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The Journal of Neuroscience, November 19, 2003, 23(33):10503-10514

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Behavioral/Systems/Cognitive
Resonant Synchronization in Heterogeneous Networks of Inhibitory Neurons

Reinoud Maex and Erik De Schutter

Laboratory of Theoretical Neurobiology, Born-Bunge Foundation, University of Antwerp, B-2610 Antwerp, Belgium

Brain rhythms arise through the synchronization of neurons and their entrainment in a regular firing pattern. In this process, networks of reciprocally connected inhibitory neurons are often involved, but what mechanism determines the oscillation frequency is not completely understood. Analytical studies predict that the emerging frequency band is primarily constrained by the decay rate of the unitary IPSC. We observed a new phenomenon of resonant synchronization in computer-simulated networks of inhibitory neurons in which the synaptic current has a delayed onset, reflecting finite spike propagation and synaptic transmission times. At the resonant level of network excitation, all neurons fire synchronously and rhythmically with a period approximately four times the mean delay of the onset of the inhibitory synaptic current. The amplitude and decay time constant of the synaptic current have relatively minor effects on the emerging frequency band. By varying the axonal delay of the inhibitory connections, networks with a realistic synaptic kinetics can be tuned to frequencies from 40 to >200 Hz. This resonance phenomenon arises in heterogeneous networks with, on average, as few as five connections per neuron. We conclude that the delay of the synaptic current is the primary parameter controlling the oscillation frequency of inhibitory networks and propose that delay-induced synchronization is a mechanism for fast brain rhythms that depend on intact inhibitory synaptic transmission.

Key words: computer; delayed response; inhibition; network; oscillator; rhythm

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Received July 19, 2003; revised September 24, 2003; accepted September 25, 2003.

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