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      Oscillatory dynamics coordinating human frontal networks in support of goal maintenance

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          Abstract

          Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. Here we utilize the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules results in greater frontal network theta phase encoding (4-8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80-150 Hz), which predicts trial-by-trial response times. Theta phase encoding couples with high gamma amplitude during interregional information encoding, suggesting that interregional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

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          Most cited references43

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          Memory, navigation and theta rhythm in the hippocampal-entorhinal system.

          Theories on the functions of the hippocampal system are based largely on two fundamental discoveries: the amnestic consequences of removing the hippocampus and associated structures in the famous patient H.M. and the observation that spiking activity of hippocampal neurons is associated with the spatial position of the rat. In the footsteps of these discoveries, many attempts were made to reconcile these seemingly disparate functions. Here we propose that mechanisms of memory and planning have evolved from mechanisms of navigation in the physical world and hypothesize that the neuronal algorithms underlying navigation in real and mental space are fundamentally the same. We review experimental data in support of this hypothesis and discuss how specific firing patterns and oscillatory dynamics in the entorhinal cortex and hippocampus can support both navigation and memory.
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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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              Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans.

              A fundamental question in neuroscience concerns the relation between the spiking of individual neurons and the aggregate electrical activity of neuronal ensembles as seen in local field potentials (LFPs). Because LFPs reflect both spiking activity and subthreshold events, this question is not simply one of data aggregation. Recording from 20 neurosurgical patients, we directly examined the relation between LFPs and neuronal spiking. Examining 2030 neurons in widespread brain regions, we found that firing rates were positively correlated with broadband (2-150 Hz) shifts in the LFP power spectrum. In contrast, narrowband oscillations correlated both positively and negatively with firing rates at different recording sites. Broadband power shifts were a more reliable predictor of neuronal spiking than narrowband power shifts. These findings suggest that broadband LFP power provides valuable information concerning neuronal activity beyond that contained in narrowband oscillations.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                6 July 2015
                27 July 2015
                September 2015
                01 March 2016
                : 18
                : 9
                : 1318-1324
                Affiliations
                [1 ]Helen Wills Neuroscience Institute, University of California, Berkeley, California, USA
                [2 ]Department of Psychology, University of California, Berkeley, California, USA
                [3 ]Department of Cognitive, Linguistic and Psychological Sciences, Rhode Island, USA
                [4 ]Brown Institute for Brain Science, Brown University, Providence, Rhode Island, USA
                [5 ]Division of Neurology, Department of Veterans Affairs, Martinez, California, USA
                [6 ]Department of Neurology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, California, USA
                [7 ]Departments of Neurological Surgery and Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, California, USA
                [8 ]Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD, USA
                [9 ]Stanford Human Intracranial Cognitive Electrophysiology Program (SHICEP), Department of Neurology and Neurological Sciences, Stanford University
                Author notes
                [* ]Correspondence should be addressed to B.V. ( bradley.voytek@ 123456gmail.com )
                Article
                NIHMS704399
                10.1038/nn.4071
                4551604
                26214371
                1ad14974-1032-43cb-95c2-513b530d2276

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