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The Journal of Neuroscience, January 15, 1999, 19(2):747-758

Dynamic Potassium Channel Distributions during Axonal Development Prevent Aberrant Firing Patterns

Ian Vabnick¹, James S. Trimmer³, Thomas L. Schwarz⁴, S. Rock Levinson⁵, Dipesh Risal¹, and Peter Shrager^{1, 2}

Departments of ¹ Biochemistry and Biophysics and ² Neurobiology and Anatomy, University of Rochester Medical Center, Rochester, New York 14642, ³ Department of Biochemistry and Cell Biology, State University of New York, Stony Brook, New York 11794, ⁴ Department of Molecular and Cellular Physiology, Beckman Center, Stanford University, Stanford, California 94305, and ⁵ Department of Physiology, University of Colorado, Denver, Colorado 80262

The distribution and function of Shaker-related K⁺ channels were studied with immunofluorescence and electrophysiology in sciatic nerves of developing rats. At nodes of Ranvier, Na⁺ channel clustering occurred very early (postnatal days 1-3). Although K⁺ channels were not yet segregated at most of these sites, they were directly involved in action potential generation, reducing duration, and the refractory period. At ~1 week, K⁺ channel clusters were first seen but were within the nodal gap and in paranodes, and only later (weeks 2-4) were they shifted to juxtaparanodal regions. K⁺ channel function was most dramatic during this transition period, with block producing repetitive firing in response to single stimuli. As K⁺ channels were increasingly sequestered in juxtaparanodes, conduction became progressively insensitive to K⁺ channel block. Over the first 3 weeks, K⁺ channel clustering was often asymmetric, with channels exclusively in the distal paranode in ~40% of cases. A computational model suggested a mechanism for the firing patterns observed, and the results provide a role for K⁺ channels in the prevention of aberrant excitation as myelination proceeds during development.

Key words: potassium channels; node of Ranvier; Schwann cell; myelin; axons; development

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Copyright © 1999 Society for Neuroscience  0270-6474/99/192747-12$05.00/0

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