Individualized parcellation of the subthalamic nucleus in patients with Parkinson's disease with 7T MRI

ABSTRACT Deep brain stimulation of the subthalamic nucleus (STN) is a widely performed surgical treatment for patients with Parkinson's disease. The goal of the surgery is to place an electrode centered in the motor region of the STN while lowering the effects of electrical stimulation on the non‐motor regions. However, distinguishing the motor region from the neighboring associative and limbic areas in individual patients using imaging modalities was until recently difficult to obtain in vivo. Here, using ultra‐high field MR imaging, we have performed a dissection of the subdivisions of the STN of individual Parkinson's disease patients. We have acquired 7 T diffusion‐weighted images of seventeen patients with Parkinson's disease scheduled for deep brain stimulation surgery. Using a structural connectivity‐based parcellation protocol, the STN's connections to the motor, limbic, and associative cortical areas were used to map the individual subdivisions of the nucleus. A reproducible patient‐specific parcellation of the STN into a posterolateral motor and gradually overlapping central associative area was found in all STNs, taking up on average 55.3% and 55.6% of the total nucleus volume. The limbic area was found in the anteromedial part of the nucleus. Our results suggest that 7T MR imaging may facilitate individualized and highly specific planning of deep brain stimulation surgery of the STN. HIGHLIGHTSThe subthalamic nucleus of individual Parkinson patients was parcellated at 7T MRI.A motor zone was found posterolaterally.Associative and limbic zones were found more anteriorly and anteromedially.A gradual overlap of the functional zones was found within the STN.

[1]  G. Sapiro,et al.  Comprehensive in vivo Mapping of the Human Basal Ganglia and Thalamic Connectome in Individuals Using 7T MRI , 2012, PloS one.

[2]  A. Roebroeck,et al.  Ultra-high field magnetic resonance imaging of the basal ganglia and related structures , 2014, Front. Hum. Neurosci..

[3]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[4]  M. Jenkinson.  Non-linear registration aka Spatial normalisation , 2007 .

[5]  L. Tremblay,et al.  The pallidosubthalamic projection: An anatomical substrate for nonmotor functions of the subthalamic nucleus in primates , 2005, Movement disorders : official journal of the Movement Disorder Society.

[6]  S. Haber,et al.  The Organization of Prefrontal-Subthalamic Inputs in Primates Provides an Anatomical Substrate for Both Functional Specificity and Integration: Implications for Basal Ganglia Models and Deep Brain Stimulation , 2013, The Journal of Neuroscience.

[7]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[8]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[9]  Birte U. Forstmann,et al.  Do we need to revise the tripartite subdivision hypothesis of the human subthalamic nucleus (STN)? , 2014, NeuroImage.

[10]  Yong Hoon Lim,et al.  The clinical impact of precise electrode positioning in STN DBS on three-year outcomes , 2013, Journal of the Neurological Sciences.

[11]  Victor Sanchez,et al.  A Randomized Trial of Deep-Brain Stimulation for Parkinson's Disease , 2010 .

[12]  M. Okun,et al.  Management of referred deep brain stimulation failures: a retrospective analysis from 2 movement disorders centers. , 2005, Archives of neurology.

[13]  K. Mewes,et al.  The subthalamic nucleus in Parkinson's disease: somatotopic organization and physiological characteristics. , 2001, Brain : a journal of neurology.

[14]  Y. Agid,et al.  Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior , 2007, Proceedings of the National Academy of Sciences.

[15]  R. Goebel,et al.  7T vs. 4T: RF power, homogeneity, and signal‐to‐noise comparison in head images , 2001, Magnetic resonance in medicine.

[16]  J. Avecillas-Chasin,et al.  Assessment of a method to determine deep brain stimulation targets using deterministic tractography in a navigation system , 2015, Neurosurgical Review.

[17]  A. Lozano,et al.  Direct visualization of deep brain stimulation targets in Parkinson disease with the use of 7-tesla magnetic resonance imaging. , 2010, Journal of neurosurgery.

[18]  John S. Thornton,et al.  High resolution MR anatomy of the subthalamic nucleus: Imaging at 9.4T with histological validation , 2012, NeuroImage.

[19]  K. Uğurbil,et al.  An Assessment of Current Brain Targets for Deep Brain Stimulation Surgery With Susceptibility-Weighted Imaging at 7 Tesla , 2010, Neurosurgery.

[20]  L. Hazrati,et al.  Functional anatomy of the basal ganglia , 1995 .

[21]  Jeff H. Duyn,et al.  The future of ultra-high field MRI and fMRI for study of the human brain , 2012, NeuroImage.

[22]  G. Deuschl,et al.  Neurostimulation for Parkinson's disease with early motor complications. , 2013, The New England journal of medicine.

[23]  Didier Dormont,et al.  Optimal target localization for subthalamic stimulation in patients with Parkinson disease , 2014, Neurology.

[24]  G. Deuschl,et al.  A randomized trial of deep-brain stimulation for Parkinson's disease. , 2006, The New England journal of medicine.

[25]  D. Bowers,et al.  Cognition and mood in Parkinson's disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: The COMPARE Trial , 2009, Annals of neurology.

[26]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[27]  Hagai Bergman,et al.  Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease. , 2010, Brain : a journal of neurology.

[28]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[29]  B. Forstmann,et al.  Are there three subdivisions in the primate subthalamic nucleus? , 2012, Front. Neuroanat..

[30]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[31]  Chantal François,et al.  Dysfunction of the subthalamic nucleus induces behavioral and movement disorders in monkeys , 2009, Movement disorders : official journal of the Movement Disorder Society.

[32]  Daniel L. Polders,et al.  Signal to noise ratio and uncertainty in diffusion tensor imaging at 1.5, 3.0, and 7.0 Tesla , 2011, Journal of magnetic resonance imaging : JMRI.

[33]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[34]  Essa Yacoub,et al.  High-field fMRI unveils orientation columns in humans , 2008, Proceedings of the National Academy of Sciences.

[35]  Richard S. Frackowiak,et al.  Confirmation of functional zones within the human subthalamic nucleus: Patterns of connectivity and sub-parcellation using diffusion weighted imaging , 2012, NeuroImage.

[36]  H. Steinbusch,et al.  The functional role of the subthalamic nucleus in cognitive and limbic circuits , 2005, Progress in Neurobiology.

[37]  Andrew G Webb,et al.  Quantitative assessment of the effects of high‐permittivity pads in 7 Tesla MRI of the brain , 2012, Magnetic resonance in medicine.

[38]  D. Louis Collins,et al.  Symmetric Atlasing and Model Based Segmentation: An Application to the Hippocampus in Older Adults , 2006, MICCAI.

[39]  Richard S. Frackowiak,et al.  Do we need to revise the tripartite subdivision hypothesis of the human subthalamic nucleus (STN)? Response to Alkemade and Forstmann , 2015, NeuroImage.

[40]  B. M. ter Haar Romeny,et al.  Structural and Resting State Functional Connectivity of the Subthalamic Nucleus: Identification of Motor STN Parts and the Hyperdirect Pathway , 2012, PloS one.