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The Journal of Neuroscience, January 7, 2004, 24(1):197-206; doi:10.1523/JNEUROSCI.4845-03.2004

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Cellular/Molecular
Selective Effects of Potassium Elevations on Glutamate Signaling and Action Potential Conduction in Hippocampus

Julian P. Meeks and Steven Mennerick

Departments of Psychiatry and Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110

High-frequency synaptic transmission is depressed by moderate rises in the extracellular potassium concentration ([K⁺]_o). Previous reports have indicated that depression of action potential signaling may underlie the synaptic depression. Here, we investigated the specific contribution of K⁺-induced action potential changes to synaptic depression. We found that glutamatergic transmission in the hippocampal area CA1 was significantly depressed by 8-10 mM [K⁺]_o, but that GABAergic transmission remained intact. Riluzole, a drug that slows recovery from inactivation of voltage-gated sodium channels (NaChs), interacts with subthreshold [K⁺]_o to depress afferent volleys and EPSCs strongly. Thus, elevated [K⁺]_o likely depresses synapses by slowing NaCh recovery from inactivation. It is unclear from previous studies whether [K⁺]_o-induced action potential depression is caused by changes in initiation, reliability, or waveform. We investigated these possibilities explicitly. [K⁺]_o-induced afferent volley depression was independent of stimulus strength, suggesting that changes in action potential initiation do not explain [K⁺]_o-induced depression. Measurements of action potentials from single axons revealed that 8 mM [K⁺]_o increased conduction failures in a subpopulation of fibers and depressed action potential amplitude in all fibers. Together, these changes quantitatively account for the afferent volley depression. We estimate that conduction failure explains more than half of the synaptic depression observed at 8 mM [K⁺]_o, with the remaining depression likely explained by waveform changes. These mechanisms of selective sensitivity of glutamate release to [K⁺]_o accumulation represent a unique neuromodulatory mechanism and a brake on runaway excitation.

Key words: potassium; axon; action potential; propagation; conduction; hippocampus; synapse; CA1

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Received Aug 30, 2003; revised November 17, 2003; accepted November 17, 2003.

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