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      Replay bursts in humans coincide with activation of the default mode and parietal alpha networks

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          Summary

          Our brains at rest spontaneously replay recently acquired information, but how this process is orchestrated to avoid interference with ongoing cognition is an open question. Here we investigated whether replay coincided with spontaneous patterns of whole-brain activity. We found, in two separate datasets, that replay sequences were packaged into transient bursts occurring selectively during activation of the default mode network (DMN) and parietal alpha networks. These networks are believed to support inwardly oriented attention and inhibit bottom-up sensory processing and were characterized by widespread synchronized oscillations coupled to increases in high frequency power, mechanisms thought to coordinate information flow between disparate cortical areas. Our data reveal a tight correspondence between two widely studied phenomena in neural physiology and suggest that the DMN may coordinate replay bursts in a manner that minimizes interference with ongoing cognition.

          Highlights

          • Replay in humans coincides with activity in specific resting brain networks

          • Clusters of heightened default mode and alpha activity are linked to replay bursts

          • These networks are characterized by highly synchronized brain-wide oscillations

          • High-frequency power bursts are uniquely linked to default mode network activation

          Abstract

          Our brains form stable memory traces by spontaneously replaying recently acquired information. Higgins et al. show that this process coincides with activity in specific resting-state brain networks, with bursts of replay events occurring selectively during clusters of heightened default mode and parietal alpha network activity.

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          Most cited references62

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          A default mode of brain function.

          A baseline or control state is fundamental to the understanding of most complex systems. Defining a baseline state in the human brain, arguably our most complex system, poses a particular challenge. Many suspect that left unconstrained, its activity will vary unpredictably. Despite this prediction we identify a baseline state of the normal adult human brain in terms of the brain oxygen extraction fraction or OEF. The OEF is defined as the ratio of oxygen used by the brain to oxygen delivered by flowing blood and is remarkably uniform in the awake but resting state (e.g., lying quietly with eyes closed). Local deviations in the OEF represent the physiological basis of signals of changes in neuronal activity obtained with functional MRI during a wide variety of human behaviors. We used quantitative metabolic and circulatory measurements from positron-emission tomography to obtain the OEF regionally throughout the brain. Areas of activation were conspicuous by their absence. All significant deviations from the mean hemisphere OEF were increases, signifying deactivations, and resided almost exclusively in the visual system. Defining the baseline state of an area in this manner attaches meaning to a group of areas that consistently exhibit decreases from this baseline, during a wide variety of goal-directed behaviors monitored with positron-emission tomography and functional MRI. These decreases suggest the existence of an organized, baseline default mode of brain function that is suspended during specific goal-directed behaviors.
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            Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.

            An MRI time course of 512 echo-planar images (EPI) in resting human brain obtained every 250 ms reveals fluctuations in signal intensity in each pixel that have a physiologic origin. Regions of the sensorimotor cortex that were activated secondary to hand movement were identified using functional MRI methodology (FMRI). Time courses of low frequency (< 0.1 Hz) fluctuations in resting brain were observed to have a high degree of temporal correlation (P < 10(-3)) within these regions and also with time courses in several other regions that can be associated with motor function. It is concluded that correlation of low frequency fluctuations, which may arise from fluctuations in blood oxygenation or flow, is a manifestation of functional connectivity of the brain.
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              The brain's default mode network.

              The brain's default mode network consists of discrete, bilateral and symmetrical cortical areas, in the medial and lateral parietal, medial prefrontal, and medial and lateral temporal cortices of the human, nonhuman primate, cat, and rodent brains. Its discovery was an unexpected consequence of brain-imaging studies first performed with positron emission tomography in which various novel, attention-demanding, and non-self-referential tasks were compared with quiet repose either with eyes closed or with simple visual fixation. The default mode network consistently decreases its activity when compared with activity during these relaxed nontask states. The discovery of the default mode network reignited a longstanding interest in the significance of the brain's ongoing or intrinsic activity. Presently, studies of the brain's intrinsic activity, popularly referred to as resting-state studies, have come to play a major role in studies of the human brain in health and disease. The brain's default mode network plays a central role in this work.
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                Author and article information

                Contributors
                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                03 March 2021
                03 March 2021
                : 109
                : 5
                : 882-893.e7
                Affiliations
                [1 ]Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK
                [2 ]Wellcome Trust Centre for Neuroimaging, University College London, London, UK
                [3 ]Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK
                [4 ]Center of Functionally Integrative Neuroscience, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
                [5 ]Deepmind, London, UK
                Author notes
                []Corresponding author cameron.higgins@ 123456ohba.ox.ac.uk
                [6]

                These authors contributed equally

                [7]

                Senior author

                [8]

                Lead contact

                Article
                S0896-6273(20)30966-1
                10.1016/j.neuron.2020.12.007
                7927915
                33357412
                175c1151-dd27-40df-949c-b18ef30daeff
                © 2020 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 3 July 2020
                : 15 October 2020
                : 4 December 2020
                Categories
                Article

                Neurosciences
                replay,resting-state networks,default mode network,parietal alpha network
                Neurosciences
                replay, resting-state networks, default mode network, parietal alpha network

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