Journal of Neurophysiology, Vol 69, Issue 5 1632-1644, Copyright © 1993 by APS

ARTICLES

Potassium currents and their modulation by muscarine and substance P in neuronal cultures from adult guinea pig celiac ganglia

S. Vanner, R. J. Evans, S. G. Matsumoto and A. Surprenant
Vollum Institute, Oregon Health Sciences University, Portland 97201.

1. Intracellular microelectrode and whole-cell patch-clamp recordings were obtained from adult guinea pig celiac ganglion neurons grown in tissue culture for 7-14 days. Over 90% of neurons showed phasic-type action-potential discharge with the use of either type of recording electrode; they stained immunohistochemically for catecholamines, tyrosine hydroxylase, and neuropeptide Y. Input resistance (140 M omega) and action-potential amplitude (103 mV) were significantly greater with whole-cell than with microelectrode recordings, but other passive electrical properties were similar. 2. Five potassium currents were characterized: an apamin-sensitive after hyperpolarizing current (IAHP), an apamin and tetraethylammonium-insensitive slow IAHP, an M-like current, a transient outward IA current, and a delayed rectifier IK current. A hyperpolarization-activated cationic Ih current was also present. The first three currents were not observed with whole-cell recordings. 3. Cadmium (200 microM), cobalt (1 mM), lanthanum (30 microM), or a low calcium/high magnesium solution blocked both IAHPS and the M-like current; barium (1 mM) also blocked these currents. 4. Kinetics of the M-like current were best described by a double exponential fit to deactivating tail currents with time constants of 50 and 390 ms at -50 mV. The apamin-sensitive and slow IAHP decayed exponentially with time constants of 145 ms and 3.5 s, respectively. There was no correlation between occurrence of M-like current (95% of neurons) and slow IAHP (40% of neurons), nor any correlation between magnitude of M-like current and IAHP in those cells exhibiting both currents. 5. Muscarine and substance P (SP) caused depolarizations or inward currents (under voltage clamp) at the resting potential (-55 mV) associated with a decreased membrane conductance. The slow IAHP and the M-like current, but not the apamin-sensitive IAHP nor the IA, were blocked by muscarine and SP (IC50 3 microM and 100 nM, respectively). Muscarine and SP also decreased a "leak" potassium current. 6. We conclude that celiac neurons express two calcium-dependent IAHP currents and a calcium-dependent M-current; these are seen by fine-tipped intracellular microelectrodes but not by whole-cell patch electrodes. These currents are not required for spike frequency accommodation. Muscarine and SP reduce these currents, as well as voltage-independent leakage potassium current.

This article has been cited by other articles:

				M. Koike-Tani, J. M Collins, T. Kawano, P. Zhao, Q. Zhao, T. Kozasa, S. Nakajima, and Y. Nakajima Signal transduction pathway for the substance P-induced inhibition of rat Kir3 (GIRK) channel J. Physiol., April 15, 2005; 564(2): 489 - 500. [Abstract] [Full Text] [PDF]

				J. Jamieson, H. D. Boyd, and E. M. McLachlan Simulations to Derive Membrane Resistivity in Three Phenotypes of Guinea Pig Sympathetic Postganglionic Neuron J Neurophysiol, May 1, 2003; 89(5): 2430 - 2440. [Abstract] [Full Text] [PDF]

				P. Jobling, J. P. Messenger, and I. L. Gibbins Differential Expression of Functionally Identified and Immunohistochemically Identified NK1 Receptors on Sympathetic Neurons J Neurophysiol, May 1, 2001; 85(5): 1888 - 1898. [Abstract] [Full Text] [PDF]

				A. B. Belousov, B. F. O'Hara, and J. V. Denisova Acetylcholine Becomes the Major Excitatory Neurotransmitter in the Hypothalamus In Vitro in the Absence of Glutamate Excitation J. Neurosci., March 15, 2001; 21(6): 2015 - 2027. [Abstract] [Full Text] [PDF]

				J. Cuevas and D. J. Adams Substance P Preferentially Inhibits Large Conductance Nicotinic ACh Receptor Channels in Rat Intracardiac Ganglion Neurons J Neurophysiol, October 1, 2000; 84(4): 1961 - 1970. [Abstract] [Full Text] [PDF]

				J. Martinez-Pinna, P. J. Davies, and E. M. McLachlan Diversity of Channels Involved in Ca2+ Activation of K+ Channels During the Prolonged AHP in Guinea-Pig Sympathetic Neurons J Neurophysiol, September 1, 2000; 84(3): 1346 - 1354. [Abstract] [Full Text] [PDF]

				Q. Lei, M. B. Jones, E. M. Talley, A. D. Schrier, W. E. McIntire, J. C. Garrison, and D. A. Bayliss Activation and inhibition of G protein-coupled inwardly rectifying potassium (Kir3) channels by G protein beta gamma subunits PNAS, August 15, 2000; 97(17): 9771 - 9776. [Abstract] [Full Text] [PDF]

				K. N. Browning, Z. L. Zheng, D. L. Kreulen, and R. A. Travagli Effects of Nitric Oxide in Cultured Prevertebral Sympathetic Ganglion Neurons J. Pharmacol. Exp. Ther., August 1, 1998; 286(2): 1086 - 1093. [Abstract] [Full Text]

				A. C. Myers Ca2+ and K+ currents regulate accommodation and firing frequency in guinea pig bronchial ganglion neurons Am J Physiol Lung Cell Mol Physiol, August 1, 1998; 275(2): L357 - L364. [Abstract] [Full Text] [PDF]

				X. Wang and D. Robertson Substance P-Induced Inward Current in Identified Auditory Efferent Neurons in Rat Brain Stem Slices J Neurophysiol, July 1, 1998; 80(1): 218 - 229. [Abstract] [Full Text] [PDF]

				R. Gilbert, J. S. Ryan, M. Horackova, F. M. Smith, and M. E. M. Kelly Actions of substance P on membrane potential and ionic currents in guinea pig stellate ganglion neurons Am J Physiol Cell Physiol, April 1, 1998; 274(4): C892 - C903. [Abstract] [Full Text] [PDF]

				C. A. D. Negro and S. H. Chandler Physiological and Theoretical Analysis of K+ Currents Controlling Discharge in Neonatal Rat Mesencephalic Trigeminal Neurons J Neurophysiol, February 1, 1997; 77(2): 537 - 553. [Abstract] [Full Text] [PDF]

				T. Aosaki and Y. Kawaguchi Actions of Substance P on Rat Neostriatal Neurons In Vitro J. Neurosci., August 15, 1996; 16(16): 5141 - 5153. [Abstract] [Full Text] [PDF]

				Q. Lei, E. M. Talley, and D. A. Bayliss Receptor-mediated Inhibition of G Protein-coupled Inwardly Rectifying Potassium Channels Involves Galpha q Family Subunits, Phospholipase C, and a Readily Diffusible Messenger J. Biol. Chem., May 11, 2001; 276(20): 16720 - 16730. [Abstract] [Full Text] [PDF]