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      Cross-Frequency Coupling in Developmental Perspective

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          Abstract

          It is generally assumed that different electroencephalogram (EEG) frequency bands are somehow related to different computational modes in the brain. Integration of these computational modes is reflected in the phenomenon of cross-frequency coupling (CFC). On slow temporal scales, CFC may reflect trait-like properties, which posits a question of its developmental trends. This is the first study that explored source-level CFC measures in a developmental perspective using both cross-sectional and longitudinal designs. CFC measures demonstrated good test-retest stability and proved to be higher in adults in cortical areas participating in sensory-motor integration, response inhibition, and attentional control. In children, greater CFC was observed in parietal regions involved in self-centered cognition. Over the period from 7 to 10 years, CFC demonstrated nonlinear growth trajectories. Introversion was associated with higher CFC in cortical areas related to emotion, attention, and social cognition, implying that the association between introversion and CFC appears early in the development.

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          Most cited references54

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          EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis.

          Evidence is presented that EEG oscillations in the alpha and theta band reflect cognitive and memory performance in particular. Good performance is related to two types of EEG phenomena (i) a tonic increase in alpha but a decrease in theta power, and (ii) a large phasic (event-related) decrease in alpha but increase in theta, depending on the type of memory demands. Because alpha frequency shows large interindividual differences which are related to age and memory performance, this double dissociation between alpha vs. theta and tonic vs. phasic changes can be observed only if fixed frequency bands are abandoned. It is suggested to adjust the frequency windows of alpha and theta for each subject by using individual alpha frequency as an anchor point. Based on this procedure, a consistent interpretation of a variety of findings is made possible. As an example, in a similar way as brain volume does, upper alpha power increases (but theta power decreases) from early childhood to adulthood, whereas the opposite holds true for the late part of the lifespan. Alpha power is lowered and theta power enhanced in subjects with a variety of different neurological disorders. Furthermore, after sustained wakefulness and during the transition from waking to sleeping when the ability to respond to external stimuli ceases, upper alpha power decreases, whereas theta increases. Event-related changes indicate that the extent of upper alpha desynchronization is positively correlated with (semantic) long-term memory performance, whereas theta synchronization is positively correlated with the ability to encode new information. The reviewed findings are interpreted on the basis of brain oscillations. It is suggested that the encoding of new information is reflected by theta oscillations in hippocampo-cortical feedback loops, whereas search and retrieval processes in (semantic) long-term memory are reflected by upper alpha oscillations in thalamo-cortical feedback loops. Copyright 1999 Elsevier Science B.V.
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            The θ-γ neural code.

            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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              Theta-gamma coupling increases during the learning of item-context associations.

              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

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                14 May 2019
                2019
                : 13
                : 158
                Affiliations
                [1] 1Laboratory of Psychophysiology of Individual Differences, Institute of Physiology and Basic Medicine , Novosibirsk, Russia
                [2] 2Humanitarian Department, Novosibirsk State University , Novosibirsk, Russia
                Author notes

                Edited by: Filippo Brighina, University of Palermo, Italy

                Reviewed by: Domenica Veniero, University of Glasgow, United Kingdom; Görsev Yener, Dokuz Eylül University, Turkey; Roberta Lizio, Institute of Research and Medical Care (IRCCS) SDN, Italy

                *Correspondence: Gennady G. Knyazev knyazev@ 123456physiol.ru
                Article
                10.3389/fnhum.2019.00158
                6527755
                31139068
                568c8e9d-67ca-433c-9a92-52f8330450fc
                Copyright © 2019 Knyazev, Savostyanov, Bocharov, Tamozhnikov, Kozlova, Leto and Slobodskaya.

                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) and the copyright owner(s) 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.

                History
                : 20 February 2019
                : 26 April 2019
                Page count
                Figures: 5, Tables: 4, Equations: 2, References: 77, Pages: 10, Words: 7966
                Funding
                Funded by: Russian Science Foundation 10.13039/501100006769
                Funded by: Russian Foundation for Basic Research 10.13039/501100002261
                Categories
                Neuroscience
                Original Research

                Neurosciences
                cross-frequency coupling,eeg,developmental trends,introversion,social anxiety,source-level analysis,growth curve analysis

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