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Volume 16, Number 20, Issue of October 15, 1996 pp. 6402-6413
Copyright ©1996 Society for Neuroscience

Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model

Received May 5, 1996; revised June 25, 1996; accepted July 31, 1996.

Xiao-Jing Wang1 and György Buzsáki2

1 Physics Department and Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02254, and 2 Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, New Jersey 07102

Fast neuronal oscillations (gamma, 20-80 Hz) have been observed in the neocortex and hippocampus during behavioral arousal. Using computer simulations, we investigated the hypothesis that such rhythmic activity can emerge in a random network of interconnected GABAergic fast-spiking interneurons. Specific conditions for the population synchronization, on properties of single cells and the circuit, were identified. These include the following: (1) that the amplitude of spike afterhyperpolarization be above the GABAA synaptic reversal potential; (2) that the ratio between the synaptic decay time constant and the oscillation period be sufficiently large; (3) that the effects of heterogeneities be modest because of a steep frequency-current relationship of fast-spiking neurons. Furthermore, using a population coherence measure, based on coincident firings of neural pairs, it is demonstrated that large-scale network synchronization requires a critical (minimal) average number of synaptic contacts per cell, which is not sensitive to the network size.

By changing the GABAA synaptic maximal conductance, synaptic decay time constant, or the mean external excitatory drive to the network, the neuronal firing frequencies were gradually and monotonically varied. By contrast, the network synchronization was found to be high only within a frequency band coinciding with the gamma (20-80 Hz) range. We conclude that the GABAA synaptic transmission provides a suitable mechanism for synchronized gamma oscillations in a sparsely connected network of fast-spiking interneurons. In turn, the interneuronal network can presumably maintain subthreshold oscillations in principal cell populations and serve to synchronize discharges of spatially distributed neurons.

Key words: gamma rhythm; hippocampus; interneurons; GABAA; synchronization; computer model




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[Abstract] [Full Text] [PDF]


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I Aradi and I Soltesz
Modulation of network behaviour by changes in variance in interneuronal properties
J. Physiol., January 1, 2002; 538(1): 227 - 251.
[Abstract] [Full Text] [PDF]


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Z. Nusser, L. M. Kay, G. Laurent, G. E. Homanics, and I. Mody
Disruption of GABAA Receptors on GABAergic Interneurons Leads to Increased Oscillatory Power in the Olfactory Bulb Network
J Neurophysiol, December 1, 2001; 86(6): 2823 - 2833.
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J. Neurophysiol.Home page
M. Alkondon and E. X. Albuquerque
Nicotinic Acetylcholine Receptor alpha 7 and alpha 4beta 2 Subtypes Differentially Control GABAergic Input to CA1 Neurons in Rat Hippocampus
J Neurophysiol, December 1, 2001; 86(6): 3043 - 3055.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
R. D. Traub, N. Kopell, A. Bibbig, E. H. Buhl, F. E. N. LeBeau, and M. A. Whittington
Gap Junctions between Interneuron Dendrites Can Enhance Synchrony of Gamma Oscillations in Distributed Networks
J. Neurosci., December 1, 2001; 21(23): 9478 - 9486.
[Abstract] [Full Text] [PDF]


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M.-J. Bourque and A. Kolta
Properties and Interconnections of Trigeminal Interneurons of the Lateral Pontine Reticular Formation in the Rat
J Neurophysiol, November 1, 2001; 86(5): 2583 - 2596.
[Abstract] [Full Text] [PDF]


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E. Bracci, M. Vreugdenhil, S. P. Hack, and J. G. R. Jefferys
Dynamic Modulation of Excitation and Inhibition During Stimulation at Gamma and Beta Frequencies in the CA1 Hippocampal Region
J Neurophysiol, June 1, 2001; 85(6): 2412 - 2422.
[Abstract] [Full Text] [PDF]


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K. Stenkamp, J. M. Palva, M. Uusisaari, S. Schuchmann, D. Schmitz, U. Heinemann, and K. Kaila
Enhanced Temporal Stability of Cholinergic Hippocampal Gamma Oscillations Following Respiratory Alkalosis In Vitro
J Neurophysiol, May 1, 2001; 85(5): 2063 - 2069.
[Abstract] [Full Text] [PDF]


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M. Bartos, I. Vida, M. Frotscher, J. R. P. Geiger, and P. Jonas
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network
J. Neurosci., April 15, 2001; 21(8): 2687 - 2698.
[Abstract] [Full Text] [PDF]


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C. Bou-Flores and A. J. Berger
Gap Junctions and Inhibitory Synapses Modulate Inspiratory Motoneuron Synchronization
J Neurophysiol, April 1, 2001; 85(4): 1543 - 1551.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
C. T. Dickson, G. Biella, and M. de Curtis
Evidence for Spatial Modules Mediated by Temporal Synchronization of Carbachol-Induced Gamma Rhythm in Medial Entorhinal Cortex
J. Neurosci., October 15, 2000; 20(20): 7846 - 7854.
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L. Acsady, I. Katona, F. J. Martinez-Guijarro, G. Buzsaki, and T. F. Freund
Unusual Target Selectivity of Perisomatic Inhibitory Cells in the Hilar Region of the Rat Hippocampus
J. Neurosci., September 15, 2000; 20(18): 6907 - 6919.
[Abstract] [Full Text] [PDF]


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Learn. Mem.Home page
S. Mahon, J.-M. Deniau, S. Charpier, and B. Delord
Role of a Striatal Slowly Inactivating Potassium Current in Short-Term Facilitation of Corticostriatal Inputs: A Computer Simulation Study
Learn. Mem., September 1, 2000; 7(5): 357 - 362.
[Abstract] [Full Text]


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J. A. White, M. I. Banks, R. A. Pearce, and N. J. Kopell
Networks of interneurons with fast and slow gamma -aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm
PNAS, June 23, 2000; (2000) 100124097.
[Abstract] [Full Text]


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R. D. Traub and A. Bibbig
A Model of High-Frequency Ripples in the Hippocampus Based on Synaptic Coupling Plus Axon-Axon Gap Junctions between Pyramidal Neurons
J. Neurosci., March 15, 2000; 20(6): 2086 - 2093.
[Abstract] [Full Text] [PDF]


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J. M. Palva, K. Lamsa, S. E. Lauri, H. Rauvala, K. Kaila, and T. Taira
Fast Network Oscillations in the Newborn Rat Hippocampus In Vitro
J. Neurosci., February 1, 2000; 20(3): 1170 - 1178.
[Abstract] [Full Text] [PDF]


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B. Hutcheon, P. Morley, and M. O Poulter
Developmental change in GABAA receptor desensitization kinetics and its role in synapse function in rat cortical neurons
J. Physiol., January 1, 2000; 522(1): 3 - 17.
[Abstract] [Full Text] [PDF]


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R. H. Joho, C. S. Ho, and G. A. Marks
Increased gamma - and Decreased delta -Oscillations in a Mouse Deficient for a Potassium Channel Expressed in Fast-Spiking Interneurons
J Neurophysiol, October 1, 1999; 82(4): 1855 - 1864.
[Abstract] [Full Text] [PDF]


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C. A. Chapman and J.-C. Lacaille
Cholinergic Induction of Theta-Frequency Oscillations in Hippocampal Inhibitory Interneurons and Pacing of Pyramidal Cell Firing
J. Neurosci., October 1, 1999; 19(19): 8637 - 8645.
[Abstract] [Full Text] [PDF]


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D. D. Mott, Q. Li, M. M. Okazaki, D. A. Turner, and D. V. Lewis
GABAB-Receptor-Mediated Currents in Interneurons of the Dentate-Hilus Border
J Neurophysiol, September 1, 1999; 82(3): 1438 - 1450.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
L. M. d. l. Prida and J. V. Sanchez-Andres
Nonlinear Frequency-Dependent Synchronization in the Developing Hippocampus
J Neurophysiol, July 1, 1999; 82(1): 202 - 208.
[Abstract] [Full Text] [PDF]


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P. Mann-Metzer and Y. Yarom
Electrotonic Coupling Interacts with Intrinsic Properties to Generate Synchronized Activity in Cerebellar Networks of Inhibitory Interneurons
J. Neurosci., May 1, 1999; 19(9): 3298 - 3306.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
F. K. Skinner, L. Zhang, J. L. P. Velazquez, and P. L. Carlen
Bursting in Inhibitory Interneuronal Networks: A Role for Gap-Junctional Coupling
J Neurophysiol, March 1, 1999; 81(3): 1274 - 1283.
[Abstract] [Full Text] [PDF]



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