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Computer simulation of action potentials and afterpotentials in mammalian myelinated axons: the case for a lower resistance myelin sheath

Blight, A.R.

Neuroscience 15(1): 13-31

1985


ISSN/ISBN: 0306-4522
PMID: 2409473
DOI: 10.1016/0306-4522(85)90119-8
Accession: 005027732

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Depolarizing afterpotentials, recorded in peripheral nerves and spinal axons, were interpreted as representing passive discharge of axolemmal capacitance. This interpretation requires a lower resistance pathway through the myelin sheath than previous measurements suggested. A computer model was used to examine the contribution of the electrical characteristics of nerve fibers to action potential conduction and afterpotential generation. The model consisted of a resistance-capacitance network representing a chain of 20 internodes. The resistances of node internode and myelin sheath were found to produce suitable length and time constants and prolonged afterpotentials, when inserted into the model. Similar length and time constants were found using a conventional model of the axon, based on measurements from isolated peripheral fibers, but this did not reproduce the afterpotentials. Action-potential conduction velocity is enhanced by reducing the time constant and increasing the length constant. The problem of minimizing the internodal time constant was met in the conventional model through the low parallel resistance of the node, while in the new model it was met by reducing the resistance of the myelin sheath. The latter strategy required the nodal leakage resistance to be higher than values from single fiber measurements (.apprx. 250 M.OMEGA. rather than .apprx. 50 M.OMEGA.) to maintain the length constant similar to the conventional model. Simulation of the recorded potentials required the resistance of the myelin lamellae to be .apprx. 100 .OMEGA. cm2. The model quantitatively reproduced the voltage response of the axon to injected current pulses and to propagated action potentials, using Frankenhaeuser-Huxley kinetics. The short duration components of the afterpotential, observed in mammalian recordings, were reproduced by assuming a leakage pathway in the myelin shealth, at the impalement site. The calculated lower resistance of the myelin sheath minimized the effective internodal time constant for a given nodal resistance. This appears to free the myelinated fiber from the alternative requirement for a high modal leakage conductance. It may also contribute to greater stability of the axon under conditions of prolonged depolarization, by allowing the internodal axolemma to be repolarized more rapidly by voltage dependent K+ currents and making the input resistance of the internode dependent on the permeability of its own axolemma, more than that of the surrounding myelin sheath. The storage of charge at the axolemma following the action potential may be of functional significance in modulating excitability.

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