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. 2012;7(6):e39061.
doi: 10.1371/journal.pone.0039061. Epub 2012 Jun 29.

Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdirect pathway

Ellen J L Brunenberg  1 , Pim Moeskops, Walter H Backes, Claudio Pollo, Leila Cammoun, Anna Vilanova, Marcus L F Janssen, Veerle E R M Visser-Vandewalle, Bart M ter Haar Romeny, Jean-Philippe Thiran, Bram Platel
Affiliations

Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdirect pathway

Ellen J L Brunenberg et al. PLoS One. 2012.

Abstract

Deep brain stimulation (DBS) for Parkinson's disease often alleviates the motor symptoms, but causes cognitive and emotional side effects in a substantial number of cases. Identification of the motor part of the subthalamic nucleus (STN) as part of the presurgical workup could minimize these adverse effects. In this study, we assessed the STN's connectivity to motor, associative, and limbic brain areas, based on structural and functional connectivity analysis of volunteer data. For the structural connectivity, we used streamline counts derived from HARDI fiber tracking. The resulting tracks supported the existence of the so-called "hyperdirect" pathway in humans. Furthermore, we determined the connectivity of each STN voxel with the motor cortical areas. Functional connectivity was calculated based on functional MRI, as the correlation of the signal within a given brain voxel with the signal in the STN. Also, the signal per STN voxel was explained in terms of the correlation with motor or limbic brain seed ROI areas. Both right and left STN ROIs appeared to be structurally and functionally connected to brain areas that are part of the motor, associative, and limbic circuit. Furthermore, this study enabled us to assess the level of segregation of the STN motor part, which is relevant for the planning of STN DBS procedures.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Flowchart of data analysis steps for structural and functional connectivity.
Figure 2
Figure 2. Illustration of the streamline counting per region of interest involved in the calculation of the connectivity measure .
Figure 3
Figure 3. Visualizations of probabilistic fiber tracking results.
(a) Sagittal view from the left. (b) Coronal view from the front. (c) Oblique view. The images show 500 streamlines per seed voxel in the right STN of one subject, color-coded for streamline direction (red  =  left-right, green  =  anterior-posterior, blue  =  inferior-superior). The right STN seed is represented by the white surface, indicated by the white arrow. Abbreviations: acc  =  anterior cingulate cortex, cc  =  corpus callosum, ifg  =  inferior frontal gyrus, phg  =  parahippocampal gyrus, sfg  =  superior frontal gyrus, sma  =  supplementary motor area, stg  =  superior temporal gyrus.
Figure 4
Figure 4. Streamlines from the right and left STN in subject 1, ending in the motor cortex, that do not pass through thalamus, caudate, putamen or globus pallidus.
These streamlines are therefore an indication for the existence of the “hyperdirect” pathway. (a) Coronal view. (b) Sagittal view on streamlines from the right STN. (c) Streamline rendering in 3D, showing an axial plane of the unweighted diffusion image.
Figure 5
Figure 5. Structural connectivity to the motor cortical areas per STN voxel, cumulated over all subjects, in MNI152 atlas space.
(a) Structural connectivity to the total motor cortical areas. (b) Structural connectivity to Brodmann area 4 (primary motor cortex). (c) Structural connectivity to Brodmann area 6 (pre- and supplementary motor cortex). (d) Structural connectivity to the precentral gyrus. Each sphere represents one voxel in atlas space (voxel size 2×2×2 mm) and is color-coded by the formula image connectivity: dark red means low connectivity, while yellow means high connectivity.
Figure 6
Figure 6. Significant functional connectivity clusters for (a) the right and (b) the left atlas-based STN ROIs, shown on three coronal slices of the MNI152 template.
The yellow lines on the axial image on the left-hand side show the position of the coronal slices. Red clusters exhibit positive regression coefficients, while blue clusters yield negative coefficients.
Figure 7
Figure 7. Functional connectivity per STN voxel in atlas space after applying the reverse regression procedure.
(a) Connectivity to motor areas per voxel of the left and right STN, cumulated over all subjects. (b) Connectivity to limbic areas per voxel of the left and right STN, cumulated over all subjects. Each sphere in (a) and (b) represents one voxel and is color-coded by functional connectivity: dark red means low connectivity, while yellow means high connectivity.
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