A three-dimensional histological atlas of the human basal ganglia. II. Atlas deformation strategy and evaluation in deep brain stimulation for Parkinson disease

Clinical article

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Object

The localization of any given target in the brain has become a challenging issue because of the increased use of deep brain stimulation to treat Parkinson disease, dystonia, and nonmotor diseases (for example, Tourette syndrome, obsessive compulsive disorders, and depression). The aim of this study was to develop an automated method of adapting an atlas of the human basal ganglia to the brains of individual patients.

Methods

Magnetic resonance images of the brain specimen were obtained before extraction from the skull and histological processing. Adaptation of the atlas to individual patient anatomy was performed by reshaping the atlas MR images to the images obtained in the individual patient using a hierarchical registration applied to a region of interest centered on the basal ganglia, and then applying the reshaping matrix to the atlas surfaces.

Results

Results were evaluated by direct visual inspection of the structures visible on MR images and atlas anatomy, by comparison with electrophysiological intraoperative data, and with previous atlas studies in patients with Parkinson disease. The method was both robust and accurate, never failing to provide an anatomically reliable atlas to patient registration. The registration obtained did not exceed a 1-mm mismatch with the electrophysiological signatures in the region of the subthalamic nucleus.

Conclusions

This registration method applied to the basal ganglia atlas forms a powerful and reliable method for determining deep brain stimulation targets within the basal ganglia of individual patients.

Abbreviations used in this paper: AC-PC = anterior commissure–posterior commissure; DBS = deep brain stimulation; PD = Parkinson disease; ROI = region of interest; RU = red nucleus; SN = substantia nigra; STN = subthalamic nucleus; SW = Schaltenbrand and Wahren.

Article Information

Address correspondence to: Jérôme Yelnik, M.D., Institut National de la Santé et de la Recherche Médicale U679, Hôpital de la Salpêtrière, 47, Boulevard de l'Hôpital, 75013, Paris, France. email: jerome.yelnik@upmc.fr.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Flow chart demonstrating the atlas MR imaging-based hierarchical deformation process. Each hemisphere (blue boxes, first row) is processed independently. Global registration (purple boxes, second row) with the atlas MR images (red box, first row) is followed by automatic ROI extraction (yellow boxes, third row) and local registration (orange boxes, third row). The atlas ROI incorporating the basal ganglia has been extracted once and for all. For the right hemisphere (left side of the figure), the MR image is flipped along the anteroposterior axis before global registration. The resulting transformations are applied to the original atlas surfaces, resulting in surfaces adapted to the patient's brain (orange box, last row).

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    Standardized visual inspection of deformed atlas structures in T1-weighted MR images. Postoperative MR images obtained in 3 patients are shown with superimposed atlas structures. The MR images were resliced along the AC-PC plane together with the contours of atlas structures visible on 3 orthogonal standard planes (sagittal, coronal, and axial): head of the caudate nucleus (CD), anterior and medial part of the putamen (PU), lateral border of the cerebral peduncle (CP), anteroventral part of the optic tract (OT), and medial border of the thalamus including the habenula (THAL). Note the close correspondence between the MR images and the atlas contours.

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    Standardized visual inspection of deformed atlas structures in T2-weighted MR images. The T2-weighted MR image was automatically coregistered with the T1-weighted MR image (used to deform the atlas), thus allowing comparison of STN (pink), SN (black), and RU (red) contours with hypointense areas. Images obtained in 2 patients are presented (left and right boxes). For each case, 2 coronal slices are presented: 1 through the center of RU (C and D), and 1 anterior to RU (A and B). The contours of the putamen and globus pallidus are in blue, that of the cerebral peduncle in fuchsia.

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    Average of spatially normalized MR images obtained in the 20 patients analyzed in this study. The green boxes showing AC-PC normalization, and the red boxes showing atlas normalization. Upper: Anterior, medial, and dorsal slices. Lower: Posterior, lateral, and ventral slices. Only 1 hemisphere is presented (the atlas is deformed independently on the 2 hemispheres). Note that the contours of gray level areas are sharper with atlas normalization. AC = nucleus accumbens; PUv = ventral putamen; VL = lateral ventricle.

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    Comparison between atlas-based STN delimitation and intraoperative microelectrode STN recordings. Left: Axial view of the patient's MR image (top) with left and right STN (transparent pink) and 73 recordings (spheres), and enlargement (bottom) of the left and right STN superimposed with the recordings. Right: Back-projection in the atlas space of 965 microelectrode recordings obtained in 10 patients. Dark blue spheres correspond to STN recordings, black to SN, and light blue to unlabeled data. The STN is shown in 2 orthogonal rotations oriented along the principal axis. Note the good correspondence between the atlas STN and the dark blue spheres. The black spheres are ventral to the STN, in conformity with the ventral position of the SN.

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    Split MR image showing a comparison between the SW atlas and our 3D atlas. Left: One section of the axial SW atlas (PC: 6 mm) was adapted to the MR image of the 3D atlas. The corresponding contours, similar to those in the SW atlas, appear as white tracings. Right: The contours of the 3D atlas, obtained by automatic sectioning of the 3D surfaces, appear as colored tracings. Note that both atlases are globally similar but that the SN and cerebral peduncle are precisely delimited in the 3D atlas while they are not present or incompletely delimited in the SW atlas. FX = anterior column of the fornix; MTT = mamillothalamic tract; PU = putamen.

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    Representative contact localization images obtained in the series of 10 patients with PD who underwent STN DBS. Sagittal slices of MR images obtained in 6 of these patients are illustrated. The therapeutic contact (yellow) is in the STN (pink) in the 5 first cases and at the limit between the zona incerta and Forel field H2 in the later case. Note that cerebral peduncle (fuchsia) and the optic tract (brown) of the 3D atlas are very tightly registered to the corresponding aspect of the MR imaging.

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    Contact localization in the series of 10 patients with PD treated by STN DBS. The 20 contacts (10 on each side represented as spheres) were back-projected onto the atlas. A: The 2 STN (pink) are seen with an axial section of the T2-weighted MR images of the atlas. B: Closer view of the same STN. Contacts localized outside the STN are dark colored; those within the STN are light colored. C and D: Sagittal views of left and right STN with T2-weighted MR images of the atlas.

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