Evidence that action potentials activate an internodal potassium conductance in lizard myelinated axons

Gavriel David, John Barrett, Ellen Barrett

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

1. We have studied action potentials and after-potentials evoked in the internodal region of visualized lizard intramuscular nerve fibres by stimulation of the proximal nerve trunk. Voltage recordings were obtained using microelectrodes inserted into the axon (intra-axonal) or into the layers of myelin (peri-internodal), with the goal of studying conditions required to activate internodal K+ currents. 2. Peri-internodal recordings made using K2SO4-, KCl- or NaCl-filled electrodes exhibited a negligible resting potential (< 2 mV), but showed action potentials with peak amplitudes of up to 78 mV and a duration less than or equal to that of the intra-axonally recorded action potential. 3. Following ionophoretic application of potassium from a peri-internodal microelectrode, the peri-internodal action potential was followed by a prolonged (hundreds of milliseconds) negative plateau. This plateau was not seen following peri-internodal ionophoresis of sodium. The prolonged negative potential (PNP) was confined to the K+-injected internode: it could be recorded by a second peri-internodal microelectrode inserted into the same internode, but not into an adjacent internode. 4. The peri-internodally recorded PNP was accompanied by an equally prolonged intra-axonal depolarizing after-potential, and by an increase in the conductance of the internodal axolemma. However, the K+ ionophoresis that produced the PNP had little or no detectable effect on the intra-axonally or peri-internodally recorded resting potential or action potential. These findings suggest that the PNP is generated by an inward current across the axolemma of the K+-injected internode, through channels opened following the action potential. 5. Following peri-internodal K+ ionophoresis a PNP could also be evoked by passage of depolarizing current pulses through an intra-axonal electrode or by passage of negative current pulses through an electrode in the K+-filled peri-internodal region. The threshold for evoking a PNP was less than the threshold for evoking an action potential, and the PNP persisted in 10 μM-tetrodotoxin. Thus the PNP is evoked by depolarization of the axolemma rather than by Na+ influx. 6. The PNP was reversibly blocked by tetraethylammonium (TEA, 2-10 mM), but was not blocked by 100 μM-3,4-diaminopyridine or 5 mM-4-aminopyridine. 7. These findings suggest that the PNP is produced by a regenerative inward K+ current across the axolemma of an internode, achieved when two conditions are met: first, [K+] outside the internode's axolemma is elevated so that the trans-axolemmal electrochemical gradient favours K+ influx, and second, the internodal axolemma is depolarized sufficiently to open TEA-sensitive K+ channels. 8. Under physiological conditions (normal extracellular [K+]) the electrochemical gradient across the internodal axolemma would be expected to favour K+ efflux from the axon. Consistent with the hypothesis that the action potential activates an internodal K+ conductance, peri-internodal recordings made using microelectrodes filled With NaCl or physiological saline show a brief positive after-potential (suggesting K+ efflux from the axon), which is blocked by TEA but not by aminopyridines. Activation of this K+ conductance would be expected to limit the peak amplitude of the passive depolarizing after-potential that follows the intra-axonally recorded action potential, and thereby limit progressive depolarization of the axon during high frequency activity.

Original languageEnglish
Pages (from-to)277-301
Number of pages25
JournalJournal of Physiology
Volume445
StatePublished - Feb 14 1992

Fingerprint

Lizards
Action Potentials
Axons
Potassium
Microelectrodes
Electrodes
Evoked Potentials
Membrane Potentials
Aminopyridines
4-Aminopyridine
Tetraethylammonium
Tetrodotoxin
Myelin Sheath
Nerve Fibers
Sodium

ASJC Scopus subject areas

  • Physiology

Cite this

Evidence that action potentials activate an internodal potassium conductance in lizard myelinated axons. / David, Gavriel; Barrett, John; Barrett, Ellen.

In: Journal of Physiology, Vol. 445, 14.02.1992, p. 277-301.

Research output: Contribution to journalArticle

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title = "Evidence that action potentials activate an internodal potassium conductance in lizard myelinated axons",
abstract = "1. We have studied action potentials and after-potentials evoked in the internodal region of visualized lizard intramuscular nerve fibres by stimulation of the proximal nerve trunk. Voltage recordings were obtained using microelectrodes inserted into the axon (intra-axonal) or into the layers of myelin (peri-internodal), with the goal of studying conditions required to activate internodal K+ currents. 2. Peri-internodal recordings made using K2SO4-, KCl- or NaCl-filled electrodes exhibited a negligible resting potential (< 2 mV), but showed action potentials with peak amplitudes of up to 78 mV and a duration less than or equal to that of the intra-axonally recorded action potential. 3. Following ionophoretic application of potassium from a peri-internodal microelectrode, the peri-internodal action potential was followed by a prolonged (hundreds of milliseconds) negative plateau. This plateau was not seen following peri-internodal ionophoresis of sodium. The prolonged negative potential (PNP) was confined to the K+-injected internode: it could be recorded by a second peri-internodal microelectrode inserted into the same internode, but not into an adjacent internode. 4. The peri-internodally recorded PNP was accompanied by an equally prolonged intra-axonal depolarizing after-potential, and by an increase in the conductance of the internodal axolemma. However, the K+ ionophoresis that produced the PNP had little or no detectable effect on the intra-axonally or peri-internodally recorded resting potential or action potential. These findings suggest that the PNP is generated by an inward current across the axolemma of the K+-injected internode, through channels opened following the action potential. 5. Following peri-internodal K+ ionophoresis a PNP could also be evoked by passage of depolarizing current pulses through an intra-axonal electrode or by passage of negative current pulses through an electrode in the K+-filled peri-internodal region. The threshold for evoking a PNP was less than the threshold for evoking an action potential, and the PNP persisted in 10 μM-tetrodotoxin. Thus the PNP is evoked by depolarization of the axolemma rather than by Na+ influx. 6. The PNP was reversibly blocked by tetraethylammonium (TEA, 2-10 mM), but was not blocked by 100 μM-3,4-diaminopyridine or 5 mM-4-aminopyridine. 7. These findings suggest that the PNP is produced by a regenerative inward K+ current across the axolemma of an internode, achieved when two conditions are met: first, [K+] outside the internode's axolemma is elevated so that the trans-axolemmal electrochemical gradient favours K+ influx, and second, the internodal axolemma is depolarized sufficiently to open TEA-sensitive K+ channels. 8. Under physiological conditions (normal extracellular [K+]) the electrochemical gradient across the internodal axolemma would be expected to favour K+ efflux from the axon. Consistent with the hypothesis that the action potential activates an internodal K+ conductance, peri-internodal recordings made using microelectrodes filled With NaCl or physiological saline show a brief positive after-potential (suggesting K+ efflux from the axon), which is blocked by TEA but not by aminopyridines. Activation of this K+ conductance would be expected to limit the peak amplitude of the passive depolarizing after-potential that follows the intra-axonally recorded action potential, and thereby limit progressive depolarization of the axon during high frequency activity.",
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N2 - 1. We have studied action potentials and after-potentials evoked in the internodal region of visualized lizard intramuscular nerve fibres by stimulation of the proximal nerve trunk. Voltage recordings were obtained using microelectrodes inserted into the axon (intra-axonal) or into the layers of myelin (peri-internodal), with the goal of studying conditions required to activate internodal K+ currents. 2. Peri-internodal recordings made using K2SO4-, KCl- or NaCl-filled electrodes exhibited a negligible resting potential (< 2 mV), but showed action potentials with peak amplitudes of up to 78 mV and a duration less than or equal to that of the intra-axonally recorded action potential. 3. Following ionophoretic application of potassium from a peri-internodal microelectrode, the peri-internodal action potential was followed by a prolonged (hundreds of milliseconds) negative plateau. This plateau was not seen following peri-internodal ionophoresis of sodium. The prolonged negative potential (PNP) was confined to the K+-injected internode: it could be recorded by a second peri-internodal microelectrode inserted into the same internode, but not into an adjacent internode. 4. The peri-internodally recorded PNP was accompanied by an equally prolonged intra-axonal depolarizing after-potential, and by an increase in the conductance of the internodal axolemma. However, the K+ ionophoresis that produced the PNP had little or no detectable effect on the intra-axonally or peri-internodally recorded resting potential or action potential. These findings suggest that the PNP is generated by an inward current across the axolemma of the K+-injected internode, through channels opened following the action potential. 5. Following peri-internodal K+ ionophoresis a PNP could also be evoked by passage of depolarizing current pulses through an intra-axonal electrode or by passage of negative current pulses through an electrode in the K+-filled peri-internodal region. The threshold for evoking a PNP was less than the threshold for evoking an action potential, and the PNP persisted in 10 μM-tetrodotoxin. Thus the PNP is evoked by depolarization of the axolemma rather than by Na+ influx. 6. The PNP was reversibly blocked by tetraethylammonium (TEA, 2-10 mM), but was not blocked by 100 μM-3,4-diaminopyridine or 5 mM-4-aminopyridine. 7. These findings suggest that the PNP is produced by a regenerative inward K+ current across the axolemma of an internode, achieved when two conditions are met: first, [K+] outside the internode's axolemma is elevated so that the trans-axolemmal electrochemical gradient favours K+ influx, and second, the internodal axolemma is depolarized sufficiently to open TEA-sensitive K+ channels. 8. Under physiological conditions (normal extracellular [K+]) the electrochemical gradient across the internodal axolemma would be expected to favour K+ efflux from the axon. Consistent with the hypothesis that the action potential activates an internodal K+ conductance, peri-internodal recordings made using microelectrodes filled With NaCl or physiological saline show a brief positive after-potential (suggesting K+ efflux from the axon), which is blocked by TEA but not by aminopyridines. Activation of this K+ conductance would be expected to limit the peak amplitude of the passive depolarizing after-potential that follows the intra-axonally recorded action potential, and thereby limit progressive depolarization of the axon during high frequency activity.

AB - 1. We have studied action potentials and after-potentials evoked in the internodal region of visualized lizard intramuscular nerve fibres by stimulation of the proximal nerve trunk. Voltage recordings were obtained using microelectrodes inserted into the axon (intra-axonal) or into the layers of myelin (peri-internodal), with the goal of studying conditions required to activate internodal K+ currents. 2. Peri-internodal recordings made using K2SO4-, KCl- or NaCl-filled electrodes exhibited a negligible resting potential (< 2 mV), but showed action potentials with peak amplitudes of up to 78 mV and a duration less than or equal to that of the intra-axonally recorded action potential. 3. Following ionophoretic application of potassium from a peri-internodal microelectrode, the peri-internodal action potential was followed by a prolonged (hundreds of milliseconds) negative plateau. This plateau was not seen following peri-internodal ionophoresis of sodium. The prolonged negative potential (PNP) was confined to the K+-injected internode: it could be recorded by a second peri-internodal microelectrode inserted into the same internode, but not into an adjacent internode. 4. The peri-internodally recorded PNP was accompanied by an equally prolonged intra-axonal depolarizing after-potential, and by an increase in the conductance of the internodal axolemma. However, the K+ ionophoresis that produced the PNP had little or no detectable effect on the intra-axonally or peri-internodally recorded resting potential or action potential. These findings suggest that the PNP is generated by an inward current across the axolemma of the K+-injected internode, through channels opened following the action potential. 5. Following peri-internodal K+ ionophoresis a PNP could also be evoked by passage of depolarizing current pulses through an intra-axonal electrode or by passage of negative current pulses through an electrode in the K+-filled peri-internodal region. The threshold for evoking a PNP was less than the threshold for evoking an action potential, and the PNP persisted in 10 μM-tetrodotoxin. Thus the PNP is evoked by depolarization of the axolemma rather than by Na+ influx. 6. The PNP was reversibly blocked by tetraethylammonium (TEA, 2-10 mM), but was not blocked by 100 μM-3,4-diaminopyridine or 5 mM-4-aminopyridine. 7. These findings suggest that the PNP is produced by a regenerative inward K+ current across the axolemma of an internode, achieved when two conditions are met: first, [K+] outside the internode's axolemma is elevated so that the trans-axolemmal electrochemical gradient favours K+ influx, and second, the internodal axolemma is depolarized sufficiently to open TEA-sensitive K+ channels. 8. Under physiological conditions (normal extracellular [K+]) the electrochemical gradient across the internodal axolemma would be expected to favour K+ efflux from the axon. Consistent with the hypothesis that the action potential activates an internodal K+ conductance, peri-internodal recordings made using microelectrodes filled With NaCl or physiological saline show a brief positive after-potential (suggesting K+ efflux from the axon), which is blocked by TEA but not by aminopyridines. Activation of this K+ conductance would be expected to limit the peak amplitude of the passive depolarizing after-potential that follows the intra-axonally recorded action potential, and thereby limit progressive depolarization of the axon during high frequency activity.

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