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Transient Depression of Excitatory Synapses on Interneurons Contributes to Epileptiform Bursts During Gamma Oscillations in the Mouse Hippocampal Slice

Roger D. Traub¹, Isabel Pais², Andrea Bibbig¹, Fiona E.N. LeBeau², Eberhard H. Buhl ^2,, Helen Garner², Hannah Monyer³ and Miles A. Whittington²

¹Departments of Physiology and Pharmacology, and Neurology, State University of New York Downstate Medical Center, Brooklyn, New York; ²School of Biomedical Sciences, The Worsley Building, University of Leeds, Leeds, United Kingdom; and ³Department of Clinical Neurobiology, University Hospital of Neurology, Heidelberg, Germany

Submitted 20 January 2005; accepted in final form 18 February 2005

Persistent gamma frequency (30–70 Hz) network oscillations occur in hippocampal slices under conditions of metabotropic glutamate receptor (mGluR) activation. Excessive mGluR activation generated a bistable pattern of network activity during which epochs of gamma oscillations of increasing amplitude were terminated by synchronized bursts and very fast oscillations (>70 Hz). We provide experimental evidence that, during this behavior, pyramidal cell-to-interneuron synaptic depression takes place, occurring spontaneously during the gamma rhythm and associated with the onset of epileptiform bursts. We further provide evidence that excitatory postsynaptic potentials (EPSPs) in pyramidal cells are potentiated during the interburst gamma oscillation. When these two types of synaptic plasticity are incorporated, phenomenologically, into a network model previously shown to account for many features of persistent gamma oscillations, we find that epochs of gamma do indeed alternate with epochs of very fast oscillations and epileptiform bursts. Thus the same neuronal network can generate either gamma oscillations or epileptiform bursts, in a manner depending on the degree of network drive and network-induced fluctuations in synaptic efficacies.

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