Abstract
High-frequency oscillation (HFO) up to 600 Hz in grouped neurons have been observed in the brain areas of vertebrates and central nerve system of invertebrates. Many studies indicate electrical synapses play key roles. With the participation of chemical synapses, neuronal oscillation can be easily generated either by computer simulation or real electrophysiological measurement. However, many reports indicate that HFO is independent of chemical synapse, but depend on gap junction and intrinsic properties of ion channels of participating neurons. Although several mechanisms have been suggested from computer simulations, no one has been verified in real neurons. It is even difficult to understand how HFO is initiated. Here we demonstrate how a paired-spike induces HFO in a gap-junction-coupled network which formed a closed loop and contained only three cells. Furthermore, HFO up to 626 Hz in an electrically coupled network of crayfish was also displayed without the involvement of chemical synapses. In fact, the oscillation only depends on weakly-coupled gap junctions and associated behaviors of spike propagation during refractory period of preceding action potential. For initiating oscillations, it is absolutely essential that the second spike is elicited during the refractory period. Even a spike is elicited; it suffers from slow propagation speed and a tendency for failure through low conductance junctions. Thus, paired-spikes with a short spike interval induce only one trans-junctional spike. At distant synaptic sites, two trans-junctional spikes are triggered because the spike interval increases with spike propagation. Consequently, trans-junctional spikes collide in a gap-junction-coupled network. The remaining single spike reverberates in a loop that serves as an oscillation centre. Since HFO is generated by spike reverberation in a closed loop. The oscillating frequency is decided by the spike traveling time through the closed loop of oscillating center. Further analysis by both simulation and electrophysiological experiment indicated that a simple insertion of spike into the oscillating spikes was verified being able to terminate the paired-spike-elicited HFO. This simple method might provide a valuable hint for the treatment of epilepsy.