Journal of Neurophysiology, Vol 72, Issue 2 634-643, Copyright © 1994 by APS

ARTICLES

Action potential propagation through embryonic dorsal root ganglion cells in culture. II. Decrease of conduction reliability during repetitive stimulation

C. Luscher, J. Streit, P. Lipp and H. R. Luscher
Institute of Physiology, University of Berne, Switzerland.

1. The reliability of the propagation of action potentials (AP) through dorsal root ganglion (DRG) cells in embryonic slice cultures was investigated during repetitive stimulation at 1-20 Hz. Membrane potentials of DRG cells were recorded intracellularly while the axons were stimulated by an extracellular electrode. 2. In analogy to the double-pulse experiments reported previously, either one or two types of propagation failures were recorded during repetitive stimulation, depending on the cell morphology. In contrast to the double-pulse experiments, the failures appeared at longer interpulse intervals and usually only after several tens of stimuli with reliable propagation. 3. In the period with reliable propagation before the failures, a decrease in the conduction velocity and in the amplitude of the afterhyperpolarization (AHP), an increase in the total membrane conductance, and the disappearance of the action potential "shoulder" were observed. 4. The reliability of conduction during repetitive stimulation was improved by lowering the extracellular calcium concentration or by replacing the extracellular calcium by strontium. The reliability of conduction decreased by the application of cadmium, a calcium channel blocker, 4-amino pyridine, a fast potassium channel blocker, or apamin or muscarine, the blockers of calcium-dependent potassium channels. The reliability of conduction was not effected by blocking the sodium potassium pump with ouabain or by replacing extracellular sodium with lithium. 5. In the period with reliable propagation cadmium, apamin, and muscarine reduced the amplitude of the AHP. The shoulder of the action potential was more pronounced and not sensitive to repetitive stimulation when extracellular calcium was replaced by strontium. It disappeared when cadmium was applied. 6. In DRG somata changes of the intracellular Ca2+ concentration were monitored by measuring the fluorescence of the Ca2+ indicator Fluo-3 with a laser-scanning confocal microscope. During repetitive stimulation, an accumulation of intracellular calcium occurred that recovered very slowly (tens of seconds) after the AP trains. 7. Computer model simulations performed in analogy to the experimental protocols produced conduction failures during repetitive stimulation only when the calcium currents during the APs were reduced. 8. From these findings it is concluded that conduction failures during repetitive stimulation are dependent on an accumulation of intracellular calcium leading to an inactivation of calcium currents, combined with small contributions of an accumulation of extracellular potassium and a summation of slow potassium conductances.

This article has been cited by other articles:

				Q. Hogan, P. Lirk, M. Poroli, M. Rigaud, A. Fuchs, P. Fillip, M. Ljubkovic, G. Gemes, and D. Sapunar Restoration of Calcium Influx Corrects Membrane Hyperexcitability in Injured Rat Dorsal Root Ganglion Neurons Anesth. Analg., September 1, 2008; 107(3): 1045 - 1051. [Abstract] [Full Text] [PDF]

				P. Lirk, M. Poroli, M. Rigaud, A. Fuchs, P. Fillip, C.-Y. Huang, M. Ljubkovic, D. Sapunar, and Q. Hogan Modulators of Calcium Influx Regulate Membrane Excitability in Rat Dorsal Root Ganglion Neurons Anesth. Analg., August 1, 2008; 107(2): 673 - 685. [Abstract] [Full Text] [PDF]

				J. P Meeks, X. Jiang, and S. Mennerick Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus J. Physiol., July 15, 2005; 566(2): 425 - 441. [Abstract] [Full Text] [PDF]

				X Fang, S McMullan, S. N Lawson, and L Djouhri Electrophysiological differences between nociceptive and non-nociceptive dorsal root ganglion neurones in the rat in vivo J. Physiol., June 15, 2005; 565(3): 927 - 943. [Abstract] [Full Text] [PDF]

				P. K. Bahia, R. Suzuki, D. C. H. Benton, A. J. Jowett, M. X. Chen, Derek. J. Trezise, A. H. Dickenson, and G. W. J. Moss A Functional Role for Small-Conductance Calcium-Activated Potassium Channels in Sensory Pathways Including Nociceptive Processes J. Neurosci., April 6, 2005; 25(14): 3489 - 3498. [Abstract] [Full Text] [PDF]

				J. Munoz-Cuevas, H. Vara, and A. Colino Characterization of release-independent short-term depression in the juvenile rat hippocampus J. Physiol., July 15, 2004; 558(2): 527 - 548. [Abstract] [Full Text] [PDF]

				G T Coleman, D A Mahns, H Q Zhang, and M J Rowe Impulse propagation over tactile and kinaesthetic sensory axons to central target neurones of the cuneate nucleus in cat J. Physiol., July 15, 2003; 550(2): 553 - 562. [Abstract] [Full Text] [PDF]

				G. T. Coleman, H.-Q. Zhang, and M. J. Rowe Transmission Security for Single Kinesthetic Afferent Fibers of Joint Origin and Their Target Cuneate Neurons in the Cat J. Neurosci., April 1, 2003; 23(7): 2980 - 2992. [Abstract] [Full Text] [PDF]

				P. Darbon, C. Pignier, E. Niggli, and J. Streit Involvement of Calcium in Rhythmic Activity Induced by Disinhibition in Cultured Spinal Cord Networks J Neurophysiol, September 1, 2002; 88(3): 1461 - 1468. [Abstract] [Full Text] [PDF]

				R. Amir, C.-N. Liu, J. D. Kocsis, and M. Devor Oscillatory mechanism in primary sensory neurones Brain, February 1, 2002; 125(2): 421 - 435. [Abstract] [Full Text] [PDF]

				R. Amir, M. Michaelis, and M. Devor Burst Discharge in Primary Sensory Neurons: Triggered by Subthreshold Oscillations, Maintained by Depolarizing Afterpotentials J. Neurosci., February 1, 2002; 22(3): 1187 - 1198. [Abstract] [Full Text] [PDF]

				L. Djouhri, D. Dawbarn, A. Robertson, R. Newton, and S. N. Lawson Time Course and Nerve Growth Factor Dependence of Inflammation-Induced Alterations in Electrophysiological Membrane Properties in Nociceptive Primary Afferent Neurons J. Neurosci., November 15, 2001; 21(22): 8722 - 8733. [Abstract] [Full Text] [PDF]

				R. Hosseini, D. C H Benton, P. M Dunn, D. H Jenkinson, and G. W J Moss SK3 is an important component of K+ channels mediating the afterhyperpolarization in cultured rat SCG neurones J. Physiol., September 1, 2001; 535(2): 323 - 334. [Abstract] [Full Text] [PDF]

				E. Rumpel and J. C. Behrends Postsynaptic Receptor Occupancy During Evoked Transmission at Striatal GABAergic Synapses In Vitro J Neurophysiol, August 1, 2000; 84(2): 771 - 779. [Abstract] [Full Text] [PDF]

				D. L. Brody and D. T. Yue Release-Independent Short-Term Synaptic Depression in Cultured Hippocampal Neurons J. Neurosci., April 1, 2000; 20(7): 2480 - 2494. [Abstract] [Full Text] [PDF]

				D. W. Hochman and P. A. Schwartzkroin Chloride-Cotransport Blockade Desynchronizes Neuronal Discharge in the "Epileptic" Hippocampal Slice J Neurophysiol, January 1, 2000; 83(1): 406 - 417. [Abstract] [Full Text] [PDF]

				D. K. Selig, R. A. Nicoll, and R. C. Malenka Hippocampal Long-Term Potentiation Preserves the Fidelity of Postsynaptic Responses to Presynaptic Bursts J. Neurosci., February 15, 1999; 19(4): 1236 - 1246. [Abstract] [Full Text] [PDF]

				E. Rumpel and J. C Behrends Sr2+-dependent asynchronous evoked transmission at rat striatal inhibitory synapses in vitro J. Physiol., January 15, 1999; 514(2): 447 - 458. [Abstract] [Full Text] [PDF]

				A. Scholz, M. Gruss, and W. Vogel Properties and functions of calcium-activated K+ channels in small neurones of rat dorsal root ganglion studied in a thin slice preparation J. Physiol., November 15, 1998; 513(1): 55 - 69. [Abstract] [Full Text] [PDF]

				P. J. Mackenzie and T. H. Murphy High Safety Factor for Action Potential Conduction Along Axons But Not Dendrites of Cultured Hippocampal and Cortical Neurons J Neurophysiol, October 1, 1998; 80(4): 2089 - 2101. [Abstract] [Full Text] [PDF]

				I. L. Kopysova and D. Debanne Critical Role of Axonal A-Type K+ Channels and Axonal Geometry in the Gating of Action Potential Propagation along CA3 Pyramidal Cell Axons: A Simulation Study J. Neurosci., September 15, 1998; 18(18): 7436 - 7451. [Abstract] [Full Text] [PDF]

				H.-R. Luscher and M. E. Larkum Modeling Action Potential Initiation and Back-Propagation in Dendrites of Cultured Rat Motoneurons J Neurophysiol, August 1, 1998; 80(2): 715 - 729. [Abstract] [Full Text] [PDF]

				W. J. Joiner, L.-Y. Wang, M. D. Tang, and L. K. Kaczmarek hSK4, a member of a novel subfamily of calcium-activated potassium channels PNAS, September 30, 1997; 94(20): 11013 - 11018. [Abstract] [Full Text] [PDF]

				B G Frenguelli and R Malinow Fluctuations in intracellular calcium responses to action potentials in single en passage presynaptic boutons of layer V neurons in neocortical slices. Learn. Mem., January 1, 1996; 3(2-3): 150 - 159. [Abstract] [PDF]

				N Spruston, Y Schiller, G Stuart, and B Sakmann Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites Science, April 14, 1995; 268(5208): 297 - 300. [Abstract] [PDF]

				C. L. Cox, W. Denk, D. W. Tank, and K. Svoboda From the Cover: Action potentials reliably invade axonal arbors of rat neocortical neurons PNAS, August 15, 2000; 97(17): 9724 - 9728. [Abstract] [Full Text] [PDF]