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Brain Advance Access originally published online on April 15, 2009
Brain 2009 132(8):2139-2150; doi:10.1093/brain/awp079
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© 2009 The Author(s)
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Resonance in subthalamo-cortical circuits in Parkinson's disease

Alexandre Eusebio1,2, Alek Pogosyan1, Shouyan Wang3, Bruno Averbeck1, Louise Doyle Gaynor1, Stéphanie Cantiniaux2, Tatiana Witjas2, Patricia Limousin1,4, Jean-Philippe Azulay2 and Peter Brown1

1 Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London, UK 2 Department of Neurology and Movement Disorders, Timone University Hospital, Marseille, France 3 Hearing and Balance Centre, Institute of Sound and Vibration Research, University of Southampton, UK 4 Unit of Functional Neurosurgery, Institute of Neurology, Queen Square, London, UK

Correspondence to: Peter Brown, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, 33 Queen Square, London, WC1N 3BG, UK E-mail: p.brown{at}ion.ucl.ac.uk

Neuronal activity within and across the cortex and basal ganglia is pathologically synchronized, particularly at ~ 20 Hz in patients with Parkinson's disease. Defining how activities in spatially distributed brain regions overtly synchronize in narrow frequency bands is critical for understanding disease processes like Parkinson's disease. To address this, we studied cortical responses to electrical stimulation of the subthalamic nucleus (STN) at various frequencies between 5 and 30 Hz in two cohorts of eight patients with Parkinson's disease from two different surgical centres. We found that evoked activity consisted of a series of diminishing waves with a peak latency of 21 ms for the first wave in the series. The cortical evoked potentials (cEPs) averaged in each group were well fitted by a damped oscillator function (r ≥0.9, P < 0.00001). Fits suggested that the natural frequency of the subthalamo-cortical circuit was around 20 Hz. When the system was forced at this frequency by stimulation of the STN at 20 Hz, the undamped amplitude of the modelled cortical response increased relative to that with 5 Hz stimulation in both groups (P ≤ 0.005), consistent with resonance. Restoration of dopaminergic input by treatment with levodopa increased the damping of oscillatory activity (as measured by the modelled damping factor) in both patient groups (P ≤0.001). The increased damping would tend to limit resonance, as confirmed in simulations. Our results show that the basal ganglia–cortical network involving the STN has a tendency to resonate at ~ 20 Hz in Parkinsonian patients. This resonance phenomenon may underlie the propagation and amplification of activities synchronized around this frequency. Crucially, dopamine acts to increase damping and thereby limit resonance in this basal ganglia–cortical network.

Key Words: synchronization; basal ganglia; resonance; Parkinson's disease; deep brain stimulation

Abbreviations: cEP, cortical evoked potential; DBS, deep brain stimulation; MRI, magnetic resonance imaging; STN, subthalamic nucleus; UPDRS, Unified Parkinson's Disease Rating Scale

Received October 1, 2008. Revised March 2, 2009. Accepted March 4, 2009.


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