Mechanism of spontaneous and self-sustained oscillations in networks connected through axo-axonal gap junctions

Electrical coupling of clusters of neurons via axo-axonal gap junctions is a candidate mechanism underlying the ultra-fast (> 100 Hz) oscillations recorded in various in vitro and in vivo normal and pathological conditions [Traub et al. (1999) Neuroscience, 92, 407-426]. The poor characterization of axo-axonal gap junctions, however, limits experimental verification of this mechanism. We simulated networks of prototype multi-compartmental neurons in order to identify the parameters constraining the production and frequency of ultra-fast oscillations. Weak axo-axonal coupling was found to synchronize networks preferentially at the gamma-range frequency (30-100 Hz). Networks with strong axo-axonal coupling were able to produce 200 Hz oscillations, a finding we extended with several new observations. Ultra-fast oscillations arose spontaneously during dendritic excitation, i.e. in the absence of extrinsic axonal background spikes, as the spike trigger zone concomitantly shifted from soma to axon. The all-or-none oscillations could be transitory or self-sustained, and lasted longer in larger networks. They occurred more likely during low to modest soma firing rates, as strong afterhyperpolarizing currents tended to impair them. The rate of the rhythm was independent of network size and of the level of excitation, but inversely proportional to the distance of the junctions from the soma. As a matter of fact, the resulting axonal firing rate was the highest one at which antidromic spikes would not collide with spikes reflected from the soma. Taken together, the observed model dynamics lends further credibility to axo-axonal coupling as a mechanism of ultra-fast oscillations.