Fast Synaptic Transmission Mediated by Alpha-bungarotoxin-sensitive Nicotinic Acetylcholine Receptors in Lamina X Neurones of Neonatal Rat Spinal Cord

Overview

Journal J Physiol

Specialty Physiology

Date 2002 Nov 2

PMID 12411519

Citations 9

Authors

A Bradaia

J Trouslard

Affiliations

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Abstract

Using patch clamp recordings on neonatal rat spinal cord slices, we have looked for the presence of alpha-bungarotoxin-sensitive nicotinic ACh receptors (nAChRs) on sympathetic preganglionic neurones (SPNs) surrounding the central canal of the spinal cord (lamina X) and examined whether they were implicated in a fast cholinergic synaptic transmission. SPNs were identified either by their morphology using biocytin in the recording electrode and/or by antidromic stimulation of the ventral rootlets. The selective alpha7-containing nAChR (alpha7*nAChR) agonist choline (10 mM) induced a fast, rapidly desensitizing inward current, which was fully blocked by alpha-bungarotoxin (alpha-BgT; 50 nM) and strychnine (1 microM), two antagonists of alpha7*nAChRs. The I-V relationship of the choline-induced current showed a strong inward-going rectification. Electrically evoked excitatory postsynaptic currents (eEPSCs) could be recorded. At -60 mV, eEPSCs peaked at -26.2 pA and decayed monoexponentially with a mean time constant of 8.5 ms. The current-voltage relationship for eEPSCs exhibited a strong inward rectification and a reversal potential close to 0 mV, compatible with a non-selective cationic current. The appearance of eEPSCs was entirely suppressed by the application of 100 microM ACh or nicotine. Choline (10 mM) and 1,1-dimethyl-4-phenylpiperazinium iodide (DMPP; 100 microM) both reduced the amplitude of eEPSCs, whereas cytisine (100 microM) had no effect. Strychnine (1 microM) and alpha-BgT (50 nM) both suppressed the eEPSCs. Blocking the P2X purinergic and 5-HT(3) receptors had no effect on eEPSCs. DMPP induced four types of current, which differed in their onset and desensitization rate. The most frequently encountered responses were insensitive to the action of strychnine and alpha-BgT, and were reproduced by ACh and nicotine but not by cytisine. We conclude that SPNs of the lamina X express several classes of nAChRs and in particular alpha-BgT-sensitive nAChRs. This is the first demonstration in a mammalian spinal cord preparation of a fast cholinergic neurotransmission in which alpha-BgT-sensitive nicotinic receptors are involved.

Citing Articles

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References

Luetje C, Patrick J . Both alpha- and beta-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci. 1991; 11(3):837-45. PMC: 6575344. View

Gerzanich V, Anand R, Lindstrom J . Homomers of alpha 8 and alpha 7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties. Mol Pharmacol. 1994; 45(2):212-20. View

Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J . Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol. 1989; 284(2):314-35. DOI: 10.1002/cne.902840212. View

Hatton G, Yang Q . Synaptic potentials mediated by alpha 7 nicotinic acetylcholine receptors in supraoptic nucleus. J Neurosci. 2002; 22(1):29-37. PMC: 6757599. View

Saitoh T, Ishida M, Maruyama M, Shinozaki H . A novel antagonist, phenylbenzene omega-phosphono-alpha-amino acid, for strychnine-sensitive glycine receptors in the rat spinal cord. Br J Pharmacol. 1994; 113(1):165-70. PMC: 1510041. DOI: 10.1111/j.1476-5381.1994.tb16189.x. View

Garcia-Colunga J, Miledi R . Modulation of nicotinic acetylcholine receptors by strychnine. Proc Natl Acad Sci U S A. 1999; 96(7):4113-8. PMC: 22429. DOI: 10.1073/pnas.96.7.4113. View

Borges L, Iversen S . Topography of choline acetyltransferase immunoreactive neurons and fibers in the rat spinal cord. Brain Res. 1986; 362(1):140-8. DOI: 10.1016/0006-8993(86)91407-1. View

Logan S, Pickering A, Gibson I, Nolan M, Spanswick D . Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. J Physiol. 1996; 495 ( Pt 2):491-502. PMC: 1160807. DOI: 10.1113/jphysiol.1996.sp021609. View

Arias H . Agonist self-inhibitory binding site of the nicotinic acetylcholine receptor. J Neurosci Res. 1996; 44(2):97-105. DOI: 10.1002/(SICI)1097-4547(19960415)44:2<97::AID-JNR1>3.0.CO;2-B. View

10.

Papke R, Bencherif M, Lippiello P . An evaluation of neuronal nicotinic acetylcholine receptor activation by quaternary nitrogen compounds indicates that choline is selective for the alpha 7 subtype. Neurosci Lett. 1996; 213(3):201-4. DOI: 10.1016/0304-3940(96)12889-5. View

11.

ECCLES J, FATT P, Koketsu K . Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol. 1954; 126(3):524-62. PMC: 1365877. DOI: 10.1113/jphysiol.1954.sp005226. View

12.

Wonnacott S . Presynaptic nicotinic ACh receptors. Trends Neurosci. 1997; 20(2):92-8. DOI: 10.1016/s0166-2236(96)10073-4. View

13.

Orr-Urtreger A, Goldner F, Saeki M, Lorenzo I, Goldberg L, De Biasi M . Mice deficient in the alpha7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents. J Neurosci. 1997; 17(23):9165-71. PMC: 6573618. View

14.

Virginio C, Giacometti A, Aldegheri L, Rimland J, Terstappen G . Pharmacological properties of rat alpha 7 nicotinic receptors expressed in native and recombinant cell systems. Eur J Pharmacol. 2002; 445(3):153-61. DOI: 10.1016/s0014-2999(02)01750-8. View

15.

Xin Q, Wightman R . Transport of choline in rat brain slices. Brain Res. 1998; 776(1-2):126-32. DOI: 10.1016/s0006-8993(97)00996-7. View

16.

Elgoyhen A, Vetter D, Katz E, Rothlin C, Heinemann S, Boulter J . alpha10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci U S A. 2001; 98(6):3501-6. PMC: 30682. DOI: 10.1073/pnas.051622798. View

17.

Sargent P . The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci. 1993; 16:403-43. DOI: 10.1146/annurev.ne.16.030193.002155. View

18.

Macdermott A, Role L, Siegelbaum S . Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci. 1999; 22:443-85. DOI: 10.1146/annurev.neuro.22.1.443. View

19.

Drasdo A, Caulfield M, Bertrand D, Bertrand S, Wonnacott S . Methyl lycaconitine: A novel nicotinic antagonist. Mol Cell Neurosci. 2009; 3(3):237-43. DOI: 10.1016/1044-7431(92)90043-2. View

20.

Bordey A, Feltz P, Trouslard J . Nicotinic actions on neurones of the central autonomic area in rat spinal cord slices. J Physiol. 1996; 497 ( Pt 1):175-87. PMC: 1160921. DOI: 10.1113/jphysiol.1996.sp021758. View