Activation of internodal potassium conductance in rat myelinated axons

Gavriel David, John Barrett, Ellen Barrett

Research output: Contribution to journalArticle

48 Citations (Scopus)

Abstract

1. Voltage changes associated with currents crossing the internodal axolemma were monitored using a microelectrode inserted into the myelin sheath (peri-internodal region) of rat phrenic nerve fibres. This microelectrode was also used to change the potential and the ionic environment in the peri-internodal region. 2. Following stimulation of the proximal nerve trunk, the peri-internodal electrode recorded a positive-going action potential whose amplitude increased (up to 75 mV) with increasing depth of microelectrode penetration into the myelin. The resting potential recorded by the peri-internodal electrode remained within 4 mV of bath ground. 3. Confocal imaging of fibres injected peri-internodally with the fluorescent dye Lucifer Yellow revealed a staining pattern consistent with spread of dye throughout the myelin sheath of the injected internode. 4. After ionophoresis of K+ (but not Na+) into the peri-internodal region, the action potential was followed by a prolonged negative potential (PNP) lasting hundreds of milliseconds to several seconds. The duration of the PNP increased as the frequency of stimulation decreased. PNPs could also be evoked by sub-threshold depolarization of the internodal axolemma with peri-internodally applied current pulses. In the absence of action potentials or applied depolarization PNPs sometimes appeared spontaneously. 5. Peri-internodal application of Rb+ also produced evoked and spontaneous PNPs. These PNPs had longer durations (up to 20 s) than those recorded from K+-loaded internodes. 6. Spontaneous action potentials sometimes appeared during the onset of the PNP, suggesting that PNPs are associated with depolarization of the underlying axon. 7. Passage of current pulses during the PNP demonstrated that the PNP is associated with an increased conductance of the pathway linking the peri-internodal recording site to the bath. At least part of this conductance increase occurs across the internodal axolemma, since peri-internodally recorded action potentials evoked during the PNP had larger amplitudes than those evoked before or after the PNP. 8. PNPs were suppressed by tetraethylammonium (TEA, 10-20 mM) and by 4-aminopyridine (1 mM). 9. These results suggest that the PNPs recorded in K+- or Rb+-loaded myelin sheaths are produced by a regenerative K+ or Rb+ current that enters the internodal axolemma via K+ channels opened by action potentials or subthreshold depolarizations. 10. When normal extracellular [K+] was preserved (by using Na+ rather than K+ salts in the peri-internodal electrode), action potentials recorded within the myelin sheath were instead followed by a brief, positive after-potential that was inhibited by TEA. This finding suggests that action potentials can also activate internodal K+ channels under normal ionic conditions.

Original languageEnglish
Pages (from-to)177-202
Number of pages26
JournalJournal of Physiology
Volume472
StatePublished - Dec 1 1993

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Action Potentials
Axons
Potassium
Myelin Sheath
Microelectrodes
Electrodes
Baths
4-Aminopyridine
Phrenic Nerve
Tetraethylammonium
Fluorescent Dyes
Nerve Fibers
Membrane Potentials
Coloring Agents
Salts
Staining and Labeling

ASJC Scopus subject areas

  • Physiology

Cite this

Activation of internodal potassium conductance in rat myelinated axons. / David, Gavriel; Barrett, John; Barrett, Ellen.

In: Journal of Physiology, Vol. 472, 01.12.1993, p. 177-202.

Research output: Contribution to journalArticle

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