Induction of high-frequency oscillations in a junction-coupled network.

Rhythmic oscillations of up to 600 Hz in grouped neurons frequently occur in the brains of animals. These high-frequency oscillations can be sustained in calcium-free conditions and may be blocked by gap junction blockers, implying a key role for electrical synapses in oscillation generation. Mathematical theories have been developed to demonstrate oscillations mediated by electrical synapses without chemical modulation; however, these models have not been verified in animals. Here we report that oscillations of up to 686 Hz are induced by paired spikes of short spike intervals (SIs) in a junction-coupled network. To initiate oscillations, it was essential that the second spike was elicited during the relative refractory period. The second spike suffered from slow propagation speed and failure to transmit through a low-conductance junction. Thus, at the spike initiation site, paired spikes of short SIs triggered one transjunctional spike in the postsynaptic neuron. At distant synaptic sites, two transjunctional spikes were produced as the SI increased during spike propagation. Consequently, spike collision of these asymmetrical transjunctional spikes occurred in the interconnected network. The remaining single spike reverberated in a network serving as an oscillator center. Paired-spike-induced oscillations were modeled by computer simulation and verified electrophysiologically in a network that mediates the tail-flip escape response of crayfish.