Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus

Julian P. Meeks, Xiaoping Jiang, Steven Mennerick

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Abstract

Although action potential initiation and propagation are fundamental to nervous system function, there are few direct electrophysiological observations of propagating action potentials in small unmyelinated fibres, such as the axons within mammalian hippocampus. To circumvent limitations of previous studies that relied on extracellular stimulation, we performed dual recordings: whole-cell recordings from hippocampal CA3 pyramidal cell somas and extracellular recordings from their axons, up to 800 μm away. During brief spike trains under normal conditions, axonal spikes were more resistant to amplitude reduction than somatic spikes. Axonal amplitude depression was greatest at the axon initial segment < 150 μm from the soma, and initiation occurred ∼75 μm from the soma. Allhough prior studies, which failed to verify spike initiation, suggested substantial axonal depression during seizure-associated extracellular K+ ([K+]o) rises, we found that 8 mM [K+]o caused relatively small decreases in axonal spike amplitude during brief spike trains. However, during sustained, epileptiform spiking induced in 8 mM [K+]o, axonal waveforms decreased significantly in peak amplitude. During epileptiform spiking, bursts of two or more action potentials > 20 Hz failed to propagate in most cases. In normal [K+]o at 25 and 32°C, spiking superimposed on sustained somatic depolarization, but not spiking alone, produced similar axonal changes as the epileptiform activity. These results highlight the likely importance of steady-state inactivation of axonal channels in maintaining action potential fidelity. Such changes in axonal propagation properties could encode information and/or serve as an endogenous brake on seizure propagation.

Original languageEnglish (US)
Pages (from-to)425-441
Number of pages17
JournalJournal of Physiology
Volume566
Issue number2
DOIs
StatePublished - Jul 15 2005

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ASJC Scopus subject areas

  • Physiology

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