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

Abstract

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.

Update on the mechanisms and roles of high‐frequency oscillations in seizures and epileptic disorders

“…However, recent work has shown that HFOs can be generated even in the absence of any network connectivity. 26 These results were recently proven analytically 15 , and though they may seem counterintuitive to the neuroscience and HFO community, they are a well-known phenomenon in complex dynamics. Essentially, a synchronous discharge from an ensemble of cells (which results in a local field potential) does not require any network synchrony or coupling at all, only that the neurons be actively firing at similar frequencies (Fig.…”

“…1). 10,[13][14][15][16] Synchronization of fast firing within the population of interconnected neurons leads to the formation of an episode of high-frequency population spikes, which is extracellularly recorded as an HFO event ( Fig. 1A,B).…”

Redaction of false high frequency oscillations due to muscle artifact improves specificity to epileptic tissue

“…The mechanisms producing this fast activity are intriguing, as they appear to require fast firing of many action potentials, indicating a highly active local network (Bragin, et al 2011;Fink, et al 2015;Foffani, et al 2007;Ibarz, et al 2010;Shamas, et al 2018). However, it is not necessary for these phenomena to produce a true coherent oscillation, as the firing cells do not have to be synchronized (Fink, et al 2015;Gliske, et al 2017;Jiruska, et al 2010;Shamas, et al 2018). In terms of detection algorithms, this means that HFOs that are potentially epileptic may have broadband frequency content extending to at least 500 Hz (Blanco, et al 2011;Blanco, et al 2010).…”

How do we use in vitro models to understand epileptiform and ictal activity? A report of the TASK1‐WG4 group of the ILAE/AES Joint Translational Task Force

“…E) . It is believed that FRs are generated by the out‐of‐phase action potential firing of small neuronal populations, each generating spikes at a much lower frequency . This out‐of‐phase firing then results in a multiplication of the frequency, which in extracellular recording manifests as an oscillation in the FR band.…”