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      Non-motor Characterization of the Basal Ganglia: Evidence From Human and Non-human Primate Electrophysiology

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          Abstract

          Although the basal ganglia have been implicated in a growing list of human behaviors, they include some of the least understood nuclei in the brain. For several decades studies have employed numerous methodologies to uncover evidence pointing to the basal ganglia as a hub of both motor and non-motor function. Recently, new electrophysiological characterization of the basal ganglia in humans has become possible through direct access to these deep structures as part of routine neurosurgery. Electrophysiological approaches for identifying non-motor function have the potential to unlock a deeper understanding of pathways that may inform clinical interventions and particularly neuromodulation. Various electrophysiological modalities can also be combined to reveal functional connections between the basal ganglia and traditional structures throughout the neocortex that have been linked to non-motor behavior. Several reviews have previously summarized evidence for non-motor function in the basal ganglia stemming from behavioral, clinical, computational, imaging, and non-primate animal studies; in this review, instead we turn to electrophysiological studies of non-human primates and humans. We begin by introducing common electrophysiological methodologies for basal ganglia investigation, and then we discuss studies across numerous non-motor domains–emotion, response inhibition, conflict, decision-making, error-detection and surprise, reward processing, language, and time processing. We discuss the limitations of current approaches and highlight the current state of the information.

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          Most cited references130

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          What makes us tick? Functional and neural mechanisms of interval timing.

          Time is a fundamental dimension of life. It is crucial for decisions about quantity, speed of movement and rate of return, as well as for motor control in walking, speech, playing or appreciating music, and participating in sports. Traditionally, the way in which time is perceived, represented and estimated has been explained using a pacemaker-accumulator model that is not only straightforward, but also surprisingly powerful in explaining behavioural and biological data. However, recent advances have challenged this traditional view. It is now proposed that the brain represents time in a distributed manner and tells the time by detecting the coincidental activation of different neural populations.
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            Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway.

            How the motor-related cortical areas modulate the activity of the output nuclei of the basal ganglia is an important issue for understanding the mechanisms of motor control by the basal ganglia. The cortico-subthalamo-pallidal 'hyperdirect' pathway conveys powerful excitatory effects from the motor-related cortical areas to the globus pallidus, bypassing the striatum, with shorter conduction time than effects conveyed through the striatum. We emphasize the functional significance of the 'hyperdirect' pathway and propose a dynamic 'center-surround model' of basal ganglia function in the control of voluntary limb movements. When a voluntary movement is about to be initiated by cortical mechanisms, a corollary signal conveyed through the cortico-subthalamo-pallidal 'hyperdirect' pathway first inhibits large areas of the thalamus and cerebral cortex that are related to both the selected motor program and other competing programs. Then, another corollary signal through the cortico-striato-pallidal 'direct' pathway disinhibits their targets and releases only the selected motor program. Finally, the third corollary signal possibly through the cortico-striato-external pallido-subthalamo-internal pallidal 'indirect' pathway inhibits their targets extensively. Through this sequential information processing, only the selected motor program is initiated, executed and terminated at the selected timing, whereas other competing programs are canceled.
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              Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring.

              Error-related activity in the medial prefrontal cortex (mPFC) is thought to work in conjunction with lateral prefrontal cortex (lPFC) as a part of an action-monitoring network, where errors signal the need for increased cognitive control. The neural mechanism by which this mPFC-lPFC interaction occurs remains unknown. We hypothesized that transient synchronous oscillations in the theta range reflect a mechanism by which these structures interact. To test this hypothesis, we extracted oscillatory phase and power from current-source-density-transformed electroencephalographic data recorded during a Flanker task. Theta power in the mPFC was diminished on the trial preceding an error and increased immediately after an error, consistent with predictions of an action-monitoring system. These power dynamics appeared to take place over a response-related background of oscillatory theta phase coherence. Theta phase synchronization between FCz (mPFC) and F5/6 (lPFC) sites was robustly increased during error trials. The degree of mPFC-lPFC oscillatory synchronization predicted the degree of mPFC power on error trials, and both of these dynamics predicted the degree of posterror reaction time slowing. Oscillatory dynamics in the theta band may in part underlie a mechanism of communication between networks involved in action monitoring and cognitive control.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                05 July 2018
                2018
                : 12
                : 385
                Affiliations
                [1] 1Department of Neuroscience, University of Florida , Gainesville, FL, United States
                [2] 2Department of Neurosurgery, Center for Movement Disorders and Neurorestoration, University of Florida , Gainesville, FL, United States
                [3] 3Department of Neurology, Center for Movement Disorders and Neurorestoration, University of Florida , Gainesville, FL, United States
                [4] 4Department of Biomedical Engineering, University of Florida , Gainesville, FL, United States
                Author notes

                Edited by: Jonathan Miller, University Hospitals Cleveland Medical Center, United States

                Reviewed by: Sabato Santaniello, University of Connecticut, United States; George C. McConnell, Stevens Institute of Technology, United States

                *Correspondence: Aysegul Gunduz agunduz@ 123456bme.ufl.edu

                This article was submitted to Neuroprosthetics, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2018.00385
                6041403
                29403346
                3d7f50fd-4996-4950-b971-dbabb931ec69
                Copyright © 2018 Eisinger, Urdaneta, Foote, Okun and Gunduz.

                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) and the copyright owner(s) 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
                : 05 February 2018
                : 22 May 2018
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 176, Pages: 17, Words: 14339
                Categories
                Neuroscience
                Review

                Neurosciences
                basal ganglia,electrophysiology,non-motor,deep brain stimulation,subthalamic nucleus
                Neurosciences
                basal ganglia, electrophysiology, non-motor, deep brain stimulation, subthalamic nucleus

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