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The Journal of Neuroscience, March 19, 2008, 28(12):3008-3016; doi:10.1523/JNEUROSCI.5295-07.2008

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Behavioral/Systems/Cognitive
Patterns of Bidirectional Communication between Cortex and Basal Ganglia during Movement in Patients with Parkinson Disease

Elodie Lalo,¹ Stéphane Thobois,² Andrew Sharott,⁴ Gustavo Polo,³ Patrick Mertens,³ Alek Pogosyan,⁵ and Peter Brown⁵

¹Laboratory of Motor Activity and Ergonomics, University of Orléans, 45067 Orléans Cedex 2, France, ²Department of Neurology C, Inserm, U864, and ³Department of Neurosurgery, University Lyon I, Hospital for Neurology Pierre Wertheimer, 69003 Lyon, France, ⁴Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany, and ⁵Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, London WCIN 3BG, United Kingdom

Correspondence should be addressed to Prof. Peter Brown, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London WCIN 3BG, UK. Email: p.brown{at}ion.ac.uk

Cortico-basal ganglia networks are considered to comprise several parallel and mostly segregated loops, where segregation is achieved in space through topographic connectivity. Recently, it has been suggested that functional segregation may also be achieved in the frequency domain, by selective coupling of related activities at different frequencies. So far, however, any coupling across frequency in the human has only been modeled in terms of unidirectional influences, a misplaced assumption given the looped architecture of the basal ganglia, and has been considered in static terms. Here, we investigate the pattern of bidirectional coupling between mesial and lateral cortical areas and the subthalamic nucleus (STN) at rest and during movement, with and without pharmacological dopaminergic input, in patients with Parkinson's disease. We simultaneously recorded scalp electroencephalographic activity and local field potentials from depth electrodes and deduced patterns of directed coherence between cortical and STN levels across three frequency bands [sub-β (3–13 Hz), β (14–35 Hz), (65–90 Hz)] in the different states. Our results show (1) asymmetric bidirectional coupling between STN and both mesial and lateral cortical areas with greater drives from cortex to STN at frequencies <35 Hz, (2) a drop of β band coupling driven from mesial cortex to STN during movement, and (3) an increase in symmetrical bidirectional drives between STN and mesial cortex and in lateral cortical drive to STN in the band after dopaminergic therapy. The results confirm a bidirectional pattern of cortico-basal ganglia communication that is differentially patterned across frequency bands and changes with movement and dopaminergic input.

Key words: directed transfer function; cortex; subthalamic nucleus; basal ganglia; Parkinson's disease; oscillations

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Received Aug. 28, 2007; revised Jan. 10, 2008; accepted Jan. 18, 2008.

Correspondence should be addressed to Prof. Peter Brown, Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, Queen Square, London WCIN 3BG, UK. Email: p.brown{at}ion.ac.uk

This article has been cited by other articles:

				R. C. Helmich, E. Aarts, F. P. de Lange, B. R. Bloem, and I. Toni Increased Dependence of Action Selection on Recent Motor History in Parkinson's Disease J. Neurosci., May 13, 2009; 29(19): 6105 - 6113. [Abstract] [Full Text] [PDF]

				A. Eusebio, A. Pogosyan, S. Wang, B. Averbeck, L. D. Gaynor, S. Cantiniaux, T. Witjas, P. Limousin, J.-P. Azulay, and P. Brown Resonance in subthalamo-cortical circuits in Parkinson's disease Brain, April 15, 2009; (2009) awp079v1. [Abstract] [Full Text] [PDF]

				A. Moran, H. Bergman, Z. Israel, and I. Bar-Gad Subthalamic nucleus functional organization revealed by parkinsonian neuronal oscillations and synchrony Brain, December 1, 2008; 131(12): 3395 - 3409. [Abstract] [Full Text] [PDF]

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