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The Journal of Neuroscience, February 1, 1999, 19(3):1088-1105

On the Mechanism of the    Frequency Shift in Neuronal Oscillations Induced in Rat Hippocampal Slices by Tetanic Stimulation

Roger D. Traub¹, Miles A. Whittington², Eberhard H. Buhl³, John G. R. Jefferys¹, and Howard J. Faulkner²

¹ Department of Physiology, University of Birmingham School of Medicine, Edgbaston, Birmingham B15 2TT, United Kingdom, ² Department of Physiology, Imperial College of Medicine at St. Mary's, London W2 1PG, United Kingdom, and ³ Medical Research Council Anatomical Neuropharmacology Unit, Oxford University, Oxford OX1 3TH, United Kingdom

Tetanic stimulation of the CA1 region of rat hippocampal slices can induce  frequency population oscillations (30-100 Hz) after a latency of 50-150 msec that are synchronized to within 1-2 msec when simultaneous stimuli are delivered to two sites 2 mm or more apart. When tetanic stimuli, twice-threshold for eliciting  oscillations, are used, new phenomena occur. (1) After a period of , there is a switch to  frequencies (10-25 Hz); (2) during the switch, pyramidal cell spike afterhyperpolarizations (AHPs) increase and rhythmic EPSPs occur in pyramidal cells; and (3) after an episode of single-site, twice-threshold-induced / oscillations, simultaneous two-site threshold stimuli induce  oscillations that are locally synchronized, but no longer are capable of long-range synchrony. We studied the cellular mechanisms of the / switch with electrophysiological techniques and computer simulations. Our model predicts that the observed increases in both pyramidal cell AHPs and in pyramidal/pyramidal cell EPSPs are necessary and sufficient for the  switch to occur. Firing patterns generated by the model, both for pyramidal cells and for interneurons, resemble experimental records. A one-site twice-threshold stimulus might lead to an inability of the two sites to synchronize at  frequencies, after subsequent two-site stimulation, via this mechanism. If depression is induced at synapses coupling pyramidal cells at one site to interneurons at the other site, then two-site stimulation cannot produce interneuron doublets; hence, as shown previously, the two sites will be unable to synchronize. This mechanism works in simulations, and we provide experimental evidence that synaptic depression and loss of doublets occur after a sufficiently strong local tetanus to one site. We suggest that long-range excitatory connections onto interneurons determine whether different pyramidal cell "assemblies" can synchronize at  frequencies, whereas excitatory connections onto pyramidal cells determine whether such assemblies can synchronize at  frequencies.

Key words: synaptic plasticity; memory; interneurons; 40 Hz oscillation; hippocampus; EEG

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Copyright © 1999 Society for Neuroscience  0270-6474/99/1931088-18$05.00/0

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