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Cerebral Cortex Advance Access first published online on August 14, 2009
This version published online on September 9, 2009
Cerebral Cortex, doi:10.1093/cercor/bhp156
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

A Selective Interplay between Aberrant EPSPKA and INaP Reduces Spike Timing Precision in Dentate Granule Cells of Epileptic Rats

Jérôme Epsztein, Elisabetta Sola, Alfonso Represa, Yehezkel Ben-Ari and Valérie Crépel

INMED, INSERM U901, Université de La Méditerranée, Parc scientifique de Luminy, BP 13, 13273, Marseille Cedex 09, France

Address correspondence to Valérie Crépel, INMED, INSERM U901, Université de La Méditerranée, Parc scientifique de Luminy, BP 13, 13273, Marseille Cedex 09, France. Email: crepel{at}inmed.univ-mrs.fr.

Spike timing precision is a fundamental aspect of neuronal information processing in the brain. Here we examined the temporal precision of input–output operation of dentate granule cells (DGCs) in an animal model of temporal lobe epilepsy (TLE). In TLE, mossy fibers sprout and establish recurrent synapses on DGCs that generate aberrant slow kainate receptor–mediated excitatory postsynaptic potentials (EPSPKA) not observed in controls. We report that, in contrast to time-locked spikes generated by EPSPAMPA in control DGCs, aberrant EPSPKA are associated with long-lasting plateaus and jittered spikes during single-spike mode firing. This is mediated by a selective voltage-dependent amplification of EPSPKA through persistent sodium current (INaP) activation. In control DGCs, a current injection of a waveform mimicking the slow shape of EPSPKA activates INaP and generates jittered spikes. Conversely in epileptic rats, blockade of EPSPKA or INaP restores the temporal precision of EPSP–spike coupling. Importantly, EPSPKA not only decrease spike timing precision at recurrent mossy fiber synapses but also at perforant path synapses during synaptic integration through INaP activation. We conclude that a selective interplay between aberrant EPSPKA and INaP severely alters the temporal precision of EPSP–spike coupling in DGCs of chronic epileptic rats.

Key Words: dentate granule cells • INaP • kainate receptors • mossy fiber sprouting • spike timing • temporal lobe epilepsy

Jérôme Epsztein and Elisabetta Sola contributed equally to this work.

The access control for this article has been changed to Oxford Open's publication model.

Received for publication May 18, 2009. Revision received June 22, 2009. Accepted for publication July 8, 2009.


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