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The Journal of Neuroscience, July 9, 2008, 28(28):7143-7152; doi:10.1523/JNEUROSCI.1486-08.2008

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Behavioral/Systems/Cognitive
Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia

Bogdan Draganski,^1 * Ferath Kherif,^1 * Stefan Klöppel,^1,3,4 Philip A. Cook,⁵ Daniel C. Alexander,² Geoff J. M. Parker,⁶ Ralf Deichmann,^1,7 John Ashburner,¹ and Richard S. J. Frackowiak^1,8,9

¹Wellcome Trust Centre for Neuroimaging, Institute of Neurology, UCL, London WC1N 3BG, United Kingdom, ²Center for Medical Image Computing and Department of Computer Science, UCL, London WC1E 6BT, United Kingdom, ³Department of Neurology, Neurozentrum, and ⁴Department of Psychiatry, University Clinic Freiburg, 79106 Freiburg, Germany, ⁵Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, ⁶Imaging Science and Biomedical Engineering, University of Manchester, Manchester M13 9PL, United Kingdom, ⁷Brain Imaging Center, University Hospital Frankfurt, 60596 Frankfurt, Germany, ⁸Département d'Études Cognitives, Ecole Normale Supérieure, 75005 Paris, France, and ⁹Laboratory of Neuroimaging, Instituto di Ricovero e Cura a Carattere Scientifico Santa Lucia, 00179 Rome, Italy

Correspondence should be addressed to Dr. Bogdan Draganski, Wellcome Trust Centre for Neuroimaging, 12 Queen Square, London WC1N 3BG, UK. Email: b.draganski{at}fil.ion.ucl.ac.uk

Detailed knowledge of the anatomy and connectivity pattern of cortico-basal ganglia circuits is essential to an understanding of abnormal cortical function and pathophysiology associated with a wide range of neurological and neuropsychiatric diseases. We aim to study the spatial extent and topography of human basal ganglia connectivity in vivo. Additionally, we explore at an anatomical level the hypothesis of coexistent segregated and integrative cortico-basal ganglia loops. We use probabilistic tractography on magnetic resonance diffusion weighted imaging data to segment basal ganglia and thalamus in 30 healthy subjects based on their cortical and subcortical projections. We introduce a novel method to define voxel-based connectivity profiles that allow representation of projections from a source to more than one target region. Using this method, we localize specific relay nuclei within predefined functional circuits. We find strong correlation between tractography-based basal ganglia parcellation and anatomical data from previously reported invasive tracing studies in nonhuman primates. Additionally, we show in vivo the anatomical basis of segregated loops and the extent of their overlap in prefrontal, premotor, and motor networks. Our findings in healthy humans support the notion that probabilistic diffusion tractography can be used to parcellate subcortical gray matter structures on the basis of their connectivity patterns. The coexistence of clearly segregated and also overlapping connections from cortical sites to basal ganglia subregions is a neuroanatomical correlate of both parallel and integrative networks within them. We believe that this method can be used to examine pathophysiological concepts in a number of basal ganglia-related disorders.

Key words: basal ganglia; thalamus; diffusion weighted imaging (DWI); white matter; connectivity; cortex

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Received Feb. 5, 2008; revised May 21, 2008; accepted May 28, 2008.

Correspondence should be addressed to Dr. Bogdan Draganski, Wellcome Trust Centre for Neuroimaging, 12 Queen Square, London WC1N 3BG, UK. Email: b.draganski{at}fil.ion.ucl.ac.uk

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