Impairment of a parieto‐premotor network specialized for handwriting in writer's cramp

Handwriting with the dominant hand is a highly skilled task singularly acquired in humans. This skill is the isolated deficit in patients with writer's cramp (WC), a form of dystonia with maladaptive plasticity, acquired through intensive and repetitive motor practice. When a skill is highly trained, a motor program is created in the brain to execute the same movement kinematics regardless of the effector used for the task. The task‐ and effector‐specific symptoms in WC suggest that a problem particularly occurs in the brain when the writing motor program is carried out by the dominant hand. In this MRI study involving 12 WC patients (with symptoms only affecting the right dominant hand during writing) and 15 age matched unaffected controls we showed that: (1) the writing program recruited the same network regardless of the effector used to write in both groups; (2) dominant handwriting recruited a segregated parieto‐premotor network only in the control group; (3) local structural alteration of the premotor area, the motor component of this network, predicted functional connectivity deficits during dominant handwriting and symptom duration in the patient group. Dysfunctions and structural abnormalities of a segregated parieto‐premotor network in WC patients suggest that network specialization in focal brain areas is crucial for well‐learned motor skill. Hum Brain Mapp 37:4363–4375, 2016. © 2016 Wiley Periodicals, Inc.

[1]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[3]  Richard S. J. Frackowiak,et al.  A Blueprint for Movement: Functional and Anatomical Representations in the Human Motor System , 1999, The Journal of Neuroscience.

[4]  J. Démonet,et al.  The “handwriting brain”: A meta-analysis of neuroimaging studies of motor versus orthographic processes , 2013, Cortex.

[5]  Catherine J. Stoodley,et al.  Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing , 2010, Cortex.

[6]  Patrik Vuilleumier,et al.  Moving with or without will: functional neural correlates of alien hand syndrome , 2007, Annals of neurology.

[7]  Keith Bush,et al.  A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI , 2014, NeuroImage.

[8]  G. Rizzolatti,et al.  Cortical mechanism for the visual guidance of hand grasping movements in the monkey: A reversible inactivation study. , 2001, Brain : a journal of neurology.

[9]  Steven L. Small,et al.  The mind of expert motor performance is cool and focused , 2007, NeuroImage.

[10]  Jean-François Démonet,et al.  The graphemic/motor frontal area Exner's area revisited , 2009, Annals of neurology.

[11]  A. W. Ellis Normality and pathology in cognitive functions , 1982 .

[12]  I. Toni,et al.  Reduced parietal connectivity with a premotor writing area in writer's cramp , 2012, Movement disorders : official journal of the Movement Disorder Society.

[13]  Susanne M. Jaeggi,et al.  Resting state cortico-cerebellar functional connectivity networks: a comparison of anatomical and self-organizing map approaches , 2012, Front. Neuroanat..

[14]  Maurizio Gentilucci,et al.  On gesture and speech , 2015 .

[15]  J. Tanji,et al.  Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties , 2007, Current Opinion in Neurobiology.

[16]  M Lotze,et al.  The musician's brain: functional imaging of amateurs and professionals during performance and imagery , 2003, NeuroImage.

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

[18]  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.

[19]  M. Miyazaki,et al.  An fMRI study of musicians with focal dystonia during tapping tasks , 2010, Journal of Neurology.

[20]  G. Schlaug,et al.  Effects of Music Training on the Child's Brain and Cognitive Development , 2005, Annals of the New York Academy of Sciences.

[21]  S. Meunier,et al.  Disorganized somatotopy in the putamen of patients with focal hand dystonia , 2005, Neurology.

[22]  Guy A Orban,et al.  Differences in Neural Activation for Object-Directed Grasping in Chimpanzees and Humans , 2013, The Journal of Neuroscience.

[23]  G. Eden,et al.  Examining the Central and Peripheral Processes of Written Word Production Through Meta-Analysis , 2011, Front. Psychology.

[24]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[25]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[26]  Daniel M. Wolpert,et al.  The Cerebellum Contributes to Somatosensory Cortical Activity during Self-Produced Tactile Stimulation , 1999, NeuroImage.

[27]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[28]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[29]  Daniel Zeller,et al.  Impairment of the rubber hand illusion in focal hand dystonia. , 2011, Brain : a journal of neurology.

[30]  M. Davare,et al.  Behavioral / Systems / Cognitive Dissociating the Role of Ventral and Dorsal Premotor Cortex in Precision Grasping , 2018 .

[31]  R. Passingham,et al.  Seeing or Doing? Influence of Visual and Motor Familiarity in Action Observation , 2006, Current Biology.

[32]  Julius Fridriksson,et al.  Preservation and Modulation of Specific Left Hemisphere Regions is Vital for Treated Recovery from Anomia in Stroke , 2010, The Journal of Neuroscience.

[33]  Frederik Barkhof,et al.  Frontostriatal system in planning complexity: a parametric functional magnetic resonance version of tower of london task , 2003, NeuroImage.

[34]  M. Desmurget,et al.  Movement Intention After Parietal Cortex Stimulation in Humans , 2009, Science.

[35]  G. Vingerhoets,et al.  Functional connectivity associated with hand shape generation: Imitating novel hand postures and pantomiming tool grips challenge different nodes of a shared neural network , 2015, Human brain mapping.

[36]  M. Hallett,et al.  Plasticity of cortical inhibition in dystonia is impaired after motor learning and paired‐associative stimulation , 2012, The European journal of neuroscience.

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

[38]  M. Desmurget,et al.  A parietal-premotor network for movement intention and motor awareness , 2009, Trends in Cognitive Sciences.

[39]  J. Rothwell,et al.  Secondary and primary dystonia: pathophysiological differences. , 2013, Brain : a journal of neurology.

[40]  Peter L Strick,et al.  Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex , 2011, Proceedings of the National Academy of Sciences.

[41]  Kristina Simonyan,et al.  What's special about task in dystonia? A voxel‐based morphometry and diffusion weighted imaging study , 2014, Movement disorders : official journal of the Movement Disorder Society.

[42]  H. Schild,et al.  Abnormal Movement Preparation in Task-Specific Focal Hand Dystonia , 2013, PloS one.

[43]  S. Meunier,et al.  Defective cerebellar control of cortical plasticity in writer's cramp. , 2013, Brain : a journal of neurology.

[44]  G. Schlaug,et al.  Brain Structures Differ between Musicians and Non-Musicians , 2003, The Journal of Neuroscience.

[45]  Mark Hallett,et al.  Timing-dependent modulation of the posterior parietal cortex-primary motor cortex pathway by sensorimotor training. , 2012, Journal of neurophysiology.

[46]  A. Schleicher,et al.  Motor cortex and hand motor skills: Structural compliance in the human brain , 1997, Human brain mapping.

[47]  J. Rothwell,et al.  Abnormal sensorimotor plasticity in organic but not in psychogenic dystonia. , 2009, Brain : a journal of neurology.

[48]  Mark Hallett,et al.  Pathophysiology of writer's cramp. , 2006, Human movement science.

[49]  Tatsuro Kaminaga,et al.  Interindividual uniformity and variety of the “Writing center”: A functional MRI study , 2006, NeuroImage.

[50]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[51]  Florian Castrop,et al.  Multiple changes of functional connectivity between sensorimotor areas in focal hand dystonia , 2014, Journal of Neurology, Neurosurgery & Psychiatry.

[52]  J. Grafman,et al.  Association of ideomotor apraxia with frontal gray matter volume loss in corticobasal syndrome. , 2009, Archives of neurology.

[53]  M. Hallett,et al.  Probing the interaction of the ipsilateral posterior parietal cortex with the premotor cortex using a novel transcranial magnetic stimulation technique , 2016, Clinical Neurophysiology.

[54]  Lutz Jäncke,et al.  The Architecture of the Golfer's Brain , 2009, PloS one.

[55]  M. Hallett,et al.  Emerging concepts in the physiological basis of dystonia , 2013, Movement disorders : official journal of the Movement Disorder Society.

[56]  B. Biswal,et al.  Repetitive transcranial magnetic stimulation induced modulations of resting state motor connectivity in writer's cramp , 2015, European journal of neurology.

[57]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[58]  S. Fairhall,et al.  Impaired sensorimotor integration in focal hand dystonia patients in the absence of symptoms , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[59]  M. Hallett,et al.  The differential modulation of the ventral premotor–motor interaction during movement initiation is deficient in patients with focal hand dystonia , 2012, The European journal of neuroscience.

[60]  R. Kaji Basal ganglia as a sensory gating devise for motor control. , 2001, The journal of medical investigation : JMI.

[61]  S. Lehéricy,et al.  The anatomical basis of dystonia: Current view using neuroimaging , 2013, Movement disorders : official journal of the Movement Disorder Society.

[62]  J. Doyon,et al.  Increased cortico-striatal connectivity during motor practice contributes to the consolidation of motor memory in writer's cramp patients , 2015, NeuroImage: Clinical.

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

[64]  Tadashi Isa,et al.  Temporal Plasticity Involved in Recovery from Manual Dexterity Deficit after Motor Cortex Lesion in Macaque Monkeys , 2015, The Journal of Neuroscience.

[65]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[66]  C. Beckmann,et al.  Task-Free Functional MRI in Cervical Dystonia Reveals Multi-Network Changes That Partially Normalize with Botulinum Toxin , 2013, PloS one.

[67]  J C Rothwell,et al.  Abnormal premovement gating of somatosensory input in writer's cramp. , 2000, Brain : a journal of neurology.

[68]  M Hallett,et al.  Gesture subtype-dependent left lateralization of praxis planning: an event-related fMRI study. , 2009, Cerebral cortex.

[69]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[70]  Mark Hallett,et al.  Individuated finger control in focal hand dystonia: An fMRI study , 2012, NeuroImage.

[71]  Yoshikazu Ugawa,et al.  Parietal Dysgraphia: Characterization of Abnormal Writing Stroke Sequences, Character Formation and Character Recall , 2007, Behavioural neurology.

[72]  A. Caramazza,et al.  The Graphemic Buffer and attentional mechanisms , 1989, Brain and Language.

[73]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[74]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[75]  M. Hallett,et al.  Functional Anatomy of Writing with the Dominant Hand , 2013, PloS one.

[76]  Gerard P. van Galen,et al.  Handwriting: Issues for a psychomotor theory ☆ , 1991 .

[77]  M. Hallett,et al.  The basal ganglia are hyperactive during the discrimination of tactile stimuli in writer's cramp. , 2006, Brain : a journal of neurology.

[78]  H. Duffau,et al.  Agraphia after awake surgery for brain tumor: new insights into the anatomo-functional network of writing. , 2009, Surgical neurology.

[79]  J. Rothwell,et al.  Task-specific hand dystonia: can too much plasticity be bad for you? , 2006, Trends in Neurosciences.

[80]  L. Bérubé,et al.  [Clinical neuropsychology]. , 1982, Nursing Quebec.