GABA-Enhanced Collective Behavior in Neuronal Axons Underlies Persistent Gamma-Frequency Oscillations

Gamma (30-80 Hz) oscillations occur in mammalian electroencephalogram in a manner that indicates cognitive relevance. In vitro models of gamma oscillations demonstrate two forms of oscillation: one occurring transiently and driven by discrete afferent input and the second occurring persistently in r...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2003-09, Vol.100 (19), p.11047-11052
Main Authors: Traub, R. D., Cunningham, M. O., Gloveli, T., LeBeau, F. E. N., Bibbig, A., Buhl, E. H., Whittington, M. A.
Format: Article
Language:English
Subjects:
Animals
Axons
Biological Sciences
Dendrites
gamma-Aminobutyric Acid - physiology
Gap junctions
In Vitro Techniques
Interneurons
Mammalia
Neurons
Neurons - physiology
Neuroscience
Plexus
Pyramidal cells
Rats
Rats, Sprague-Dawley
Receptors
Receptors, GABA-A - physiology
Synapses
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Summary:Gamma (30-80 Hz) oscillations occur in mammalian electroencephalogram in a manner that indicates cognitive relevance. In vitro models of gamma oscillations demonstrate two forms of oscillation: one occurring transiently and driven by discrete afferent input and the second occurring persistently in response to activation of excitatory metabotropic receptors. The mechanism underlying persistent gamma oscillations has been suggested to involve gap-junctional communication between axons of principal neurons, but the precise relationship between this neuronal activity and the gamma oscillation has remained elusive. Here we demonstrate that gamma oscillations coexist with high-frequency oscillations (>90 Hz). High-frequency oscillations can be generated in the axonal plexus even when it is physically isolated from pyramidal cell bodies. They were enhanced in networks by nonsomatic γ-aminobutyric acid type A (GABAA) receptor activation, were modulated by perisomatic GABAAreceptor-mediated synaptic input to principal cells, and provided the phasic input to interneurons required to generate persistent gamma-frequency oscillations. The data suggest that high-frequency oscillations occurred as a consequence of random activity within the axonal plexus. Interneurons provide a mechanism by which this random activity is both amplified and organized into a coherent network rhythm.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1934854100