What's special about task in dystonia? A voxel‐based morphometry and diffusion weighted imaging study

Numerous brain imaging studies have demonstrated structural changes in the basal ganglia, thalamus, sensorimotor cortex, and cerebellum across different forms of primary dystonia. However, our understanding of brain abnormalities contributing to the clinically well‐described phenomenon of task specificity in dystonia remained limited. We used high‐resolution magnetic resonance imaging (MRI) with voxel‐based morphometry and diffusion weighted imaging with tract‐based spatial statistics of fractional anisotropy to examine gray and white matter organization in two task‐specific dystonia forms, writer's cramp and laryngeal dystonia, and two non–task‐specific dystonia forms, cervical dystonia and blepharospasm. A direct comparison between both dystonia forms indicated that characteristic gray matter volumetric changes in task‐specific dystonia involve the brain regions responsible for sensorimotor control during writing and speaking, such as primary somatosensory cortex, middle frontal gyrus, superior/inferior temporal gyrus, middle/posterior cingulate cortex, and occipital cortex as well as the striatum and cerebellum (lobules VI‐VIIa). These gray matter changes were accompanied by white matter abnormalities in the premotor cortex, middle/inferior frontal gyrus, genu of the corpus callosum, anterior limb/genu of the internal capsule, and putamen. Conversely, gray matter volumetric changes in the non–task‐specific group were limited to the left cerebellum (lobule VIIa) only, whereas white matter alterations were found to underlie the primary sensorimotor cortex, inferior parietal lobule, and middle cingulate gyrus. Distinct microstructural patterns in task‐specific and non–task‐specific dystonias may represent neuroimaging markers and provide evidence that these two dystonia subclasses likely follow divergent pathophysiological mechanisms precipitated by different triggers. © 2014 International Parkinson and Movement Disorder Society

[1]  Kevin J. Black,et al.  Putamen volume in idiopathic focal dystonia , 1998, Neurology.

[2]  A Berardelli,et al.  Diffusion tensor imaging in primary cervical dystonia , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[3]  M. Hallett,et al.  Changes in brain anatomy in focal hand dystonia , 2004, Annals of neurology.

[4]  Ritesh A. Ramdhani,et al.  Primary Dystonia: Conceptualizing the Disorder Through a Structural Brain Imaging Lens , 2013, Tremor and other hyperkinetic movements.

[5]  S. Lehéricy,et al.  The functional neuroanatomy of dystonia , 2011, Neurobiology of Disease.

[6]  Christian Gaser,et al.  Bilateral grey-matter increase in the putamen in primary blepharospasm , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[7]  G. M. Contessa,et al.  A Transverse and Longitudinal MR Imaging Voxel-Based Morphometry Study in Patients with Primary Cervical Dystonia , 2010, American Journal of Neuroradiology.

[8]  C. Marsden,et al.  The anatomical basis of symptomatic hemidystonia. , 1985, Brain : a journal of neurology.

[9]  Mark Hallett,et al.  Voxel based morphometry reveals specific gray matter changes in primary dystonia , 2007, Movement disorders : official journal of the Movement Disorder Society.

[10]  C D Marsden,et al.  Botulinum toxin does not reverse the cortical dysfunction associated with writer's cramp. A PET study. , 1997, Brain : a journal of neurology.

[11]  Hans-Christian Jabusch,et al.  Sensorimotor skills and focal dystonia are linked to putaminal grey-matter volume in pianists , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[12]  Alan C. Evans,et al.  Functional Anatomy of Visuomotor Skill Learning in Human Subjects Examined with Positron Emission Tomography , 1996, The European journal of neuroscience.

[13]  J. Gottlieb From Thought to Action: The Parietal Cortex as a Bridge between Perception, Action, and Cognition , 2007, Neuron.

[14]  A. Berardelli,et al.  Abnormal plasticity of sensorimotor circuits extends beyond the affected body part in focal dystonia , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[15]  H. Diener,et al.  Morphometric changes of sensorimotor structures in focal dystonia , 2007, Movement disorders : official journal of the Movement Disorder Society.

[16]  Bogdan Draganski,et al.  “Motor circuit” gray matter changes in idiopathic cervical dystonia , 2003, Neurology.

[17]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[18]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[19]  M. Hallett,et al.  Anatomical correlates of blepharospasm , 2012, Translational Neurodegeneration.

[20]  M. Molinari,et al.  Neuronal plasticity of interrelated cerebellar and cortical networks , 2002, Neuroscience.

[21]  Stefan Klöppel,et al.  Genotype–phenotype interactions in primary dystonias revealed by differential changes in brain structure , 2009, NeuroImage.

[22]  Michael K. Hutchinson,et al.  Striatal morphology correlates with sensory abnormalities in unaffected relatives of cervical dystonia patients , 2009, Journal of Neurology.

[23]  Jacqueline Gottlieb,et al.  Parietal control of attentional guidance: The significance of sensory, motivational and motor factors , 2009, Neurobiology of Learning and Memory.

[24]  J. Vitek Pathophysiology of dystonia: A neuronal model , 2002, Movement disorders : official journal of the Movement Disorder Society.

[25]  Leslie G. Ungerleider,et al.  Experience-dependent changes in cerebellar contributions to motor sequence learning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Rachid Deriche,et al.  Diffusion abnormalities in the primary sensorimotor pathways in writer's cramp. , 2009, Archives of neurology.

[27]  D. Eidelberg,et al.  Hereditary dystonia as a neurodevelopmental circuit disorder: Evidence from neuroimaging , 2011, Neurobiology of Disease.

[28]  H. Voss,et al.  Cerebellothalamocortical Connectivity Regulates Penetrance in Dystonia , 2009, The Journal of Neuroscience.

[29]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[30]  Mark Hallett,et al.  Focal white matter changes in spasmodic dysphonia: a combined diffusion tensor imaging and neuropathological study. , 2008, Brain : a journal of neurology.

[31]  Aart J. Nederveen,et al.  Structural, functional and molecular imaging of the brain in primary focal dystonia—A review , 2011, NeuroImage.

[32]  Kristina Simonyan,et al.  Abnormal structure-function relationship in spasmodic dysphonia. , 2012, Cerebral cortex.

[33]  A. Elbaz,et al.  Structural abnormalities in the cerebellum and sensorimotor circuit in writer's cramp , 2007, Neurology.

[34]  V. Dhawan,et al.  Functional brain networks in DYT1 dystonia , 1998, Annals of neurology.

[35]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[36]  A. Pisani,et al.  Abnormal plasticity in dystonia: Disruption of synaptic homeostasis , 2011, Neurobiology of Disease.

[37]  D. Perani,et al.  Basal ganglia and thalamo‐cortical hypermetabolism in patients with spasmodic torticollis , 1996, Acta neurologica Scandinavica.

[38]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.