate rigidity. Brain Res 116: 131–138Google Scholar
  49. Pompeiano O, Wand P, Sontag K-H (1975) Response of Renshaw cells to sinusoidal stretch of hindlimb extensor muscles. Arch Ital Biol 113: 205–237PubMedGoogle Scholar
  50. Pompeiano O, Wand P, Srivastava UC (1985 a) Responses of Renshaw cells coupled with hindlimb extensor motoneurons to sinusoidal stimulation of labyrinth receptors in the decerebrate cat. Pflügers Arch 403: 245–257CrossRefGoogle Scholar
  51. Pompeiano O, Wand P, Srivastava UC (1985 b) Influence of Renshaw cells on the gain of hindlimb extensor muscles to sinusoidal labyrinth stimulation. Pflügers Arch 404: 107–118CrossRefGoogle Scholar
  52. Pompeiano O, d’Ascanio P, Horn E, Stamacchia G (1987 a) Effects of local injection of the α2-adrenergic agonist clonidine into the locus complex on the gain of vestibulospinal and cervicospinal reflexes in decerebrate cats. Arch Ital Biol 125: 225–269Google Scholar
  53. Pompeiano O, Stampacchia G, Horn E, d’Ascanio P (1987 b) The role of the locus coeruleus in the gain regulation of vestibulospinal reflexes. Acta Otolaryngol (Stockh) 103: 404–409Google Scholar
  54. Pompeiano O, Manzoni D, Barnes CD, Stampacchia G, d’Ascanio P (1988) Labyrinthine influences on locus coeruleus neurons. Acta Otolaryngol (Stockh) 105: 576–581CrossRefGoogle Scholar
  55. Reddy VK, Fung SJ, Bowker RM, Barnes CD (1987) Quantitative composition of tyrosine hydroxylase ( TH)-like immunoreactive nurons of the dorsolateral pons projecting to cervical and lumbar enlargements in the cat. Anat Rec 218: 111ACrossRefGoogle Scholar
  56. Renshaw B (1941) Influence of discharge of motoneurons upon excitation of neighboring motoneurons. J Neurophysiol 4: 167–183Google Scholar
  57. Ross H-G, Cleveland S, Haase J (1972) Quantitative relation of Renshaw cell discharges to monosynaptic reflex height. Pflügers Arch 332: 73–79PubMedCrossRefGoogle Scholar
  58. Ryall RW, Belcher G (1977) Stubstance P selectively blocks nicotinic receptors on Renshaw cells: a possible synaptic inhibitory mechanism. Brain Res 137: 376–380PubMedCrossRefGoogle Scholar
  59. Sakai K, Sastre JP, Salvert D, Touret M, Tohyama M, Jouvet M (1979) Tegmentoreticular projections with special reference to the muscular atonia during paradoxical sleep in the cat: an HRP study. Brain Res 176: 233–254PubMedCrossRefGoogle Scholar
  60. Schor RH, Miller AD (1981) Vestibular reflexes in neck and forelimb muscles evoked by roll tilt. J Neurophysiol 46: 167–178PubMedGoogle Scholar
  61. Watabe K, Satoh T (1979) Mechanism underlying prolonged inhibition of rat locus coeruleus neurons following anti- and orthodromic activation. Brain Res 165: 343–347PubMedCrossRefGoogle Scholar
  62. Watabe K, Nakai K, Kasamatsu T (1982) Visual afferents to norepinephrine-containing neurons in cat locus coeruleus. Exp Brain Res 48: 66–80PubMedCrossRefGoogle Scholar
  63. Weight FF, Salmoiraghi GC (1966) Adrenergic responses of Renshaw cells. J Pharmacol Exp Ther 154: s391–397Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1988

Authors and Affiliations

  • O. Pompeiano
    • 1
  1. 1.Dipartimento di Fisiologia e BiochimicaUniversita’ di PisaPisaItaly

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