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. 1993 Nov;471:801–815. doi: 10.1113/jphysiol.1993.sp019929

Effects of axotomy or target atrophy on membrane properties of rat sympathetic ganglion cells.

M V Sánchez-Vives 1, R Gallego 1
PMCID: PMC1143990  PMID: 8120834

Abstract

1. The electrical properties of rat superior cervical ganglion cells were examined in vitro with intracellular microelectrodes after axotomy or atrophy of the submandibular salivary gland. 2. Membrane time constant, input resistance and excitatory synaptic potentials (EPSPs) were decreased to about 50% of their control values 7-10 days after axotomy. 3. Axotomized ganglion cells also showed reduced action potentials and after-hyperpolarizations (AHPs). The AHP duration was reduced to 40% of the control value. 4. In 25% of the axotomized cells, the action potential was followed by an after-depolarization (ADP) instead of the AHP that was always present in control cells. In eleven out of seventeen axotomized cells with ADP, preganglionic stimulation failed to evoke an EPSP, whereas the failure of the synaptic response was never observed in control cells and occurred only in two of fifty-three axotomized cells with AHP. 5. In some axotomized cells with AHP, a depolarizing potential developed after a train of action potentials. This was never observed in control cells. 6. Sympathetic neurones innervating the submandibular gland in control animals had membrane properties similar to those observed in other ganglion cells. 7. The properties of neurones innervating the submandibular gland remained unaltered after the experimentally induced atrophy of the gland. 8. It is concluded that the marked effects of short-term axotomy on membrane properties of sympathetic ganglion cells are not reproduced by long-term atrophy of the target tissue.

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Selected References

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  1. Aguayo L. G., Weight F. F., White G. TTX-sensitive action potentials and excitability of adult rat sensory neurons cultured in serum- and exogenous nerve growth factor-free medium. Neurosci Lett. 1991 Jan 2;121(1-2):88–92. doi: 10.1016/0304-3940(91)90656-e. [DOI] [PubMed] [Google Scholar]
  2. Barrett E. F., Barret J. N. Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones. J Physiol. 1976 Mar;255(3):737–774. doi: 10.1113/jphysiol.1976.sp011306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrett E. F., Barrett J. N., Crill W. E. Voltage-sensitive outward currents in cat motoneurones. J Physiol. 1980 Jul;304:251–276. doi: 10.1113/jphysiol.1980.sp013323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belmonte C., Gallego R. Membrane properties of cat sensory neurones with chemoreceptor and baroreceptor endings. J Physiol. 1983 Sep;342:603–614. doi: 10.1113/jphysiol.1983.sp014871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belmonte C., Gallego R., Morales A. Membrane properties of primary sensory neurones of the cat after peripheral reinnervation. J Physiol. 1988 Nov;405:219–232. doi: 10.1113/jphysiol.1988.sp017330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown D. A., Adams P. R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature. 1980 Feb 14;283(5748):673–676. doi: 10.1038/283673a0. [DOI] [PubMed] [Google Scholar]
  7. Busis N. A., Weight F. F. Spike after-hyperpolarisation of a sympathetic neurone is calcium sensitive and is potentiated by theophylline. Nature. 1976 Sep 30;263(5576):434–436. doi: 10.1038/263434a0. [DOI] [PubMed] [Google Scholar]
  8. Caviedes P., Koistinaho J., Ault B., Rapoport S. I. Effects of nerve growth factor on electrical membrane properties of cultured dorsal root ganglia neurons from normal and trisomy 21 human fetuses. Brain Res. 1991 Aug 16;556(2):285–291. doi: 10.1016/0006-8993(91)90317-o. [DOI] [PubMed] [Google Scholar]
  9. Chalazonitis A., Peterson E. R., Crain S. M. Nerve growth factor regulates the action potential duration of mature sensory neurons. Proc Natl Acad Sci U S A. 1987 Jan;84(1):289–293. doi: 10.1073/pnas.84.1.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Constanti A., Brown D. A. M-Currents in voltage-clamped mammalian sympathetic neurones. Neurosci Lett. 1981 Jul 17;24(3):289–294. doi: 10.1016/0304-3940(81)90173-7. [DOI] [PubMed] [Google Scholar]
  11. Czéh G., Gallego R., Kudo N., Kuno M. Evidence for the maintenance of motoneurone properties by muscle activity. J Physiol. 1978 Aug;281:239–252. doi: 10.1113/jphysiol.1978.sp012419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Czéh G., Kudo N., Kuno M. Membrane properties and conduction velocity in sensory neurones following central or peripheral axotomy. J Physiol. 1977 Aug;270(1):165–180. doi: 10.1113/jphysiol.1977.sp011944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. ECCLES J. C., LIBET B., YOUNG R. R. The behaviour of chromatolysed motoneurones studied by intracellular recording. J Physiol. 1958 Aug 29;143(1):11–40. doi: 10.1113/jphysiol.1958.sp006041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eugene D., Taxi J. Effects of axotomy on synaptic transmission and structure in frog sympathetic ganglia. J Neurocytol. 1991 May;20(5):404–419. doi: 10.1007/BF01355537. [DOI] [PubMed] [Google Scholar]
  15. Flett D. L., Bell C. Topography of functional subpopulations of neurons in the superior cervical ganglion of the rat. J Anat. 1991 Aug;177:55–66. [PMC free article] [PubMed] [Google Scholar]
  16. Foehring R. C., Sypert G. W., Munson J. B. Properties of self-reinnervated motor units of medial gastrocnemius of cat. II. Axotomized motoneurons and time course of recovery. J Neurophysiol. 1986 May;55(5):947–965. doi: 10.1152/jn.1986.55.5.947. [DOI] [PubMed] [Google Scholar]
  17. Gallego R., Geijo E. Chronic block of the cervical trunk increases synaptic efficacy in the superior and stellate ganglia of the guinea-pig. J Physiol. 1987 Jan;382:449–462. doi: 10.1113/jphysiol.1987.sp016377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gallego R., Ivorra I., Morales A. Effects of central or peripheral axotomy on membrane properties of sensory neurones in the petrosal ganglion of the cat. J Physiol. 1987 Oct;391:39–56. doi: 10.1113/jphysiol.1987.sp016724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gallego R., Kuno M., Núez R., Snider W. D. Dependence of motoneurone properties on the length of immobilized muscle. J Physiol. 1979 Jun;291:179–189. doi: 10.1113/jphysiol.1979.sp012806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gallego R. The ionic basis of action potentials in petrosal ganglion cells of the cat. J Physiol. 1983 Sep;342:591–602. doi: 10.1113/jphysiol.1983.sp014870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gordon T., Kelly M. E., Sanders E. J., Shapiro J., Smith P. A. The effects of axotomy on bullfrog sympathetic neurones. J Physiol. 1987 Nov;392:213–229. doi: 10.1113/jphysiol.1987.sp016777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gustafsson B. Changes in motoneurone electrical properties following axotomy. J Physiol. 1979 Aug;293:197–215. doi: 10.1113/jphysiol.1979.sp012885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kawai T., Watanabe M. Blockade of Ca-activated K conductance by apamin in rat sympathetic neurones. Br J Pharmacol. 1986 Jan;87(1):225–232. doi: 10.1111/j.1476-5381.1986.tb10175.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kelly M. E., Gordon T., Shapiro J., Smith P. A. Axotomy affects calcium-sensitive potassium conductance in sympathetic neurones. Neurosci Lett. 1986 Jun 18;67(2):163–168. doi: 10.1016/0304-3940(86)90391-5. [DOI] [PubMed] [Google Scholar]
  25. Kuno M., Miyata Y., Muñoz-Martinez E. J. Differential reaction of fast and slow alpha-motoneurones to axotomy. J Physiol. 1974 Aug;240(3):725–739. doi: 10.1113/jphysiol.1974.sp010631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Laiwand R., Werman R., Yarom Y. Electrophysiology of degenerating neurones in the vagal motor nucleus of the guinea-pig following axotomy. J Physiol. 1988 Oct;404:749–766. doi: 10.1113/jphysiol.1988.sp017317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Matthews M. R., Nelson V. H. Detachment of structurally intact nerve endings from chromatolytic neurones of rat superior cervical ganglion during the depression of synaptic transmission induced by post-ganglionic axotomy. J Physiol. 1975 Feb;245(1):91–135. doi: 10.1113/jphysiol.1975.sp010837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McAfee D. A., Yarowsky P. J. Calcium-dependent potentials in the mammalian sympathetic neurone. J Physiol. 1979 May;290(2):507–523. doi: 10.1113/jphysiol.1979.sp012787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nishi S., North R. A. Intracellular recording from the myenteric plexus of the guinea-pig ileum. J Physiol. 1973 Jun;231(3):471–491. doi: 10.1113/jphysiol.1973.sp010244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Omri G., Meiri H. Characterization of sodium currents in mammalian sensory neurons cultured in serum-free defined medium with and without nerve growth factor. J Membr Biol. 1990 Apr;115(1):13–29. doi: 10.1007/BF01869102. [DOI] [PubMed] [Google Scholar]
  31. Pennefather P., Lancaster B., Adams P. R., Nicoll R. A. Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cells. Proc Natl Acad Sci U S A. 1985 May;82(9):3040–3044. doi: 10.1073/pnas.82.9.3040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Purves D. Functional and structural changes in mammalian sympathetic neurones following interruption of their axons. J Physiol. 1975 Nov;252(2):429–463. doi: 10.1113/jphysiol.1975.sp011151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Purves D., Lichtman J. W. Geometrical differences among homologous neurons in mammals. Science. 1985 Apr 19;228(4697):298–302. doi: 10.1126/science.3983631. [DOI] [PubMed] [Google Scholar]
  34. Purves D., Snider W. D., Voyvodic J. T. Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature. 1988 Nov 10;336(6195):123–128. doi: 10.1038/336123a0. [DOI] [PubMed] [Google Scholar]
  35. Redman S. J., McLachlan E. M., Hirst G. D. Nonuniform passive membrane properties of rat lumbar sympathetic ganglion cells. J Neurophysiol. 1987 Mar;57(3):633–644. doi: 10.1152/jn.1987.57.3.633. [DOI] [PubMed] [Google Scholar]
  36. Sah P., McLachlan E. M. Ca(2+)-activated K+ currents underlying the afterhyperpolarization in guinea pig vagal neurons: a role for Ca(2+)-activated Ca2+ release. Neuron. 1991 Aug;7(2):257–264. doi: 10.1016/0896-6273(91)90264-z. [DOI] [PubMed] [Google Scholar]
  37. Titmus M. J., Faber D. S. Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog Neurobiol. 1990;35(1):1–51. doi: 10.1016/0301-0082(90)90039-j. [DOI] [PubMed] [Google Scholar]
  38. Titmus M. J., Faber D. S., Zottoli S. J. Altered excitability of goldfish mauthner cell following axotomy. I. Characterization and correlations with somatic and axonal morphological reactions. J Neurophysiol. 1986 Jun;55(6):1424–1439. doi: 10.1152/jn.1986.55.6.1424. [DOI] [PubMed] [Google Scholar]
  39. Traynor P., Dryden W. F., Smith P. A. Trophic regulation of action potential in bullfrog sympathetic neurones. Can J Physiol Pharmacol. 1992 Jun;70(6):826–834. doi: 10.1139/y92-111. [DOI] [PubMed] [Google Scholar]
  40. Voyvodic J. T. Peripheral target regulation of dendritic geometry in the rat superior cervical ganglion. J Neurosci. 1989 Jun;9(6):1997–2010. doi: 10.1523/JNEUROSCI.09-06-01997.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Womble M. D., Roper S. Retrograde effects of target atrophy on submandibular ganglion neurons. J Neurophysiol. 1987 Aug;58(2):276–287. doi: 10.1152/jn.1987.58.2.276. [DOI] [PubMed] [Google Scholar]
  42. Yawo H. Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy. J Neurosci. 1987 Nov;7(11):3703–3711. doi: 10.1523/JNEUROSCI.07-11-03703.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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