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The Journal of Neuroscience, September 15, 1999, 19(18):8104-8113

On the Synchronizing Mechanisms of Tetanically Induced Hippocampal Oscillations

Enrico Bracci, Martin Vreugdenhil, Stephen P. Hack, and John G. R. Jefferys

Department of Neurophysiology, Division of Neuroscience, The Medical School, The University of Birmingham, Birmingham B15 2TT, United Kingdom

(30-100 Hz) and  (10-30 Hz) oscillations follow tetanic stimulation in the CA1 region of the rat hippocampal slice. Pyramidal neurons undergo a slow depolarization after the tetanus and generate synchronous action potentials. The slow depolarization was previously attributed to metabotropic glutamate receptor (mGluR) activation. However, we found that this event was mediated by GABA_A receptors, being blocked by bicuculline (50 µM) and accompanied by a dramatic drop in input resistance. Experiments with NMDA and non-NMDA glutamate receptor antagonists revealed that fast synaptic excitation was not necessary for oscillations. IPSPs were strongly depressed during the oscillations. Instead, synchronization was caused by field effects, as shown by: (1) Action potentials of pyramidal neurons proximal (<200 µm) to the stimulation site were often preceded by negative deflections of the intracellular potential that masked a net transmembrane depolarization caused by the population spike. (2) Pyramidal neurons located on the surface of the slice, where field effects are weak, fired repetitively but were not synchronized to the network activity. (3) A moderate decrease (50 mOsm) in artificial CSF (ACSF) osmolality did not affect the slow depolarization but increased oscillation amplitude and duration and recruited previously silent neurons into oscillations. (4) 50 mOsm increase in ACSF osmolality dramatically reduced, or abolished, post-tetanic oscillations. Phasic IPSPs, not detectable in proximal neurons, were present, late in the oscillation, in cells located 200-400 µm from the stimulation site and possibly contributed to slowing the rhythm during the  to  transition.

Key words: rhythms; neuronal networks; hippocampus; depolarizing GABA response; field effect (ephaptic) interactions; neuronal synchronization

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Copyright © 1999 Society for Neuroscience  0270-6474/99/19188104-10$05.00/0

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