Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice

• Published in: The Journal of physiology 1997-08, Vol.502 (Pt 3), p.591-607
• Main Authors: Whittington, Miles A., Stanford, Ian M., Colling, Simon B., Jefferys, John G. R., Traub, Roger D.
• Format: Article
• Language: English
• Subjects: Action Potentials - drug effects; Action Potentials - physiology; Animals; Electric Stimulation; Electrophysiology; Excitatory Amino Acid Antagonists - pharmacology; Hippocampus - cytology; Hippocampus - physiology; Interneurons - chemistry; Interneurons - physiology; Male; Organ Culture Techniques; Periodicity; Potassium - pharmacology; Pyramidal Cells - chemistry; Pyramidal Cells - physiology; Quinoxalines - pharmacology; Rats; Rats, Sprague-Dawley; Receptors, AMPA - antagonists & inhibitors; Receptors, AMPA - physiology
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1111/j.1469-7793.1997.591bj.x

1. We used transverse and longitudinal rat hippocampal slices to study the synchronization of gamma frequency (> 20 Hz) oscillations, across distances of up to 4.5 mm. gamma oscillations were evoked in the CA1 region by tetanic stimulation at one or two sites simultaneously, and were associated with population spikes. Tetanic stimuli that were strong enough to induce oscillations were associated with depolarization of both pyramidal cells and interneurones, largely produced by activation of metabotropic glutamate receptors. 2. Computer simulations of gamma oscillations were also performed in a model with pyramidal cells and interneurones, arranged in a chain of five cell groups. This model had suggested previously that interneurone networks alone could generate synchronous gamma oscillations locally, but that pyramidal cell firing, by inducing spike doublets in interneurones, was necessary for the occurrence of highly correlated oscillations with small phase lag (< 2.5 ms), in a distributed network possessing long axon conduction delays. 3. In both experiment and model, pyramidal cell spikes occurred in phase with local population spikes, as did the first spike of the interneurone doublet. 4. The conductance of the interneurone alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) receptor-mediated conductance was manipulated in the model, while the relation between oscillations at opposite ends of the chain was examined. When the conductance was large enough for doublet firing to be synaptically induced in interneurones, oscillation phase lags were < 2.25 ms across the chain. As predicted, experimental blockade of AMPA receptors resulted in increased phase lags between two sites oscillating simultaneously, compared with control conditions. 5. Both in model and in experiment, when stimuli to the two ends of the network were slightly different, cross-network synchronization occurred with a shorter phase lag at high frequencies than at lower frequencies. 6. These data suggest that, while interneurone networks alone can generate locally synchronized gamma oscillations, firing of pyramidal cells, and the synaptically induced doublet firing in interneurones, contribute to the stability and tight synchrony of the oscillations in distributed networks.