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The Journal of Neurophysiology Vol. 81 No. 4 April 1999, pp. 1645-1660
Copyright ©1999 by the American Physiological Society
Department of Pharmacology and Cancer Biology and Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710
Okazaki, Maxine M.,
Péter Molnár, and
J. Victor Nadler.
Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents
evoked in presence and absence of seizure-induced growth. A
common feature of temporal lobe epilepsy and of animal models of
epilepsy is the growth of hippocampal mossy fibers into the dentate
molecular layer, where at least some of them innervate granule cells.
Because the mossy fibers are axons of granule cells, the recurrent
mossy fiber pathway provides monosynaptic excitatory feedback to these
neurons that could facilitate seizure discharge. We used the
pilocarpine model of temporal lobe epilepsy to study the synaptic
responses evoked by activating this pathway. Whole cell patch-clamp
recording demonstrated that antidromic stimulation of the mossy fibers
evoked an excitatory postsynaptic current (EPSC) in ~74% of granule
cells from rats that had survived >10 wk after pilocarpine-induced
status epilepticus. Recurrent mossy fiber growth was demonstrated with
the Timm stain in all instances. In contrast, antidromic stimulation of
the mossy fibers evoked an EPSC in only 5% of granule cells studied
4-6 days after status epilepticus, before recurrent mossy fiber growth
became detectable. Notably, antidromic mossy fiber stimulation also
evoked an EPSC in many granule cells from control rats. Clusters of
mossy fiber-like Timm staining normally were present in the inner third
of the dentate molecular layer at the level of the hippocampal
formation from which slices were prepared, and several considerations
suggested that the recorded EPSCs depended mainly on activation of
recurrent mossy fibers rather than associational fibers. In both status epilepticus and control groups, the antidromically evoked EPSC was
glutamatergic and involved the activation of both AMPA/kainate and
N-methyl-D-aspartate (NMDA) receptors. EPSCs
recorded in granule cells from rats with recurrent mossy fiber growth
differed in three respects from those recorded in control granule
cells: they were much more frequently evoked, a number of them were
unusually large, and the NMDA component of the response was generally
much more prominent. In contrast to the antidromically evoked EPSC, the
EPSC evoked by stimulation of the perforant path appeared to be
unaffected by a prior episode of status epilepticus. These results
support the hypothesis that recurrent mossy fiber growth and synapse
formation increases the excitatory drive to dentate granule cells and
thus facilitates repetitive synchronous discharge. Activation of NMDA
receptors in the recurrent pathway may contribute to seizure
propagation under depolarizing conditions. Mossy fiber-granule cell
synapses also are present in normal rats, where they may contribute to
repetitive granule cell discharge in regions of the dentate gyrus where
their numbers are significant.
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