Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks Journal Article


Author(s): Bartos, Marlene; Vida, Imre; Frotscher, Michael; Meyer, Axel; Monyer, Hannah; Geiger, Jörg R; Jonas, Peter
Article Title: Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks
Affiliation
Abstract: 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 parvalbumin 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), respectively (33-34 degrees C). The decay of unitary IPSCs at BC-BC synapses was significantly faster than that at BC-principal cell synapses, indicating 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 models, 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.
Keywords: Animals; Time Factors; Mice; Mice, Transgenic; Green Fluorescent Proteins; Recombinant Fusion Proteins/metabolism; Synapses/metabolism; Luminescent Proteins/metabolism; *Nerve Net; Hippocampus/cytology/metabolism/pathology; Neurons/metabolism/physiology
Journal Title: PNAS
Volume: 99
Issue 20
ISSN: 1091-6490
Publisher: National Academy of Sciences  
Publication Place: United States
Date Published: 2002-01-01
Start Page: 13222
End Page: 13227
DOI: 10.1073/pnas.192233099
Open access: no