ORIGINAL RESEARCH article

Front. Behav. Neurosci.

Sec. Learning and Memory

Volume 19 - 2025 | doi: 10.3389/fnbeh.2025.1553000

This article is part of the Research TopicTheta rhythm generation in learning and memory: cognitive processes and neurological applicationsView all articles

Theta-gamma coupling: nonlinearity as a universal cross-frequency coupling mechanism

Provisionally accepted
  • University of Florida, Gainesville, United States

The final, formatted version of the article will be published soon.

The Cross Frequency Coupling (CFC) phenomenon is defined as a statistical correlation between characteristic parameters neural oscillations. This study demonstrates and analyzes the nonlinear mechanism of the CFC, with a focus on the coupling between slow and fast oscillations, as a model for theta-gamma coupling. We first discuss the usage of the spectrum/bispectrum CFC measure using experimental data. As a physical paradigm, we propose the concept of a Class II neural population at low activity: neurons fire intermittently, and the time spent in the subthreshold regime is much larger that the duration of an action potential. We verify the emergence of fast oscillations (gamma) using a direct numerical simulations (DNS) of a population of Hodgkin-Huxley neurons [Hodgkin and Huxley, 1952] forced by a slow theta oscillation. To deconstruct the mechanism, we derive a mean field approximation based on a reduction of the Hodgkin-Huxley model to a two-equation leaky-integrate-and-fire (LIF) model. Under theta forcing, mean field model generates gamma oscillations; the solutions exhibit spectrum/bispectrum CFC patterns that agree qualitatively with both the DNS model and experimental data. For the theta-gamma coupling problem, the mean field model may be linearized using an asymptotic expansion. The analytical solution of the linear system describes theta-gamma interaction as a gamma stabilization/destabilization cycle and provides explicit expressions of the gamma amplitude and frequency modulation by theta. The results demonstrate that nonlinearity as a universal/unifying mechanism of all CFC types.

Keywords: cross frequency coupling, theta-gamma interaction, nonlinear neural activity, twoequation leaky integrate and fire, gamma instability

Received: 29 Dec 2024; Accepted: 29 May 2025.

Copyright: © 2025 Sheremet and Qin. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Alex Sheremet, University of Florida, Gainesville, United States

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