Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1993 Jan;460:327–349. doi: 10.1113/jphysiol.1993.sp019474

Electrical and integrative properties of rabbit sympathetic neurones re-evaluated by patch clamping non-dissociated cells.

M Gola 1, J P Niel 1
PMCID: PMC1175216  PMID: 8487198

Abstract

1. Voltage recordings were performed on non-dissociated sympathetic neurones from rabbit coeliac ganglia using the whole-cell configuration of the patch clamp technique. 2. Cells were classified depending on their firing pattern as silent cells (63%) producing either phasic (24%) or tonic (76%) spike discharge in response to depolarizing currents, and pacemaker cells (37%). 3. All the cells produced large overshooting spikes and prolonged postspike after-hyperpolarization. The peak-to-peak spike amplitude was 113.8 +/- 1 mV. Spikes were shortened and the after-hyperpolarization was suppressed when calcium channel blockers (Cd2+ and La3+) were added. 4. Silent cells have a resting potential of -58.8 +/- 1.5 mV. At potentials ranging from -50 to -90 mV, the input impedance was 490 +/- 27 M omega at 22-24 degrees C and 426 +/- 47 M omega at 35-36 degrees C. The time constant at voltages corresponding to the high input impedance region was 126 +/- 7 ms at 22-24 degrees C and 86 +/- 7 ms at 35-36 degrees C. 5. The firing frequency of the pacemaker cells was 3.2 +/- 0.5 Hz at 35-36 degrees C in the presence of nicotinic blockers. Evidence is given that the firing did not result from cell injury but was induced by an intrinsic pacemaker mechanism. Input impedance of pacemaker neurones was 580 +/- 47 M omega at 22-24 degrees C and 473 +/- 56 M omega at 35-36 degrees C. 6. Most of the pacemaker cells (63%) were motoneurones, since they were antidromically fired by stimulating post-ganglionic nerves. In addition, they received synaptic inputs from both preganglionic fibres (splanchnic nerves) and the periphery (postganglionic nerves). Long-lasting depolarizations were induced in either silent or pacemaker cells by single shocks applied to pre- and postganglionic nerves. 7. Slowly rising voltage ramps revealed the presence of an N-shaped current-voltage relationship in voltage clamped pacemaker cells. The negative slope was located in a subthreshold voltage range, between -83.4 +/- 1.4 and -59.0 +/- 1.8 mV. It was induced by the activation of a low threshold persistent inward current. Although it was tiny (22 +/- 3 pA at its peak level) this current brought the null-current voltage up to -41.0 +/- 1.4 mV, which resulted in continuous firing. 8. Due to the instability introduced by the N-shaped I-V relationship, pacemaker cells can display bistable behaviour characterized by hyperpolarizing responses.(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
327

Images in this article

330Fig. 1
on p.330

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amann R., Dray A., Hankins M. W. Stimulation of afferent fibres of the guinea-pig ureter evokes potentials in inferior mesenteric ganglion neurones. J Physiol. 1988 Aug;402:543–553. doi: 10.1113/jphysiol.1988.sp017220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barry P. H., Lynch J. W. Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol. 1991 Apr;121(2):101–117. doi: 10.1007/BF01870526. [DOI] [PubMed] [Google Scholar]
  3. Blanton M. G., Lo Turco J. J., Kriegstein A. R. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods. 1989 Dec;30(3):203–210. doi: 10.1016/0165-0270(89)90131-3. [DOI] [PubMed] [Google Scholar]
  4. Cassell J. F., Clark A. L., McLachlan E. M. Characteristics of phasic and tonic sympathetic ganglion cells of the guinea-pig. J Physiol. 1986 Mar;372:457–483. doi: 10.1113/jphysiol.1986.sp016020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cassell J. F., McLachlan E. M. Two calcium-activated potassium conductances in a subpopulation of coeliac neurones of guinea-pig and rabbit. J Physiol. 1987 Dec;394:331–349. doi: 10.1113/jphysiol.1987.sp016873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crowcroft P. J., Szurszewski J. H. A study of the inferior mesenteric and pelvic ganglia of guinea-pigs with intracellular electrodes. J Physiol. 1971 Dec;219(2):421–441. doi: 10.1113/jphysiol.1971.sp009670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Decktor D. L., Weems W. A. An intracellular characterization of neurones and neural connexions within the left coeliac ganglion of cats. J Physiol. 1983 Aug;341:197–211. doi: 10.1113/jphysiol.1983.sp014801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dun N. J., Ma R. C. Slow non-cholinergic excitatory potentials in neurones of the guinea-pig coeliac ganglia. J Physiol. 1984 Jun;351:47–60. doi: 10.1113/jphysiol.1984.sp015231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. ECCLES R. M. Intracellular potentials recorded from a mammalian sympathetic ganglion. J Physiol. 1955 Dec 29;130(3):572–584. doi: 10.1113/jphysiol.1955.sp005428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eccles J. C. Facilitation and inhibition in the superior cervical ganglion. J Physiol. 1935 Oct 26;85(2):207–238.3. doi: 10.1113/jphysiol.1935.sp003314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Edwards F. A., Konnerth A., Sakmann B., Takahashi T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch. 1989 Sep;414(5):600–612. doi: 10.1007/BF00580998. [DOI] [PubMed] [Google Scholar]
  12. Gola M. Neurones à ondes-salves des mollusques. Variations cycliques lentes des conductances ioniques. Pflugers Arch. 1974;352(1):17–36. doi: 10.1007/BF01061947. [DOI] [PubMed] [Google Scholar]
  13. Gola M., Niel J. P., Bessone R., Fayolle R. Single-channel and whole-cell recordings from non-dissociated sympathetic neurones in rabbit coeliac ganglia. J Neurosci Methods. 1992 Jun;43(1):13–22. doi: 10.1016/0165-0270(92)90062-i. [DOI] [PubMed] [Google Scholar]
  14. Hankins M. W., Dray A. Non-cholinergic synaptic potentials mediated by lumbar colonic nerve in the guinea-pig inferior mesenteric ganglion in vitro. Neuroscience. 1988 Sep;26(3):1073–1081. doi: 10.1016/0306-4522(88)90119-4. [DOI] [PubMed] [Google Scholar]
  15. Johnston D., Hablitz J. J., Wilson W. A. Voltage clamp discloses slow inward current in hippocampal burst-firing neurones. Nature. 1980 Jul 24;286(5771):391–393. doi: 10.1038/286391a0. [DOI] [PubMed] [Google Scholar]
  16. Julé Y., Niel J. P. Physiologie des ganglions sympathiques chez les mammifères. II--Activités synaptiques, aspects fonctionnels. Gastroenterol Clin Biol. 1990;14(5):451–460. [PubMed] [Google Scholar]
  17. Julé Y., Szurszewski J. H. Electrophysiology of neurones of the inferior mesenteric ganglion of the cat. J Physiol. 1983 Nov;344:277–292. doi: 10.1113/jphysiol.1983.sp014939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Keef K. D., Kreulen D. L. Peripheral nerve pathways to neurons in the guinea pig inferior mesenteric ganglion determined electrophysiologically after chronic nerve section. J Auton Nerv Syst. 1990 Feb;29(2):113–127. doi: 10.1016/0165-1838(90)90177-k. [DOI] [PubMed] [Google Scholar]
  19. King B. F., Szurszewski J. H. An electrophysiological study of inferior mesenteric ganglion of the dog. J Neurophysiol. 1984 Apr;51(4):607–615. doi: 10.1152/jn.1984.51.4.607. [DOI] [PubMed] [Google Scholar]
  20. King B. F., Szurszewski J. H. Effects of potassium channel-blocking agents on neurons in the inferior mesenteric ganglion in guinea-pig. J Auton Nerv Syst. 1988 Sep;23(3):241–252. doi: 10.1016/0165-1838(88)90099-9. [DOI] [PubMed] [Google Scholar]
  21. King B. F., Szurszewski J. H. Electronic characteristics and membrane properties of neurons in the inferior mesenteric ganglion in guinea-pig. J Auton Nerv Syst. 1988 Sep;23(3):229–239. doi: 10.1016/0165-1838(88)90098-7. [DOI] [PubMed] [Google Scholar]
  22. Konnerth A., Keller B. U., Lev-Tov A. Patch clamp analysis of excitatory synapses in mammalian spinal cord slices. Pflugers Arch. 1990 Nov;417(3):285–290. doi: 10.1007/BF00370994. [DOI] [PubMed] [Google Scholar]
  23. Kreulen D. L., Peters S. Non-cholinergic transmission in a sympathetic ganglion of the guinea-pig elicited by colon distension. J Physiol. 1986 May;374:315–334. doi: 10.1113/jphysiol.1986.sp016081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kreulen D. L., Szurszewski J. H. Nerve pathways in celiac plexus of the guinea pig. Am J Physiol. 1979 Jul;237(1):E90–E97. doi: 10.1152/ajpendo.1979.237.1.E90. [DOI] [PubMed] [Google Scholar]
  25. Krier J., Schmalz P. F., Szurszewski J. H. Central innervation of neurones in the inferior mesenteric ganglion and of the large intestine of the cat. J Physiol. 1982 Nov;332:125–138. doi: 10.1113/jphysiol.1982.sp014405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Love J. A., Szurszewski J. H. The electrophysiological effects of vasoactive intestinal polypeptide in the guinea-pig inferior mesenteric ganglion. J Physiol. 1987 Dec;394:67–84. doi: 10.1113/jphysiol.1987.sp016860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ma R. C., Dun N. J., Jiang Z. G. Evidence of slow IPSP in mammalian prevertebral ganglia. Brain Res. 1983 Jul 4;270(2):350–354. doi: 10.1016/0006-8993(83)90612-1. [DOI] [PubMed] [Google Scholar]
  28. Mazet B., Miolan J. P., Niel J. P., Julé Y., Roman C. Modulation of synaptic transmission in the rabbit coeliac ganglia by gastric and duodenal mechanoreceptors. Neuroscience. 1989;32(1):235–243. doi: 10.1016/0306-4522(89)90122-x. [DOI] [PubMed] [Google Scholar]
  29. McLachlan E. M., Meckler R. L. Characteristics of synaptic input to three classes of sympathetic neurone in the coeliac ganglion of the guinea-pig. J Physiol. 1989 Aug;415:109–129. doi: 10.1113/jphysiol.1989.sp017714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Neher E., Sakmann B. Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature. 1976 Apr 29;260(5554):799–802. doi: 10.1038/260799a0. [DOI] [PubMed] [Google Scholar]
  31. Niel J. P., Clerc N., Jule Y. Patterns of fast synaptic cholinergic activation of neurons in the celiac ganglia of cats. Am J Physiol. 1988 Dec;255(6 Pt 1):G759–G766. doi: 10.1152/ajpgi.1988.255.6.G759. [DOI] [PubMed] [Google Scholar]
  32. Niel J. P., Julé Y. Physiologie des ganglions sympathiques chez les mammifères. I--Morphologie, rôle intégrateur, neuromédiateurs. Gastroenterol Clin Biol. 1990;14(5):442–450. [PubMed] [Google Scholar]
  33. Partridge L. D., Thompson S. H., Smith S. J., Connor J. A. Current-voltage relationships of repetitively firing neurons. Brain Res. 1979 Mar 23;164:69–79. doi: 10.1016/0006-8993(79)90007-6. [DOI] [PubMed] [Google Scholar]
  34. Pongracz F., Firestein S., Shepherd G. M. Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. J Neurophysiol. 1991 Mar;65(3):747–758. doi: 10.1152/jn.1991.65.3.747. [DOI] [PubMed] [Google Scholar]
  35. Schofield G. G., Ikeda S. R. Sodium and calcium currents of acutely isolated adult rat superior cervical ganglion neurons. Pflugers Arch. 1988 May;411(5):481–490. doi: 10.1007/BF00582368. [DOI] [PubMed] [Google Scholar]
  36. Schwindt P., Crill W. Role of a persistent inward current in motoneuron bursting during spinal seizures. J Neurophysiol. 1980 May;43(5):1296–1318. doi: 10.1152/jn.1980.43.5.1296. [DOI] [PubMed] [Google Scholar]
  37. Simmons M. A., Dun N. J. Synaptic transmission in the rabbit inferior mesenteric ganglion. J Auton Nerv Syst. 1985 Dec;14(4):335–350. doi: 10.1016/0165-1838(85)90080-3. [DOI] [PubMed] [Google Scholar]
  38. Simmons M. A. The complexity and diversity of synaptic transmission in the prevertebral sympathetic ganglia. Prog Neurobiol. 1985;24(1):43–93. doi: 10.1016/0301-0082(85)90015-2. [DOI] [PubMed] [Google Scholar]
  39. Szurszewski J. H. Physiology of mammalian prevertebral ganglia. Annu Rev Physiol. 1981;43:53–68. doi: 10.1146/annurev.ph.43.030181.000413. [DOI] [PubMed] [Google Scholar]
  40. Tsunoo A., Konishi S., Otsuka M. Substance P as an excitatory transmitter of primary afferent neurons in guinea-pig sympathetic ganglia. Neuroscience. 1982;7(9):2025–2037. doi: 10.1016/0306-4522(82)90117-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES

OSZAR »