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The Journal of Neuroscience, July 15, 1999, 19(14):5758-5767

Glutamate Receptors Mediate TTX-Resistant Synchronous Activity in the Rat Hippocampus

Ben W. Strowbridge

Department of Neurosciences, Case Western Reserve University, Cleveland, Ohio 44106, and Departments of Neurological Surgery and Physiology/Biophysics, University of Washington, Seattle, Washington 98195

4-Aminopyridine (4-AP) is a well known convulsant that enhances the release of both excitatory and inhibitory neurotransmitters in the CNS. Low concentrations of 4-AP (~100 µM) readily induce synchronized discharges in the hippocampus that are blocked by tetrodotoxin (TTX), suggesting that they require Na⁺-dependent action potentials in addition to the enhanced release of neurotransmitters. However, in the present study we have found that higher concentrations of 4-AP (1 mM) in combination with 5 mM tetraethylammonium (TEA) induce spontaneous synchronized discharges in rat hippocampal slices that are resistant to blockade by TTX. These synchronous discharges are evident in field potential recordings, which progress from the hilus to CA1 at 0.023 ± 0.002 m/sec and in intracellular recordings from the hilar mossy cells and CA3 pyramidal cells. In some slices exposed to 4-AP and TEA, smaller-amplitude asynchronous responses also were recorded. 4-AP-induced spontaneous discharges are blocked by 20 µM DNQX and by 100 µM Cd²⁺ but are resistant to blockade by either 25 µM bicuculline or 25 µM D-APV. These results suggest that the activation of postsynaptic AMPA receptors is necessary to produce TTX-resistant synchronized discharges. The laminar profile of field potentials recorded in CA3 and CA1 suggests that glutamate is released from axons of CA3 pyramidal cells despite the blockade of fast axonal Na⁺ channels by TTX. Synchronous discharges may result from glutamate released at proximal recurrent collaterals after spontaneous Ca²⁺ spikes in CA3 pyramidal cells.

Key words: glutamate; synaptic transmission; hippocampus; epilepsy; axon conduction; AMPA receptors

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19145758-10$05.00/0

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