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      Phase-amplitude cross-frequency coupling in the human nucleus accumbens tracks action monitoring during cognitive control

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          Abstract

          The Nucleus Accumbens (NAcc) is an important structure for the transfer of information between cortical and subcortical structures, especially the prefrontal cortex and the hippocampus. However, the mechanism that allows the NAcc to achieve this integration is not well understood. Phase-amplitude cross-frequency coupling (PAC) of oscillations in different frequency bands has been proposed as an effective mechanism to form functional networks to optimize transfer and integration of information. Here we assess PAC between theta and high gamma oscillations as a potential mechanism that facilitates motor adaptation. To address this issue we recorded intracranial field potentials directly from the bilateral human NAcc in three patients while they performed a motor learning task that varied in the level of cognitive control needed to perform the task. As in rodents, PAC was observable in the human NAcc, transiently occurring contralateral to a movement following the motor response. Importantly, PAC correlated with the level of cognitive control needed to monitor the action performed. This functional relation indicates that the NAcc is engaged in action monitoring and supports the evaluation of motor programs during adaptive behavior by means of PAC.

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          Most cited references31

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          The role of the medial frontal cortex in cognitive control.

          Adaptive goal-directed behavior involves monitoring of ongoing actions and performance outcomes, and subsequent adjustments of behavior and learning. We evaluate new findings in cognitive neuroscience concerning cortical interactions that subserve the recruitment and implementation of such cognitive control. A review of primate and human studies, along with a meta-analysis of the human functional neuroimaging literature, suggest that the detection of unfavorable outcomes, response errors, response conflict, and decision uncertainty elicits largely overlapping clusters of activation foci in an extensive part of the posterior medial frontal cortex (pMFC). A direct link is delineated between activity in this area and subsequent adjustments in performance. Emerging evidence points to functional interactions between the pMFC and the lateral prefrontal cortex (LPFC), so that monitoring-related pMFC activity serves as a signal that engages regulatory processes in the LPFC to implement performance adjustments.
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            Attentional requirements of learning: Evidence from performance measures

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              Theta-gamma coupling increases during the learning of item-context associations.

              Phase-amplitude cross-frequency coupling (CFC) between theta (4-12 Hz) and gamma (30-100 Hz) oscillations occurs frequently in the hippocampus. However, it still remains unclear whether theta-gamma coupling has any functional significance. To address this issue, we studied CFC in local field potential oscillations recorded from the CA3 region of the dorsal hippocampus of rats as they learned to associate items with their spatial context. During the course of learning, the amplitude of the low gamma subband (30-60 Hz) became more strongly modulated by theta phase in CA3, and higher levels of theta-gamma modulation were maintained throughout overtraining sessions. Furthermore, the strength of theta-gamma coupling was directly correlated with the increase in performance accuracy during learning sessions. These findings suggest a role for hippocampal theta-gamma coupling in memory recall.
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                Author and article information

                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                07 October 2013
                2013
                : 7
                : 635
                Affiliations
                [1] 1Departments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University Magdeburg, Germany
                [2] 2Department of Behavioural Neurology, Leibniz Institute for Neurobiology Magdeburg, Germany
                [3] 3German Center for Neurodegenerative Disease (DZNE) Magdeburg, Germany
                [4] 4Department of Psychology, Helen Wills Neuroscience Institute, University of California Berkeley, Berkeley, CA, USA
                [5] 5Department of Psychology, University of California Berkeley, Berkeley, CA, USA
                Author notes

                Edited by: John J. Foxe, Albert Einstein College of Medicine, USA

                Reviewed by: Peter Lakatos, Hungarian Academy of Sciences, Hungary; Ian C. Fiebelkorn, Princeton University, USA

                *Correspondence: Hermann Hinrichs, Department of Behavioural Neurology, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39120 Magdeburg, Germany e-mail: hermann.hinrichs@ 123456med.ovgu.de

                This article was submitted to the journal Frontiers in Human Neuroscience.

                Article
                10.3389/fnhum.2013.00635
                3791425
                24109448
                d4c8868d-5e60-4dfc-b117-a4aaa65dd1af
                Copyright © 2013 Dürschmid, Zaehle, Kopitzki, Voges, Schmitt, Heinze, Knight and Hinrichs.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 17 May 2013
                : 12 September 2013
                Page count
                Figures: 14, Tables: 4, Equations: 7, References: 39, Pages: 17, Words: 13123
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                phase-amplitude coupling,nucleus accumbens,cognitive control,action monitoring,learning

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