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      Working memory revived in older adults by synchronizing rhythmic brain circuits

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      Nature neuroscience

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          Abstract

          Understanding normal brain aging and developing methods to maintain or improve cognition in older adults are major goals of fundamental and translational neuroscience. Here, we show a core feature of cognitive decline - working memory deficits - emerges from disconnected local and long-range circuits instantiated by theta-gamma phase-amplitude codes in temporal cortex and theta phase synchronization across frontotemporal cortex. We developed a noninvasive stimulation procedure for modulating long-range theta interactions in adults aged 60–76 years. After 25 minutes of stimulation, frequency tuned to individual brain network dynamics, we observed a preferential increase in neural synchronization patterns and the return of sender-receiver relationships of information flow within and between frontotemporal regions. The end result was rapid improvement in working memory performance that outlasted a 50-minute post-stimulation period. The results provide insight into the physiological foundations of age-related cognitive impairment and contribute groundwork for future non-pharmacological interventions targeting aspects of cognitive decline.

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          Most cited references74

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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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              Identifying true brain interaction from EEG data using the imaginary part of coherency.

              The main obstacle in interpreting EEG/MEG data in terms of brain connectivity is the fact that because of volume conduction, the activity of a single brain source can be observed in many channels. Here, we present an approach which is insensitive to false connectivity arising from volume conduction. We show that the (complex) coherency of non-interacting sources is necessarily real and, hence, the imaginary part of coherency provides an excellent candidate to study brain interactions. Although the usual magnitude and phase of coherency contain the same information as the real and imaginary parts, we argue that the Cartesian representation is far superior for studying brain interactions. The method is demonstrated for EEG measurements of voluntary finger movement. We found: (a) from 5 s before to movement onset a relatively weak interaction around 20 Hz between left and right motor areas where the contralateral side leads the ipsilateral side; and (b) approximately 2-4 s after movement, a stronger interaction also at 20 Hz in the opposite direction. It is possible to reliably detect brain interaction during movement from EEG data. The method allows unambiguous detection of brain interaction from rhythmic EEG/MEG data.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                22 February 2019
                08 April 2019
                May 2019
                08 October 2019
                : 22
                : 5
                : 820-827
                Affiliations
                Department of Psychological & Brain Sciences, Center for Systems Neuroscience, Cognitive Neuroimaging Center, Center for Research in Sensory Communications and Neural Technology, Boston University, Boston, MA 02215, USA.
                Author notes

                Author contributions

                R.M.G.R. conceived the experiments. R.M.G.R. and J.A.N. conducted the experiments and analyzed the data. R.M.G.R. wrote the paper.

                [* ]Correspondence to: Robert M. G. Reinhart, 677 Beacon St., Rm 312, Boston, MA 02215, rmgr@ 123456bu.edu
                Article
                NIHMS1522405
                10.1038/s41593-019-0371-x
                6486414
                30962628
                41496e3e-eb28-4b30-a3f9-878c60c1a591

                Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

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                Neurosciences
                Neurosciences

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