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      Discriminating Valid from Spurious Indices of Phase-Amplitude Coupling

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      Author(s): 1 , , 2 , 3
      Publication date (Electronic):
      Journal: eNeuro
      Publisher: Society for Neuroscience
      Keywords: alpha, EEG, gamma, MEG, oscillations, theta

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          Abstract

          Recently there has been a strong interest in cross-frequency coupling, the interaction between neuronal oscillations in different frequency bands. In particular, measures quantifying the coupling between the phase of slow oscillations and the amplitude of fast oscillations have been applied to a wide range of data recorded from animals and humans. Some of the measures applied to detect phase-amplitude coupling have been criticized for being sensitive to nonsinusoidal properties of the oscillations and thus spuriously indicate the presence of coupling. While such instances of spurious identification of coupling have been observed, in this commentary we give concrete examples illustrating cases when the identification of cross-frequency coupling can be trusted. These examples are based on control analyses and empirical observations rather than signal-processing tools. Finally, we provide concrete advice on how to determine when measures of phase-amplitude coupling can be considered trustworthy.

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          The θ-γ neural code.

          John Lisman, Ole Jensen (2013)
          Theta and gamma frequency oscillations occur in the same brain regions and interact with each other, a process called cross-frequency coupling. Here, we review evidence for the following hypothesis: that the dual oscillations form a code for representing multiple items in an ordered way. This form of coding has been most clearly demonstrated in the hippocampus, where different spatial information is represented in different gamma subcycles of a theta cycle. Other experiments have tested the functional importance of oscillations and their coupling. These involve correlation of oscillatory properties with memory states, correlation with memory performance, and effects of disrupting oscillations on memory. Recent work suggests that this coding scheme coordinates communication between brain regions and is involved in sensory as well as memory processes. Copyright © 2013 Elsevier Inc. All rights reserved.
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            Measuring phase-amplitude coupling between neuronal oscillations of different frequencies.

            Adriano B. L. Tort, Robert Komorowski, Howard Eichenbaum … (2010)
            Neuronal oscillations of different frequencies can interact in several ways. There has been particular interest in the modulation of the amplitude of high-frequency oscillations by the phase of low-frequency oscillations, since recent evidence suggests a functional role for this type of cross-frequency coupling (CFC). Phase-amplitude coupling has been reported in continuous electrophysiological signals obtained from the brain at both local and macroscopic levels. In the present work, we present a new measure for assessing phase-amplitude CFC. This measure is defined as an adaptation of the Kullback-Leibler distance-a function that is used to infer the distance between two distributions-and calculates how much an empirical amplitude distribution-like function over phase bins deviates from the uniform distribution. We show that a CFC measure defined this way is well suited for assessing the intensity of phase-amplitude coupling. We also review seven other CFC measures; we show that, by some performance benchmarks, our measure is especially attractive for this task. We also discuss some technical aspects related to the measure, such as the length of the epochs used for these analyses and the utility of surrogate control analyses. Finally, we apply the measure and a related CFC tool to actual hippocampal recordings obtained from freely moving rats and show, for the first time, that the CA3 and CA1 regions present different CFC characteristics.
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              Theta-gamma coupling increases during the learning of item-context associations.

              Adriano B. L. Tort, Robert Komorowski, Joseph Manns … (2009)
              Phase-amplitude cross-frequency coupling (CFC) between theta (4-12 Hz) and gamma (30-100 Hz) oscillations occurs frequently in the hippocampus. However, it still remains unclear whether theta-gamma coupling has any functional significance. To address this issue, we studied CFC in local field potential oscillations recorded from the CA3 region of the dorsal hippocampus of rats as they learned to associate items with their spatial context. During the course of learning, the amplitude of the low gamma subband (30-60 Hz) became more strongly modulated by theta phase in CA3, and higher levels of theta-gamma modulation were maintained throughout overtraining sessions. Furthermore, the strength of theta-gamma coupling was directly correlated with the increase in performance accuracy during learning sessions. These findings suggest a role for hippocampal theta-gamma coupling in memory recall.
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                Author and article information

                Journal
                Journal ID (nlm-ta): eNeuro
                Journal ID (iso-abbrev): eNeuro
                Journal ID (hwp): eneuro
                Journal ID (pmc): eneuro
                Journal ID (publisher-id): eNeuro
                Title: eNeuro
                Publisher: Society for Neuroscience
                ISSN (Electronic): 2373-2822
                Publication date (Electronic preprint): 26 December 2016
                Publication date (Electronic): 16 January 2017
                Publication date Collection: Nov-Dec 2016
                Volume: 3
                Issue: 6
                Electronic Location Identifier: ENEURO.0334-16.2016
                Affiliations
                [1 ]Centre for Human Brain Health, School of Psychology, University of Birmingham , Birmingham B15 2TT, United Kingdom
                [2 ]Department of Experimental Psychology, University of Oxford , OX1 3UD Oxford, United Kingdom
                [3 ]Institute of Neuroscience and Psychology, University of Glasgow , Glasgow G12 8QB, United Kingdom
                Author notes

                The authors declare no competing financial interests.

                Author contributions: O.J., E.S., and H.P. wrote the paper.

                This research was supported by James S. McDonnell Foundation Understanding Human Cognition Collaborative Award 220020448.

                Correspondence should be addressed to Ole Jensen, Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham B15 2TT, UK. E-mail: o.jensen@ 123456bham.ac.uk .
                Author information
                http://orcid.org/0000-0001-8193-8348
                http://orcid.org/0000-0002-7527-8280
                Article
                Publisher ID: eN-OPN-0334-16
                DOI: 10.1523/ENEURO.0334-16.2016
                PMC ID: 5237829
                PubMed ID: 28101528
                SO-VID: 1d906a49-1415-428c-af16-95a3b34f1eb2
                Copyright © Copyright © 2016 Jensen et al.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                Date received : 22 October 2016
                Date revision received : 22 December 2016
                Date accepted : 22 December 2016
                Page count
                Figures: 6, Tables: 0, Equations: 4, References: 41, Pages: 8, Words: 4773
                Funding
                Funded by: James S. McDonnell Foundation (JSMF)
                Award ID: 100000913
                Award ID: 220020448
                Categories
                Subject: 1
                Subject: Opinion
                Subject: Cognition and Behavior
                Custom metadata
                cover-date November/December 2016

                Keywords: alpha,eeg,gamma,meg,oscillations,theta
                Data availability:
                Keywords: alpha, eeg, gamma, meg, oscillations, theta

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