Abstract

Tetanic stimulation of the CA1 region of rat hippocampal slices can induce γ 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 γ oscillations, are used, new phenomena occur. (1) After a period of γ, there is a switch to β 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 γ/β oscillations, simultaneous two-site threshold stimuli induce γ oscillations that are locally synchronized, but no longer are capable of long-range synchrony. We studied the cellular mechanisms of the γ/β 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 β 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 γ 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 γ frequencies, whereas excitatory connections onto pyramidal cells determine whether such assemblies can synchronize at β frequencies.