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Synaptic transmission in sympathetic vasoconstrictor pathways and its modification after injuries

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Neurophysiology Aims and scope

Abstract

The discharge of vasoconstrictor pathways arising in the CNS is largely unmodified as it passes through the sympathetic ganglia to the vasculature. The underlying synaptic events have been revealed by intracellular recordings from sympathetic paravertebral ganglion cells in the course of ongoing and reflex activity in anesthetized animals, first made in Skok’s Laboratory in Kyiv (Ukraine). Each preganglionic neuron diverges to contact a number of post-ganglionic neurons, on each of which several pre-ganglionic inputs converge. However, only suprathreshold “strong,” or “dominant” synapses are effective in transmitting the CNS signals. Strong synapses differ from the other subthreshold “weak,” or “accessory” inputs: (a) excitatory synaptic currents are >1 nA in their amplitude, (b) 3 to ≈>30 times more quanta of acetylcholine are released, (c) pre-synaptic Ca2+ entry through channels resistant to all-known antagonists triggers acetylcholine release, and (d) post-synaptic Ca2+ entry boosts and prolongs the nicotinic current. While the majority of postganglionic neurons have only one strong input, a proportion receives two or, rarely, three such inputs. In cells with multiple strong inputs, an equivalent number of discrete Ca2+ currents can be evoked at distinct foci electrically distant from the soma, suggesting that each strong input has a unique dendritic association with a cluster of Ca2+ channels. When strong preganglionic inputs are destroyed, residual weak synapses sprout and rapidly restore the suprathreshold connections. While much remains to be discovered about how strong synapses are established, their high safety factor ensures the wide and secure distribution of vasoconstrictor command signals from the CNS.

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References

  1. J. H. Coote, “Landmarks in understanding the central nervous control of the cardiovascular system,” Exp. Physiol., 92, 3–18 (2007).

    Article  PubMed  Google Scholar 

  2. P. G. Guyenet, “The sympathetic control of blood pressure,” Nat. Rev. Neurosci., 7, 335–346 (2006).

    Article  PubMed  CAS  Google Scholar 

  3. K. Dembowsky, J. Czachurski, and H. Seller, “An intracellular study of the synaptic input to sympathetic preganglionic neurons of the third thoracic segment of the cat,” J. Auton. Nerv. Syst., 13, 201–244 (1985).

    Article  PubMed  CAS  Google Scholar 

  4. E. M. McLachlan and G. D. S. Hirst, “Some properties of preganglionic neurons in the upper thoracic spinal cord of the cat,” J. Neurophysiol., 43, 1251–1265 (1980).

    PubMed  CAS  Google Scholar 

  5. P. Sah and E. M. McLachlan, “Membrane properties and synaptic potentials in rat sympathetic preganglionic neurons studied in horizontal spinal cord slices in vitro,” J. Auton. Nerv. Syst., 53, 1–15 (1995).

    Article  PubMed  CAS  Google Scholar 

  6. W. Jänig, The Integrative Action of the Autonomic Nervous System: Neurobiology of Homeostasis, Cambridge Univ. Press, New York (2006).

    Google Scholar 

  7. R. A. Dampney, M. J. Coleman, M. A. Fontes, et al., “Central mechanisms underlying short-and long-term regulation of the cardiovascular system,” Clin. Exp. Pharmacol. Physiol., 29, 261–268 (2002).

    Article  PubMed  CAS  Google Scholar 

  8. D. W. Wheeler, P. H. Kullmann, and J. P. Horn, “Estimating use-dependent synaptic gain in autonomic ganglia by computational simulation and dynamic-clamp analysis,” J. Neurophysiol., 92, 2659–2671 (2004).

    Article  PubMed  Google Scholar 

  9. J. N. Langley, “The autonomic nervous system,” Brain, 26, 1–26 (1903).

    Article  Google Scholar 

  10. W. Feldberg and J. H. Gaddum, “The chemical transmitter at synapses in a sympathetic ganglion,” J. Physiol., 81, 305–319 (1934).

    PubMed  CAS  Google Scholar 

  11. V. I. Skok, “Channel-blocking mechanism ensures specific blockade of synaptic transmission,” Neuroscience, 17, 1–9 (1986).

    Article  PubMed  CAS  Google Scholar 

  12. V. I. Skok, “Nicotinic acetylcholine receptors in autonomic ganglia,” Auton. Neurosci., 97, 1–11 (2002).

    Article  PubMed  CAS  Google Scholar 

  13. R. J. Evans, V. Derkach, and A. Surprenant, “ATP mediates fast synaptic transmission in mammalian neurons,” Nature, 357, 503–505 (1992).

    Article  PubMed  CAS  Google Scholar 

  14. H. Inokuchi and E. M. McLachlan, “Lack of evidence for P2X-purinoceptor involvement in fast synaptic responses in intact sympathetic ganglia isolated from guinea-pigs,” Neuroscience, 69, 651–659 (1995).

    Article  PubMed  CAS  Google Scholar 

  15. V. I. Skok, Physiology of Autonomic Ganglia, Igaku Shoin, Tokyo (1973).

    Google Scholar 

  16. V. I. Skok and A. I. Ivanov, “What is the ongoing activity of sympathetic neurons?” J. Auton. Nerv. Syst., 7, 263–270 (1983).

    Article  PubMed  CAS  Google Scholar 

  17. A. Ivanov and D. Purves, “Ongoing electrical activity of superior cervical ganglion cells in mammals of different sizes,” J. Comp. Neurol., 284, 398–404 (1989).

    Article  PubMed  CAS  Google Scholar 

  18. E. M. McLachlan, P. J. Davies, H.-J. Häbler, et al., “On-going and reflex synaptic events in rat superior cervical ganglion cells,” J. Physiol., 501, 165–182 (1997).

    Article  PubMed  CAS  Google Scholar 

  19. E. M. McLachlan, H.-J. Häbler, J. Jamieson, et al., “Analysis of the periodicity of synaptic events in neurons in the superior cervical ganglion of anaesthetized rats,” J. Physiol., 511, 461–478 (1998).

    Article  PubMed  CAS  Google Scholar 

  20. V. G. Macefield and B. G. Wallin, “Respiratory and cardiac modulation of single sympathetic vasoconstrictor and sudomotor neurons to human skin,” J. Physiol., 516, 303–314 (1999).

    Article  PubMed  CAS  Google Scholar 

  21. M. E. Holman and G. D. S. Hirst, “Junctional transmission in smooth muscle and the autonomic nervous system,” in: Handbook of Physiology, Sect. 1, The Nervous System, E. R. Kandel, (ed.), Am. Physiol. Society, Bethesda (1977), pp. 417–462.

    Google Scholar 

  22. J. Jamieson, H. D. Boyd, and E. M. McLachlan, “Simulations to derive membrane resistivity in three phenotypes of guinea pig sympathetic neuron,” J. Neurophysiol., 89, 2430–2440 (2003).

    Article  PubMed  Google Scholar 

  23. D. Purves, “Functional and structural changes in mammalian sympathetic neurones following interruption of their axons,” J. Physiol., 252, 429–463 (1975).

    PubMed  CAS  Google Scholar 

  24. A. S. Finkel and S. Redman, “Theory and operation of a single microelectrode voltage clamp,” J. Neurosci. Meth., 11, 101–127 (1984).

    Article  CAS  Google Scholar 

  25. J. G. Blackman and R. D. Purves, “Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig,” J. Physiol., 203, 173–198 (1969).

    PubMed  CAS  Google Scholar 

  26. G. D. S. Hirst and E. M. McLachlan, “Post-natal development of ganglia in the lower lumbar sympathetic chain of the rat,” J. Physiol., 349, 119–134 (1984).

    PubMed  CAS  Google Scholar 

  27. P. Jobling and I. L. Gibbins, “Electrophysiological and morphological diversity of mouse sympathetic neurons,” J. Neurophysiol., 82, 2747–2764 (1999).

    PubMed  CAS  Google Scholar 

  28. D. Purves, E. Rubin, W. D. Snider, et al., “Relation of animal size to convergence, divergence, and neuronal number in peripheral sympathetic pathways,” J. Neurosci., 6, 158–163 (1986).

    PubMed  CAS  Google Scholar 

  29. W. D. Snider, “Rostrocaudal differences in dendritic growth and synaptogenesis in rat sympathetic chain ganglia,” J. Comp. Neurol., 244, 245–253 (1986).

    Article  PubMed  CAS  Google Scholar 

  30. D. Purves and R. I. Hume, “The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells,” J. Neurosci., 1, 441–452 (1981).

    PubMed  CAS  Google Scholar 

  31. I. L. Gibbins, P. Jobling, J. P. Messenger, et al., “Neuronal morphology and the synaptic organisation of sympathetic ganglia,” J. Auton. Nerv. Syst., 81, 104–109 (2000).

    Article  PubMed  CAS  Google Scholar 

  32. E. M. McLachlan, “An analysis of the release of acetylcholine from preganglionic nerve terminals,” J. Physiol., 245, 447–466 (1975).

    CAS  Google Scholar 

  33. E. M. McLachlan, “The statistics of transmitter release at chemical synapses,” in: International Review of Physiology-Neurophysiology III, R. Porter (ed.), Univ. Park Press, Baltimore (1978), pp. 49–117.

    Google Scholar 

  34. D. R. Ireland, P. J. Davies, and E. M. McLachlan, “Calcium channel subtypes differ at two types of cholinergic synapse in lumbar sympathetic neurons of guinea-pigs,” J. Physiol., 514, 59–69 (1999).

    Article  PubMed  CAS  Google Scholar 

  35. P. Jobling, I. L. Gibbins, R. J. Lewis, et al., “Differential expression of calcium channels in sympathetic and parasympathetic preganglionic inputs to neurons in paracervical ganglia of guinea-pigs,” Neuroscience, 127, 455–466 (2004).

    Article  PubMed  CAS  Google Scholar 

  36. G. R. Seabrook and D. J. Adams, “Inhibition of neurally evoked transmitter release by calcium channel antagonists in rat parasympathetic ganglia,” Br. J. Pharmacol., 97, 1125–1136 (1989).

    PubMed  CAS  Google Scholar 

  37. A. B. Smith and T. C. Cunnane, “Calcium channels controlling acetylcholine release in the guinea-pig isolated anterior pelvic ganglion: an electrophysiological study,” Neuroscience, 94, 891–896 (1999).

    Article  PubMed  CAS  Google Scholar 

  38. A. B. Smith, L. Motin, N. A. Lavidis, et al., “Calcium channels controlling acetylcholine release from preganglionic nerve terminals in rat autonomic ganglia,” Neuroscience, 95, 1121–1127 (2000).

    Article  PubMed  CAS  Google Scholar 

  39. S. Mochida, H. Saisu, H. Kobayashi, et al., “Impairment of syntaxin by botulinum neurotoxin C1 or antibodies inhibits acetylcholine release but not Ca2+ channel activity,” Neuroscience, 65, 905–915 (1995).

    Article  PubMed  CAS  Google Scholar 

  40. P. M. Lundy and R. Frew, “Effect of omega-agatoxin-IVA on autonomic neurotransmission,” Eur. J. Pharmacol., 261, 79–84 (1994).

    Article  PubMed  CAS  Google Scholar 

  41. J. F. Cassell and E. M. McLachlan, “The effect of a transient outward current (IA) on synaptic potentials in sympathetic ganglion cells of the guinea-pig,” J. Physiol., 374, 273–288 (1986).

    PubMed  CAS  Google Scholar 

  42. V. A. Derkach, A. A. Selyanko, and V. I. Skok, “Acetylcholine-induced current fluctuations and fast excitatory post-synaptic currents in rabbit sympathetic neurons,” J. Physiol., 336, 511–526 (1983).

    PubMed  CAS  Google Scholar 

  43. V. A. Derkach, R. A. North, A. A. Selyanko, et al., “Single channels activated by acetylcholine in rat superior cervical ganglion,” J. Physiol., 388, 141–151 (1987).

    PubMed  CAS  Google Scholar 

  44. G. D. S. Hirst and E. M. McLachlan, “Development of dendritic calcium currents in ganglion cells of the rat lower lumbar sympathetic chain,” J. Physiol., 377, 349–368 (1986).

    PubMed  CAS  Google Scholar 

  45. R. J. Callister, J. R. Keast, and P. Sah, “Ca2+-activated K+ channels in rat otic ganglion cells: role of Ca2+ entry via Ca2+ channels and nicotinic receptors,” J. Physiol., 500, 571–582 (1997).

    PubMed  CAS  Google Scholar 

  46. H. J. Häbler, W. Jänig, and M. Michaelis, “Respiratory modulation in the activity of sympathetic neurones,” Prog. Neurobiol., 43, 567–606 (1994).

    Article  PubMed  Google Scholar 

  47. E. M. McLachlan, “Transmission of signals through sympathetic ganglia-modulation, integration or simply distribution?” Acta Physiol. Scand., 177, 227–235 (2003).

    Article  PubMed  CAS  Google Scholar 

  48. H. J. Habler, E. M. McLachlan, J. Jamieson, et al., “Synaptic responses evoked by lower urinary tract stimulation in superior cervical ganglion cells in the rat,” J. Urol., 161, 1666–1671 (1999).

    Article  PubMed  CAS  Google Scholar 

  49. K. Liestol, J. Maehlen, and A. Nja, “Two types of synaptic selectivity and their interrelation during sprouting in the guinea-pig superior cervical ganglion,” J. Physiol., 384, 233–245 (1987).

    PubMed  CAS  Google Scholar 

  50. J. G. Murray and J. W. Thompson, “The occurrence and function of collateral sprouting in the sympathetic nervous system of the cat,” J. Physiol., 135, 133–162 (1957).

    PubMed  CAS  Google Scholar 

  51. J. W. Lichtman and D. Purves, “The elimination of redundant preganglionic innervation to hamster sympathetic ganglion cells in early postnatal life,” J. Physiol., 301, 213–228 (1980).

    PubMed  CAS  Google Scholar 

  52. I. L. Gibbins, P. Jobling, E. H. Teo, et al., “Heterogeneous expression of SNAP-25 and synaptic vesicle proteins by central and peripheral inputs to sympathetic neurons,” J. Comp. Neurol., 459, 25–43 (2003).

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Randwick, Australia

    E. M. McLachlan

  2. Randwick, Australia

    E. M. McLachlan

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Correspondence to E. M. McLachlan.

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Neirofiziologiya/Neurophysiology, Vol. 39, Nos. 4/5, pp. 294–301, July–October, 2007.

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McLachlan, E.M. Synaptic transmission in sympathetic vasoconstrictor pathways and its modification after injuries. Neurophysiology 39, 251–258 (2007). https://doi.org/10.1007/s11062-007-0035-4

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  • DOI: https://doi.org/10.1007/s11062-007-0035-4

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