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The Journal of Neuroscience, June 7, 2006, 26(23):6318-6329; doi:10.1523/JNEUROSCI.0620-06.2006

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Behavioral/Systems/Cognitive
Changes in Functional Connectivity within the Rat Striatopallidal Axis during Global Brain Activation In Vivo

Peter J. Magill,1 * Alek Pogosyan,2,3 * Andrew Sharott,2,4 * Jozsef Csicsvari,1 J. Paul Bolam,1 and Peter Brown2

1Medical Research Council Anatomical Neuropharmacology Unit, University of Oxford, Oxford, OX1 3TH, United Kingdom, 2Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, London, WC1N 3BG, United Kingdom, 3Sechenov Institute of Evolutionary Physiology and Biochemistry, St. Petersburg 194223, Russia, and 4Institute of Neurophysiology and Pathophysiology, University Hospital Hamburg-Eppendorf, University of Hamburg, 20246 Hamburg, Germany

Correspondence should be addressed to Dr. Peter J. Magill, Medical Research Council Anatomical Neuropharmacology Unit, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK. Email: peter.magill{at}pharm.ox.ac.uk

The functional organization of the basal ganglia (BG) is often defined according to one of two opposing schemes. The first proposes multiple, essentially independent channels of information processing. The second posits convergence and lateral integration of striatal channels at the level of the globus pallidus (GP). We tested the hypothesis that these proposed aspects of functional connectivity within the striatopallidal axis are dynamic and related to brain state. Local field potentials (LFPs) were simultaneously recorded from multiple sites in striatum and GP in anesthetized rats during slow-wave activity (SWA) and during global activation evoked by sensory stimulation. Functional connectivity was inferred from comparative analyses of the internuclear and intranuclear coherence between bipolar derivations of LFPs.

During prominent SWA, as shown in the electrocorticogram and local field potentials in the basal ganglia, intranuclear coherence, and, thus, lateral functional connectivity within striatum or globus pallidus was relatively weak. Furthermore, the temporal coupling of LFPs recorded across these two nuclei involved functional convergence at the level of GP. Global activation, indicated by a loss of SWA, was accompanied by a rapid functional reorganization of the striatopallidal axis. Prominent lateral functional connectivity developed within GP and, to a significantly more constrained spatial extent, striatum. Additionally, functional convergence on GP was no longer apparent, despite increased internuclear coherence.

These data demonstrate that functional connectivity within the BG is highly dynamic and suggest that the relative expression of organizational principles, such as parallel, independent processing channels, striatopallidal convergence, and lateral integration within BG nuclei, is dependent on brain state.

Key words: basal ganglia; striatum; globus pallidus; coherence; local field potentials; convergence


Received Aug. 12, 2005; revised April 11, 2006; accepted April 12, 2006.

Correspondence should be addressed to Dr. Peter J. Magill, Medical Research Council Anatomical Neuropharmacology Unit, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK. Email: peter.magill{at}pharm.ox.ac.uk




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