Modulation of Fibers to Motor Cortex during Thalamic DBS in Tourette Patients Correlates with Tic Reduction

Probabilistic tractography in Tourette syndrome (TS) patients have shown an alteration in the connectivity of the primary motor cortex and supplementary motor area with the striatum and thalamus, suggesting an abnormal connectivity of the cortico-striatum-thalamocortical-pathways in TS. Deep brain stimulation (DBS) of the centromedian nucleus–nucleus ventrooralis internus (CM-Voi complex) in the thalamus is an effective treatment for refractory TS patients. We investigated the connectivity of activated fibers from CM-Voi to the motor cortex and its correlation between these projections and their clinical outcome. Seven patients with TS underwent CM-Voi-DBS surgery and were clinically evaluated preoperatively and six months postoperatively. We performed diffusion tensor imaging to display the activated fibers projecting from the CM-Voi to the different motor cortex regions of interest. These analyses showed that the extent of tic reduction during DBS is associated with the degree of stimulation-dependent connectivity between CM-Voi and the motor cortex, and in particular, an increased density of projections to the presupplementary motor area (preSMA). Non-responder patients displayed the largest amount of active fibers projecting into cortical areas other than motor cortex compared to responder patients. These findings support the notion that an abnormal connectivity of thalamocortical pathways underlies TS, and that modulation of these circuits through DBS could restore the function and reduce symptoms.

[1]  M. Teixeira,et al.  Exploring the clinical outcomes after deep brain stimulation in Tourette syndrome , 2019, Journal of the Neurological Sciences.

[2]  James C Gee,et al.  Learning image-based spatial transformations via convolutional neural networks: A review. , 2019, Magnetic resonance imaging.

[3]  Kara A. Johnson,et al.  Image-based analysis and long-term clinical outcomes of deep brain stimulation for Tourette syndrome: a multisite study , 2019, Journal of Neurology, Neurosurgery, and Psychiatry.

[4]  H. Abe,et al.  A retrospective evaluation of thalamic targeting for tremor deep brain stimulation using high-resolution anatomical imaging with supplementary fiber tractography , 2019, Journal of the Neurological Sciences.

[5]  H. Critchley,et al.  Centrality of prefrontal and motor preparation cortices to Tourette Syndrome revealed by meta-analysis of task-based neuroimaging studies , 2017, NeuroImage: Clinical.

[6]  M. Hallett,et al.  Neurobiology of the Premonitory Urge in Tourette's Syndrome: Pathophysiology and Treatment Implications. , 2017, The Journal of neuropsychiatry and clinical neurosciences.

[7]  G. Fink,et al.  Probabilistic mapping of deep brain stimulation effects in essential tremor , 2016, NeuroImage: Clinical.

[8]  V. Visser-Vandewalle,et al.  DBS in Tourette syndrome: where are we standing now? , 2016, Journal of Neural Transmission.

[9]  M. Hallett,et al.  Tractography patterns of subthalamic nucleus deep brain stimulation. , 2016, Brain : a journal of neurology.

[10]  V. Visser-Vandewalle,et al.  Deep Brain Stimulation for Tourette-Syndrome: A Systematic Review and Meta-Analysis , 2016, Brain Stimulation.

[11]  C. McIntyre,et al.  Tractography Activation Patterns in Dorsolateral Prefrontal Cortex Suggest Better Clinical Responses in OCD DBS , 2016, Front. Neurosci..

[12]  Stamatios N. Sotiropoulos,et al.  An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging , 2016, NeuroImage.

[13]  E. Paulesu,et al.  The anarchic brain in action: the contribution of task-based fMRI studies to the understanding of Gilles de la Tourette syndrome. , 2015, Current opinion in neurology.

[14]  Stamatios N. Sotiropoulos,et al.  Non-parametric representation and prediction of single- and multi-shell diffusion-weighted MRI data using Gaussian processes , 2015, NeuroImage.

[15]  Thomas Foltynie,et al.  Tourette syndrome deep brain stimulation: A review and updated recommendations , 2015, Movement disorders : official journal of the Movement Disorder Society.

[16]  Andrea A Kühn,et al.  Lead-DBS: A toolbox for deep brain stimulation electrode localizations and visualizations , 2015, NeuroImage.

[17]  Pamela Guevara,et al.  Altered structural connectivity of cortico-striato-pallido-thalamic networks in Gilles de la Tourette syndrome , 2014, Brain : a journal of neurology.

[18]  Alexander Münchau,et al.  Altered intrahemispheric structural connectivity in Gilles de la Tourette syndrome☆☆☆ , 2013, NeuroImage: Clinical.

[19]  Alexander Münchau,et al.  The functional anatomy of Gilles de la Tourette syndrome , 2013, Neuroscience & Biobehavioral Reviews.

[20]  H. Benali,et al.  Functional immaturity of cortico-basal ganglia networks in Gilles de la Tourette syndrome. , 2012, Brain : a journal of neurology.

[21]  J. Henderson “Connectomic surgery”: diffusion tensor imaging (DTI) tractography as a targeting modality for surgical modulation of neural networks , 2012, Front. Integr. Neurosci..

[22]  J. Jankovic,et al.  Tourette syndrome: Evolving concepts , 2011, Movement disorders : official journal of the Movement Disorder Society.

[23]  V. Visser-Vandewalle,et al.  Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. , 2011, Brain : a journal of neurology.

[24]  A Münchau,et al.  Altered modulation of intracortical excitability during movement preparation in Gilles de la Tourette syndrome. , 2010, Brain : a journal of neurology.

[25]  Michael E. Behen,et al.  Altered Fronto-Striato-Thalamic Connectivity in Children with Tourette Syndrome Assessed with Diffusion Tensor MRI and Probabilistic Fiber Tracking , 2009, Journal of child neurology.

[26]  Alexander Münchau,et al.  Structural changes in the somatosensory system correlate with tic severity in Gilles de la Tourette syndrome. , 2009, Brain : a journal of neurology.

[27]  C. Kennard,et al.  The role of the pre-supplementary motor area in the control of action , 2007, NeuroImage.

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

[29]  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.

[30]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[31]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[32]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

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

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

[35]  V. Vandewalle,et al.  Stereotactic treatment of Gilles de la Tourette syndrome by high frequency stimulation of thalamus , 1999, The Lancet.

[36]  Bradley S. Peterson,et al.  Course of Tic Severity in Tourette Syndrome: The First Two Decades , 1998, Pediatrics.

[37]  R. Hassler,et al.  [Stereotaxic treatment of tics and inarticulate cries or coprolalia considered as motor obsessional phenomena in Gilles de la Tourette's disease]. , 1970, Revue neurologique.