Emergence of Narrowband High Frequency Oscillations from Asynchronous, Uncoupled Neural Firing

Previous experimental studies have demonstrated the emergence of narrowband local field potential oscillations during epileptic seizures in which the underlying neural activity appears to be completely asynchronous. We derive a mathematical model explaining how this counterintuitive phenomenon may occur, showing that a population of independent, completely asynchronous neurons may produce narrowband oscillations if each neuron fires quasi-periodically, without requiring any intrinsic oscillatory cells or feedback inhibition. This quasi-periodicity can occur through cells with similar frequency-current (f-I) curves receiving a similar, high amount of uncorrelated synaptic noise. Thus, this source of oscillatory behavior is distinct from the usual cases (pacemaker cells entraining a network, or oscillations being an inherent property of the network structure), as it requires no oscillatory drive nor any specific network or cellular properties other than cells that repetitively fire with continual stimulus. We also deduce bounds on the degree of variability in neural spike-timing which will permit the emergence of such oscillations, both for action potential- and postsynaptic potential-dominated LFPs. These results suggest that even an uncoupled network may generate collective rhythms, implying that the breakdown of inhibition and high synaptic input often observed during epileptic seizures may generate narrowband oscillations. We propose that this mechanism may explain why so many disparate epileptic and normal brain mechanisms can produce similar high frequency oscillations.