Abstract
Despite advances in understanding basic organizational principles of the human basal ganglia, accurate in vivo assessment of their anatomical properties is essential to improve early diagnosis in disorders with corticosubcortical pathology and optimize target planning in deep brain stimulation. Main goal of this study was the detailed topological characterization of limbic, associative, and motor subdivisions of the subthalamic nucleus (STN) in relation to corresponding corticosubcortical circuits. To this aim, we used magnetic resonance imaging and investigated independently anatomical connectivity via white matter tracts next to brain tissue properties. On the basis of probabilistic diffusion tractography we identified STN subregions with predominantly motor, associative, and limbic connectivity. We then computed for each of the nonoverlapping STN subregions the covariance between local brain tissue properties and the rest of the brain using high‐resolution maps of magnetization transfer (MT) saturation and longitudinal (R1) and transverse relaxation rate (R2*). The demonstrated spatial distribution pattern of covariance between brain tissue properties linked to myelin (R1 and MT) and iron (R2*) content clearly segregates between motor and limbic basal ganglia circuits. We interpret the demonstrated covariance pattern as evidence for shared tissue properties within a functional circuit, which is closely linked to its function. Our findings open new possibilities for investigation of changes in the established covariance pattern aiming at accurate diagnosis of basal ganglia disorders and prediction of treatment outcome. Hum Brain Mapp 35:5083–5092, 2014. © 2014 The Authors. Human Brain Mapping Published by Wiley Periodicals, Inc.
Highlights
The steadily growing number of patients treated with deep brain stimulation of basal ganglia structures motivates further in-depth investigation of the anatomy and function of the corticosubcortical circuits
The opposite was observed for connectivity to limbic areas with a maximum reached in the anterior tip of the nucleus, while connectivity to associative areas was highest in the centroinferior portion of the nucleus
subthalamic nucleus (STN) segmentation was consistent with this pattern, with most posterosuperior regions labeled as motor, central as associative, and the most anteromedial as limbic
Summary
The steadily growing number of patients treated with deep brain stimulation of basal ganglia structures motivates further in-depth investigation of the anatomy and function of the corticosubcortical circuits. Experimental and clinical findings confirm the existence of a certain degree of topological specialization within the basal ganglia corresponding to their implication in motor, associative, and limbic functions. Neither invasive animal nor in vivo human imaging studies were able to provide strong empiric evidence for its tripartite organization [for review, see Keuken et al, 2012] or for strict anatomical borders among functional subregions [Haynes and Haber, 2013]. The functional anatomy of basal ganglia can be studied in vivo using magnetic resonance imaging (MRI) under the assumption of topological correspondence between anatomical connectivity patterns and functional subdivisions. Topology estimates of STN anatomical projections based on MRI sensitive to water diffusion suggested a tripartite organization of the STN; this notion was confirmed only in 14 of 24 STNs studied [Lambert et al, 2012]. A recent report using similar methodology reported the existence of a posterior–anterior gradient in STN motor projections rather than clearly delineated partitions [Brunenberg et al, 2012]
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