Gamma Oscillations

Fast synaptic inhibition promotes synchronized

gamma oscillations in hippocampal

interneuron networks

Marlene Bartos*†, Imre Vida†‡, Michael Frotscher‡, Axel Meyer§, Hannah Monyer§, Jo ̈ rg R. P. Geiger*, and Peter Jonas*¶

*Physiologisches Institut and ‡Anatomisches Institut, Universita ̈ t Freiburg, D-79104 Freiburg, Germany; and §Klinische Neurobiologie, JZN, Universita ̈ t Heidelberg, D-69120 Heidelberg, Germany

Edited by Roger A. Nicoll, University of California, San Francisco, CA, and approved July 19, 2002 (received for review April 18, 2002)



Networks of GABAergic interneurons are of critical importance for the generation of gamma frequency oscillations in the brain. To examine the underlying synaptic mechanisms, we made paired recordings from ‘‘basket cells’’ (BCs) in different subfields of hippocampal slices, using transgenic mice that express enhanced green fluorescent protein (EGFP) under the control of the parval- bumin promoter. Unitary inhibitory postsynaptic currents (IPSCs) showed large amplitude and fast time course with mean amplitude- weighted decay time constants of 2.5, 1.2, and 1.8 ms in the dentate gyrus, and the cornu ammonis area 3 (CA3) and 1 (CA1), respec- tively (33–34°C). The decay of unitary IPSCs at BC–BC synapses was significantly faster than that at BC–principal cell synapses, indi- cating target cell-specific differences in IPSC kinetics. In addition, electrical coupling was found in a subset of BC–BC pairs. To examine whether an interneuron network with fast inhibitory synapses can act as a gamma frequency oscillator, we developed an interneuron network model based on experimentally determined properties. In comparison to previous interneuron network mod- els, our model was able to generate oscillatory activity with higher coherence over a broad range of frequencies (20–110 Hz). In this model, high coherence and flexibility in frequency control emerge from the combination of synaptic properties, network structure, and electrical coupling.

Gamma frequency oscillations are thought to be of key importance for higher brain functions, such as feature binding and temporal encoding of information (1–5). Experimental and theoretical evidence suggests that local networks of synaptically connected GABAergic interneurons are critically involved in the generation of these oscillations (6–19). First, perisomatic inhibitory interneurons (basket cells) fire action potentials at high frequency during gamma activity in vivo, with single spikes phase-locked to the oscillations of the field poten- tial (6, 7). Second, pharmacologically isolated networks of inhibitory interneurons in vitro can oscillate at gamma frequency in response to metabotropic glutamate receptor activation (8). Finally, models of mutually connected interneurons generate coherent action potential activity in the gamma frequency range in the presence of a tonic excitatory drive (9–19).




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