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      Enhancement of multitasking performance and neural oscillations by transcranial alternating current stimulation

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          Abstract

          Multitasking is associated with the generation of stimulus-locked theta (4–7 Hz) oscillations arising from prefrontal cortex (PFC). Transcranial alternating current stimulation (tACS) is a non-invasive brain stimulation technique that influences endogenous brain oscillations. Here, we investigate whether applying alternating current stimulation within the theta frequency band would affect multitasking performance, and explore tACS effects on neurophysiological measures. Brief runs of bilateral PFC theta-tACS were applied while participants were engaged in a multitasking paradigm accompanied by electroencephalography (EEG) data collection. Unlike an active control group, a tACS stimulation group showed enhancement of multitasking performance after a 90-minute session (F 1,35 = 6.63, p = 0.01, ηp 2 = 0.16; effect size = 0.96), coupled with significant modulation of posterior beta (13–30 Hz) activities (F 1,32 = 7.66, p = 0.009, ηp 2 = 0.19; effect size = 0.96). Across participant regression analyses indicated that those participants with greater increases in frontal theta, alpha and beta oscillations exhibited greater multitasking performance improvements. These results indicate frontal theta-tACS generates benefits on multitasking performance accompanied by widespread neuronal oscillatory changes, and suggests that future tACS studies with extended treatments are worth exploring as promising tools for cognitive enhancement.

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          Most cited references44

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          Alpha-band oscillations, attention, and controlled access to stored information

          Alpha-band oscillations are the dominant oscillations in the human brain and recent evidence suggests that they have an inhibitory function. Nonetheless, there is little doubt that alpha-band oscillations also play an active role in information processing. In this article, I suggest that alpha-band oscillations have two roles (inhibition and timing) that are closely linked to two fundamental functions of attention (suppression and selection), which enable controlled knowledge access and semantic orientation (the ability to be consciously oriented in time, space, and context). As such, alpha-band oscillations reflect one of the most basic cognitive processes and can also be shown to play a key role in the coalescence of brain activity in different frequencies.
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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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              Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation.

              In this paper we demonstrate in the intact human the possibility of a non-invasive modulation of motor cortex excitability by the application of weak direct current through the scalp. Excitability changes of up to 40 %, revealed by transcranial magnetic stimulation, were accomplished and lasted for several minutes after the end of current stimulation. Excitation could be achieved selectively by anodal stimulation, and inhibition by cathodal stimulation. By varying the current intensity and duration, the strength and duration of the after-effects could be controlled. The effects were probably induced by modification of membrane polarisation. Functional alterations related to post-tetanic potentiation, short-term potentiation and processes similar to postexcitatory central inhibition are the likely candidates for the excitability changes after the end of stimulation. Transcranial electrical stimulation using weak current may thus be a promising tool to modulate cerebral excitability in a non-invasive, painless, reversible, selective and focal way.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                31 May 2017
                2017
                : 12
                : 5
                : e0178579
                Affiliations
                [1 ]Department of Neurology, University of California San Francisco, San Francisco, California, United States of America
                [2 ]Neuroscape, University of California San Francisco, San Francisco, California, United States of America
                [3 ]Department of Psychiatry, University of California San Francisco, San Francisco, California, United States of America
                [4 ]Department of Physiology, University of California San Francisco, San Francisco, California, United States of America
                University Medical Center Goettingen, GERMANY
                Author notes

                Competing Interests: I have read the journal's policy and the authors of this manuscript have the following competing interests: A.G. is a scientific advisor for Neuroelectrics, a company that produces a tACS device, and co-founder, shareholder, BOD member, and advisor for Akili Interactive Lab, a company that produces therapeutic video games. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

                • Conceptualization: W-YH TPZ AG.

                • Data curation: W-YH.

                • Formal analysis: W-YH MRvS.

                • Funding acquisition: AG.

                • Investigation: WYH.

                • Methodology: W-YH TPZ AG.

                • Project administration: W-YH.

                • Software: MRvS.

                • Supervision: TPZ.

                • Visualization: W-YH.

                • Writing – original draft: W-YH.

                • Writing – review & editing: TPZ AG.

                Author information
                http://orcid.org/0000-0002-8136-9875
                Article
                PONE-D-17-07279
                10.1371/journal.pone.0178579
                5451121
                28562642
                35e0134c-5f32-44f0-95b1-437ed81dadac
                © 2017 Hsu et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 22 February 2017
                : 15 May 2017
                Page count
                Figures: 3, Tables: 2, Pages: 17
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01MH096861
                Award Recipient :
                This work was supported by the NIH Grant R01MH096861 and Hart Center for Deep Rhythm. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Brain Electrophysiology
                Transcranial Stimulation
                Transcranial Alternating Current Stimulation
                Biology and Life Sciences
                Physiology
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