Theta-gamma cascades and running speed

Abstract

Oscillations in the hippocampal local field potential at theta and gamma frequencies are prominent during awake behavior and have demonstrated several behavioral correlates. Both oscillations have been observed to increase in amplitude and frequency as a function of running speed. Previous investigations, however, have examined the relationship between speed and each of these oscillation bands separately. Based on energy cascade models where “…perturbations of slow frequencies cause a cascade of energy dissipation at all frequency scales” (Buzsaki G. Rhythms of the Brain, 2006), we hypothesized that cross-frequency interactions between theta and gamma should increase as a function of speed. We examined these relationships across multiple layers of the CA1 subregion, which correspond to synaptic zones receiving different afferents. Across layers, we found a reliable correlation between the power of theta and the power of gamma, indicative of an amplitude-amplitude relationship. Moreover, there was an increase in the coherence between the power of gamma and the phase of theta, demonstrating increased phase-amplitude coupling with speed. Finally, at higher velocities, phase entrainment between theta and gamma increases. These results have important implications and provide new insights regarding how theta and gamma are integrated for neuronal circuit dynamics, with coupling strength determined by the excitatory drive within the hippocampus. Specifically, rather than arguing that different frequencies can be attributed to different psychological processes, we contend that cognitive processes occur across multiple frequency bands simultaneously with organization occurring as a function of the amount of energy iteratively propagated through the brain. NEW & NOTEWORTHY Often, the theta and gamma oscillations in the hippocampus have been believed to be a consequence of two marginally overlapping phenomena. This perspective, however, runs counter to an alternative hypothesis in which a slow-frequency, high-amplitude oscillation provides energy that cascades into higher frequency, lower amplitude oscillations. We found that as running speed increases, all measures of cross-frequency theta-gamma coupling intensify, providing evidence in favor of the energy cascade hypothesis.

A Thermodynamic Model of Mesoscale Neural Field Dynamics: Derivation and Linear Analysis

“…Recent investigations of hippocampal LFP in rats show a strong relation between energy input into the hippocampus (as inferred based on rat speed) and the nonlinear character of neural activity [Sheremet et al, 2016b,a, 2019b,a]. Both spectra and bispectra are well ordered with input power, as parameterized by rat speed.…”

“…If the latter were true, then collective activity would be indeed at most of a secondary concern. However, as observations and hypotheses accumulate that contradict the “multiplexing” model, such as the degeneracy and role of turbulence and self-organized criticality in collective neural activity (e.g., Edelman, 1987, Edelman and Gally, 2001, Beggs and Plenz, 2003, Shew et al, 2011, Beggs and Timma, 2012, Sheremet et al, 2018a, 2019b and others), or perhaps simply due to the growing interest in mesoscale processes, the capabilities of the Wilson and Cowan [1972a, 1973] model are bound to undergo further scrutiny.…”

“…However, waves generated in a single brain region are never confined in a single scale, but always corresponds to a spectrum spanning at least the domain from 1 Hz – 300 Hz. The dynamics of the spectral distribution of energy in a hippocampus LFP raises a number of questions (e.g., Sheremet et al, 2017, 2018a, 2019b) that cannot be addressed directly using the current formulations. While the value of the Wilson and Cowan [1972a, 1973] formulation is beyond dispute, a number of small changes are needed to address the problem of the spectral evolution.…”

Cell type, sub-region, and layer-specific speed representation in the hippocampal–entorhinal circuit

“…Hippocampal CA1 gamma power and frequency also increase as a function of running speed [42][43][44] . Accordingly, the stratum lacunosum-moleculare of the CA1 region has been shown to exhibit a strong positive correlation between theta-gamma coupling and running speed 45 , suggesting that the speed signal of theta-modulated gamma inputs are conveyed from the entorhinal cortex to the hippocampus 46,47 . Consistent with this notion, the majority of speed cells in the MEC are suggested to encode speed prospectively, whereas those in the hippocampus are suggested to encode speed retrospectively 10 .…”

Decoding Adaptive Visuomotor Behavior Mediated by Non-linear Phase Coupling in Macaque Area MT

“…Bicoherence is an advanced signal processing technique capable of tracking the neuronal non-linearity and non-Gaussian signals underlying brain functions (Bullock et al, 1997;Darvas et al, 2009;Li et al, 2009Li et al, , 2013. Many studies has shown that this technique can quantify the strength of non-linear phase-phase CFC [i.e., quadratic phase coupling (QPC)] between frequency components of the LFP signal (von Stein et al, 2000;Wang et al, 2007;Darvas et al, 2009;Sheremet et al, 2019). The neural generators of QPC have been reported for object coding in single neuron, in which different features of an object (e.g., size and angular speed) are encoded by a multiplicative process (Gabbiani et al, 2002).…”