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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 (EPSP KA ) not observed in controls. We report that, in contrast to time-locked spikes generated by EPSP AMPA  in control DGCs, aberrant EPSP KA  are associated with long-lasting plateaus and jittered spikes during single-spike mode firing. This is mediated by a selective voltage-dependent amplification of EPSP KA  through persistent sodium current ( I  NaP ) activation. In control DGCs, a current injection of a waveform mimicking the slow shape of EPSP KA  activates  I  NaP  and generates jittered spikes. Conversely in epileptic rats, blockade of EPSP KA  or  I  NaP  restores the temporal precision of EPSP–spike coupling. Importantly, EPSP KA  not only decrease spike timing precision at recurrent mossy fiber synapses but also at perforant path synapses during synaptic integration through  I  NaP  activation. We conclude that a selective interplay between aberrant EPSP KA  and  I  NaP  severely alters the temporal precision of EPSP–spike coupling in DGCs of chronic epileptic rats.

A Selective Interplay between Aberrant EPSP KA and I NaP Reduces Spike Timing Precision in Dentate Granule Cells of Epileptic Rats