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J Neurophysiol (February 23, 2005). doi:10.1152/jn.00069.2005
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Submitted on January 20, 2005
Accepted on February 18, 2005

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. LeBeau2, Eberhard H. Buhl2, Helen Garner2, Hannah Monyer3, and Miles A. Whittington2

1 Physiology, Pharmacology, and Neurology, SUNY Downstate Medical Center, Brooklyn, NY, USA
2 School of Biomedical Sciences, University of Leeds, Leeds, Yorkshire, United Kingdom
3 Clinical Neurobiology, University Hospital of Neurology, Heidelberg, Germany

* To whom correspondence should be addressed. E-mail: roger.traub{at}downstate.edu.

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 EPSPs in pyramidal cells are potentiated during the inter-burst 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 upon the degree of network drive and network-induced fluctuations in synaptic efficacies.




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