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      Beyond the Status Quo: A Role for Beta Oscillations in Endogenous Content (Re)Activation

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          Abstract

          Among the rhythms of the brain, oscillations in the beta frequency range (∼13–30 Hz) have been considered the most enigmatic. Traditionally associated with sensorimotor functions, beta oscillations have recently become more broadly implicated in top-down processing, long-range communication, and preservation of the current brain state. Here, we extend and refine these views based on accumulating new findings of content-specific beta-synchronization during endogenous information processing in working memory (WM) and decision making. We characterize such content-specific beta activity as short-lived, flexible network dynamics supporting the endogenous (re)activation of cortical representations. Specifically, we suggest that beta-mediated ensemble formation within and between cortical areas may awake, rather than merely preserve, an endogenous cognitive set in the service of current task demands. This proposal accommodates key aspects of content-specific beta modulations in monkeys and humans, integrates with timely computational models, and outlines a functional role for beta that fits its transient temporal characteristics.

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          Most cited references118

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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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            The importance of mixed selectivity in complex cognitive tasks.

            Single-neuron activity in the prefrontal cortex (PFC) is tuned to mixtures of multiple task-related aspects. Such mixed selectivity is highly heterogeneous, seemingly disordered and therefore difficult to interpret. We analysed the neural activity recorded in monkeys during an object sequence memory task to identify a role of mixed selectivity in subserving the cognitive functions ascribed to the PFC. We show that mixed selectivity neurons encode distributed information about all task-relevant aspects. Each aspect can be decoded from the population of neurons even when single-cell selectivity to that aspect is eliminated. Moreover, mixed selectivity offers a significant computational advantage over specialized responses in terms of the repertoire of input-output functions implementable by readout neurons. This advantage originates from the highly diverse nonlinear selectivity to mixtures of task-relevant variables, a signature of high-dimensional neural representations. Crucially, this dimensionality is predictive of animal behaviour as it collapses in error trials. Our findings recommend a shift of focus for future studies from neurons that have easily interpretable response tuning to the widely observed, but rarely analysed, mixed selectivity neurons.
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              Synaptic theory of working memory.

              It is usually assumed that enhanced spiking activity in the form of persistent reverberation for several seconds is the neural correlate of working memory. Here, we propose that working memory is sustained by calcium-mediated synaptic facilitation in the recurrent connections of neocortical networks. In this account, the presynaptic residual calcium is used as a buffer that is loaded, refreshed, and read out by spiking activity. Because of the long time constants of calcium kinetics, the refresh rate can be low, resulting in a mechanism that is metabolically efficient and robust. The duration and stability of working memory can be regulated by modulating the spontaneous activity in the network.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                21 July 2017
                2 August 2017
                Jul-Aug 2017
                : 4
                : 4
                : ENEURO.0170-17.2017
                Affiliations
                [1 ]Department of Experimental Psychology, University of Oxford , Oxford OX1 3UD, United Kingdom
                [2 ]Department of Neurological Surgery, Columbia University College of Physicians and Surgeons , New York, NY 10032
                [3 ]Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen , Nijmegen 6500 HB, The Netherlands
                Author notes

                The authors declare no competing financial interests.

                Author contributions: B.S. and S.H. wrote the paper.

                This work was supported by Deutsche Forschungsgemeinschaft Grants SP 1510/1-1 and SP 1510/2-1 (to B.S.) and by the NWO Veni Grant 451-14-027 (to S.H.).

                Correspondence should be addressed to either of the following: Bernhard Spitzer, Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom, E-mail: bernardodispitz@ 123456gmail.com ; or Saskia Haegens, Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York, NY 10032, E-mail: shaegens@ 123456gmail.com.
                Author information
                http://orcid.org/0000-0002-9676-6275
                Article
                eN-REV-0170-17
                10.1523/ENEURO.0170-17.2017
                5539431
                28785729
                554c8f7e-db3f-4304-881e-1e35693e622e
                Copyright © 2017 Spitzer and Haegens

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

                History
                : 16 May 2017
                : 14 July 2017
                : 17 July 2017
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 152, Pages: 15, Words: 12196
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG)
                Award ID: 501100001659
                Award ID: SP 1510/2-1
                Funded by: Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)
                Award ID: 501100003246
                Award ID: VENI 451-14-027
                Funded by: Deutsche Forschungsgemeinschaft (DFG)
                Award ID: 501100001659
                Award ID: SP 1510/1-1
                Categories
                1
                1.7
                Review
                Cognition and Behavior
                Custom metadata
                July/August 2017

                beta rhythm,decision making,network interactions,neural oscillations,top-down control,working memory

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