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J Physiol. 1984 Oct;355:619-33.

Chloride conductance and extracellular potassium concentration interact to modify the excitability of rat optic nerve fibres.


The excitability of developing rat optic nerves has been studied under conditions in which extracellular Cl- was replaced with other anions. In nerves younger than 3 days old, replacing Cl- with propionate or SO4(2-) usually led to spontaneous and repetitive cycling of extracellular K+ concentration ([K+]o). [K+]o reached peaks of 8-12 mM and then fell transiently below the base-line level of 5 mM before increasing again. This cycling behaviour continued, with a wave-length of 1-2 min, for as long as 2 h. Nerves older than 5 days either did not cycle or did so only transiently. Substitution of ten different anions for Cl- indicated that a minimum hydrated radius, between that of BrO3- and HCO3-, was necessary to induce cycling behaviour. Cycling behaviour was abolished by the Na+-channel blocker tetrodotoxin. Reduction of the bath [K+] to 2.5 mM slowed the frequency of spontaneous cycles; a bath [K+] of 1 mM abolished them. When the temperature was lowered, cycle frequency slowed. Substitution of large anions for Cl- enhanced axonal excitability. This was inferred from the prevalence of spontaneous action potentials during cycling behaviour, and from the generation of relatively large evoked increases of [K+]o. Cycling behaviour is hypothesized to result from a repetition of the following three processes: (i) spontaneous axonal firing elicits a gradual increase in [K+]o which increases axonal excitability and facilitates further K+ release, (ii) axonal firing and K+ release are eventually halted by a combination of depolarization block, intracellular Na+ accumulation and hyperpolarization from electrogenic pumping, (iii) recovery of [K+]o to its minimal value depends on active K+ reuptake mediated by a highly stimulated axonal Na+-K+-ATPase. We conclude that a large proportion of the resting membrane conductance of optic nerve fibres is Cl- specific. A high Cl- conductance may stabilize fine central axons against the depolarizing effects of [K+]o increases.

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