Cross-frequency coupling between neuronal oscillations

doi:10.1016/j.tics.2007.05.003

Trends in Cognitive Sciences

Volume 11, Issue 7, July 2007, Pages 267-269

https://doi.org/10.1016/j.tics.2007.05.003 Get rights and content

Electrophysiological recordings in animals, including humans, are modulated by oscillatory activities in several frequency bands. Little is known about how oscillations in various frequency bands interact. Recent findings from the human neocortex show that the power of fast gamma oscillations (30–150 Hz) is modulated by the phase of slower theta oscillations (5–8 Hz). Given that this coupling reflects a specific interplay between large ensembles of neurons, it is likely to have profound implications for neuronal processing.

Introduction

Oscillatory brain activity in various frequency bands is modulated by a range of cognitive tasks in humans and animals. These oscillations reflect electrophysiological signals produced by large ensembles of synchronized neuronal firing and are measured in humans and other animals using intracranial electrical recordings, electroencephalography or magnetoencephalography. Oscillations in both the theta (5–8 Hz) and gamma (30–150 Hz) bands are modulated during perception and memory tasks, but little is known about how oscillations in these frequency bands interact.

Recently, Canolty et al.[1] conducted a study in which they investigated the relationship between theta and gamma oscillations. They acquired data from five human subjects who had had subdural electrodes implanted intracranially as part of neurosurgical treatment for epilepsy. The authors found that the power (or amplitude) of the fast gamma oscillations was systematically modulated during the course of a theta cycle. In other words, there was a cross-frequency coupling observed as a strong correlation between theta phase and gamma power. This was observed in time-frequency representations of power calculated from traces phase-aligned in the theta band. A full cross-frequency analysis revealed that high frequency power modulations were constrained to the 4–8 Hz theta band. The high frequency coupling was strongest in the 80–150 Hz band.

Although gamma band effects above 80 Hz have not been reported in scalp EEG studies, they have been demonstrated in previous intracranial EEG studies. The observed modulations in cross-frequency interactions correlated positively with theta power over sensors. During the recordings, subjects were performing various cognitive tasks, including passive listening to tones or phonemes, verb generation and auditory working memory. Importantly, the cross-frequency coupling was modulated by these tasks and was observed in a large fraction of the subdural electrodes; it did not appear to be specific to particular neocortical brain regions.

Section snippets

Theta phase-locking to gamma power in various species

The findings of Canolty et al. add to an increasing body of evidence demonstrating cross-frequency interactions between theta phase and the power of gamma oscillations. Such interactions have been identified in in vivo recordings in anesthetized [2] and behaving rats [3]. In monkeys, theta phase to gamma power interactions have been reported in the auditory cortex both during spontaneous and stimulus driven activity [4]. Mormann et al.[5] demonstrated a similar coupling in humans implanted with

How are cross-frequency interactions produced?

From a theoretical point of view, there are several ways in which cross-frequency interactions might occur (Figure 1). The phase-to-power interaction reported by Canolty et al. is, in particular, sensible from a physiological perspective. Consider a network producing spontaneous gamma oscillations in which the excitability of the neurons is modulated by a theta rhythm that either is imposed by another network or emerges from the intrinsic network dynamics. Given that the excitability of the

What is the computational role of theta–gamma interaction?

Several theories have been proposed regarding the computational role of the interplay between oscillations in various frequency bands. For instance, it has been suggested that slow oscillations serve to synchronize networks over long distances. Because of conduction delays, low frequency oscillations, such as the theta rhythm, are particularly suited for this purpose 7, 8. Fast oscillations, such as the gamma rhythm, are thought to synchronize cell assemblies over relatively short spatial

Conclusion

The experimental findings thus far on cross-frequency interactions raise many interesting questions. During which tasks and in which brain areas do such interactions occur? What is the computational purpose of theta–gamma coupling? It might facilitate the transient coordination of local networks on short time scales and integrate multiple networks in disparate locations across longer time scales. Gamma activity might divide theta cycles into discrete temporal segments supporting phase coding.

Acknowledgements

This work was supported by the Volkswagen Foundation Grant I/79876 and Netherlands Organization for Scientific Research Innovative Research Incentive Schemes 864.03.007.

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Trends in Cognitive Sciences

UpdateResearch FocusCross-frequency coupling between neuronal oscillations

Introduction

Section snippets

Theta phase-locking to gamma power in various species

How are cross-frequency interactions produced?

What is the computational role of theta–gamma interaction?

Conclusion

Acknowledgements

Int. J. Psychophysiol.

Neuroscience

Int. J. Psychophysiol.

Int. J. Psychophysiol.

High gamma power is phase-locked to theta oscillations in human neocortex

Science

Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia

J. Neurophysiol.

Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat

J. Neurosci.

An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex

J. Neurophysiol.

Update
Research Focus
Cross-frequency coupling between neuronal oscillations