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      Subthalamic nucleus phase–amplitude coupling correlates with motor impairment in Parkinson’s disease

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          Highlights

          • We obtained invasive subthalamic nucleus recordings in 33 Parkinson’s disease patients.

          • Phase–amplitude coupling between beta band and high-frequency oscillations correlates with severity of motor impairments.

          • Parkinsonian pathophysiology is more closely linked with low-beta band frequencies.

          Abstract

          Objective

          High-amplitude beta band oscillations within the subthalamic nucleus are frequently associated with Parkinson’s disease but it is unclear how they might lead to motor impairments. Here we investigate a likely pathological coupling between the phase of beta band oscillations and the amplitude of high-frequency oscillations around 300 Hz.

          Methods

          We analysed an extensive data set comprising resting-state recordings obtained from deep brain stimulation electrodes in 33 patients before and/or after taking dopaminergic medication. We correlated mean values of spectral power and phase–amplitude coupling with severity of hemibody bradykinesia/rigidity. In addition, we used simultaneously recorded magnetoencephalography to look at functional interactions between the subthalamic nucleus and ipsilateral motor cortex.

          Results

          Beta band power and phase–amplitude coupling within the subthalamic nucleus correlated positively with severity of motor impairment. This effect was more pronounced within the low-beta range, whilst coherence between subthalamic nucleus and motor cortex was dominant in the high-beta range.

          Conclusions

          We speculate that the beta band might impede pro-kinetic high-frequency activity patterns when phase–amplitude coupling is prominent. Furthermore, results provide evidence for a functional subdivision of the beta band into low and high frequencies.

          Significance

          Our findings contribute to the interpretation of oscillatory activity within the cortico-basal ganglia circuit.

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          Most cited references32

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          The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors.

          The equation for the magnetic lead field for a given magnetoencephalography (MEG) channel is well known for arbitrary frequencies omega but is not directly applicable to MEG in the quasi-static approximation. In this paper we derive an equation for omega = 0 starting from the very definition of the lead field instead of using Helmholtz's reciprocity theorems. The results are (a) the transpose of the conductivity times the lead field is divergence-free, and (b) the lead field differs from the one in any other volume conductor by a gradient of a scalar function. Consequently, for a piecewise homogeneous and isotropic volume conductor, the lead field is always tangential at the outermost surface. Based on this theoretical result, we formulated a simple and fast method for the MEG forward calculation for one shell of arbitrary shape: we correct the corresponding lead field for a spherical volume conductor by a superposition of basis functions, gradients of harmonic functions constructed here from spherical harmonics, with coefficients fitted to the boundary conditions. The algorithm was tested for a prolate spheroid of realistic shape for which the analytical solution is known. For high order in the expansion, we found the solutions to be essentially exact and for reasonable accuracies much fewer multiplications are needed than in typical implementations of the boundary element methods. The generalization to more shells is straightforward.
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            Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans.

            We test the hypothesis that interaction between the human basal ganglia and cerebral cortex involves activity in multiple functional circuits characterized by their frequency of oscillation, phase characteristics, dopamine dependency and topography. To this end we took recordings from macroelectrodes (MEs) inserted into the subthalamic nucleus (STN) in eight awake patients following functional neurosurgery for Parkinson's disease. An EEG was also recorded, as were the signals from MEs in the globus pallidus interna (GPi) in two of the cases. Coherence between EEG and ME potentials was apparent in three major frequency bands, 2-10 Hz, 10-30 Hz and 70-85 Hz. These rhythmic activities differed in their cortical topography, although coherence was always strongest over the midline. Coherence between EEG and ME potentials in the 70-85 Hz band was only recorded in patients treated with levodopa. Cortical activity phase led that in the basal ganglia in those oscillatory activities with frequencies <30 Hz. In contrast, STN and GPi phase led cortex in the 70-85 Hz band. The temporal differences in the way in which cortical activity led or lagged behind that in STN/GPi were similar, around 20 ms, regardless of the overall direction of information flow and frequency band. We conclude that the basal ganglia may receive multiple cortical inputs at frequencies <30 Hz and, in the presence of dopaminergic activity, produce a high frequency drive back to the cerebral cortex, in particular the supplementary motor area (SMA).
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              Pathophysiology of parkinsonism.

              The motor signs of Parkinson's disease are thought to result in large part from a reduction of the level of dopamine in the basal ganglia. Over the last few years, many of the functional and anatomical consequences of dopamine loss in these structures have been identified, both in the basal ganglia and in related areas in thalamus and cortex. This knowledge has contributed significantly to our understanding of the link between the degeneration of dopamine neurons in the midbrain and the development of parkinsonism. This review discusses the evidence that implicates electrophysiologic changes (including altered discharge rates, increased incidence of burst firing, interneuronal synchrony, oscillatory activity, and altered sensorimotor processing) in basal ganglia, thalamus, and cortex, in parkinsonism. From these studies, parkinsonism emerges as a complex network disorder, in which abnormal activity in groups of neurons in the basal ganglia strongly affects the excitability, oscillatory activity, synchrony and sensory responses of areas of the cerebral cortex that are involved in the planning and execution of movement, as well as in executive, limbic or sensory functions. Detailed knowledge of these changes will help us to develop more effective and specific symptomatic treatments for patients with Parkinson's disease.
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                Author and article information

                Contributors
                Journal
                Clin Neurophysiol
                Clin Neurophysiol
                Clinical Neurophysiology
                Elsevier
                1388-2457
                1872-8952
                1 April 2016
                April 2016
                : 127
                : 4
                : 2010-2019
                Affiliations
                [a ]Wellcome Trust Centre for Neuroimaging, UCL Institute of Neurology, 12 Queen Square, WC1N 3BG London, United Kingdom
                [b ]Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, 33 Queen Square, WC1N 3BG London, United Kingdom
                [c ]Nuffield Department of Clinical Neuroscience, University of Oxford, John Radcliffe Hospital, OX3 9DU Oxford, United Kingdom
                [d ]University Medical Center Groningen, University of Groningen, Hanzeplein 1, 9713 GZ Groningen, The Netherlands
                [e ]Unit of Functional Neurosurgery, UCL Institute of Neurology, Queen Square, WC1N 3BG London, United Kingdom
                [f ]Department of Surgical Sciences, University of Oxford, John Radcliffe Hospital, OX3 9DU Oxford, United Kingdom
                [g ]Medical Research Council Brain Network Dynamics Unit at the University of Oxford, OX3 9DU Oxford, United Kingdom
                Author notes
                [* ]Corresponding author at: Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, WC1N 3BG London, United Kingdom. Tel.: +44 20 3448 4362; fax: +44 20 7813 1420.Wellcome Trust Centre for NeuroimagingInstitute of NeurologyUniversity College London12 Queen SquareWC1N 3BG LondonUnited Kingdom vanwijk.bernadette@ 123456gmail.com
                Article
                S1388-2457(16)00046-8
                10.1016/j.clinph.2016.01.015
                4803022
                26971483
                927fcfee-09db-4249-99e5-d0383f516f72
                © 2016 International Federation of Clinical Neurophysiology. Elsevier Ireland Ltd. All rights reserved.

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

                History
                : 16 January 2016
                Categories
                Article

                Neurology
                dbs, deep brain stimulation,hfo, high-frequency oscillations,lfp, local field potential,meg, magnetoencephalography,pac, phase–amplitude coupling,stn, subthalamic nucleus,updrs, unified parkinson’s disease rating scale,parkinson’s disease,subthalamic nucleus,cross-frequency coupling,beta oscillations,motor system,local field potentials

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