Ma. Whittington et al., SPATIOTEMPORAL PATTERNS OF GAMMA-FREQUENCY OSCILLATIONS TETANICALLY INDUCED IN THE RAT HIPPOCAMPAL SLICE, Journal of physiology, 502(3), 1997, pp. 591-607
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 stro
ng enough to induce oscillations were associated with depolarization o
f both pyramidal cells and interneurones, largely produced by activati
on of metabotropic glutamate receptors. 2. Computer simulations of gam
ma oscillations were also performed in a model with pyramidal cells an
d interneurones, arranged in a chain of five cell groups. This model h
ad suggested previously that interneurone networks alone could generat
e synchronous gamma oscillations locally but that pyramidal cell firin
g, 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 delay
s. 3. In both experiment and model, pyramidal cell spikes occurred in
phase with local population spikes, as did the first spike of the inte
rneurone doublet. 4. The conductance of the interneurone alpha-amino-3
-hyrdroxy-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 cond
uctance was large enough for doublet firing to be synaptically induced
in interneurones, oscillation phase lags were < 2.25 ms across the ch
ain. As predicted, experimental blockade of AMPA receptors resulted in
increased phase lags between two sites oscillating simultaneously, co
mpared with control conditions. 5. Both in model and in experiment, wh
en stimuli to the two ends of the network were slightly different, cro
ss-network synchronization occurred with a shorter phase lag at high f
requencies than at lower frequencies. 6. These data suggest that, whil
e 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.