Grey matter volumetric changes related to recovery from hand paresis after cortical sensorimotor stroke

Abstract Preclinical studies using animal models have shown that grey matter plasticity in both perilesional and distant neural networks contributes to behavioural recovery of sensorimotor functions after ischaemic cortical stroke. Whether such morphological changes can be detected after human cortical stroke is not yet known, but this would be essential to better understand post-stroke brain architecture and its impact on recovery. Using serial behavioural and high-resolution magnetic resonance imaging (MRI) measurements, we tracked recovery of dexterous hand function in 28 patients with ischaemic stroke involving the primary sensorimotor cortices. We were able to classify three recovery subgroups (fast, slow, and poor) using response feature analysis of individual recovery curves. To detect areas with significant longitudinal grey matter volume (GMV) change, we performed tensor-based morphometry of MRI data acquired in the subacute phase, i.e. after the stage compromised by acute oedema and inflammation. We found significant GMV expansion in the perilesional premotor cortex, ipsilesional mediodorsal thalamus, and caudate nucleus, and GMV contraction in the contralesional cerebellum. According to an interaction model, patients with fast recovery had more perilesional than subcortical expansion, whereas the contrary was true for patients with impaired recovery. Also, there were significant voxel-wise correlations between motor performance and ipsilesional GMV contraction in the posterior parietal lobes and expansion in dorsolateral prefrontal cortex. In sum, perilesional GMV expansion is associated with successful recovery after cortical stroke, possibly reflecting the restructuring of local cortical networks. Distant changes within the prefrontal-striato-thalamic network are related to impaired recovery, probably indicating higher demands on cognitive control of motor behaviour.

[1]  G E Alexander,et al.  The contribution of basal ganglia to limb control. , 1986, Progress in brain research.

[2]  K. Amunts,et al.  The human inferior parietal lobule in stereotaxic space , 2008, Brain Structure and Function.

[3]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[4]  S. Barbay,et al.  Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey. , 2008, Journal of neurophysiology.

[5]  Ann M. Stowe,et al.  Extensive Cortical Rewiring after Brain Injury , 2005, The Journal of Neuroscience.

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

[7]  R. Wiest,et al.  Chronic pelvic pain syndrome in men is associated with reduction of relative gray matter volume in the anterior cingulate cortex compared to healthy controls. , 2013, The Journal of urology.

[8]  John Ashburner,et al.  A tensor based morphometry study of longitudinal gray matter contraction in FTD , 2007, NeuroImage.

[9]  Alan C. Evans,et al.  Fast and robust parameter estimation for statistical partial volume models in brain MRI , 2004, NeuroImage.

[10]  Maria Assunta Rocca,et al.  Cognitive learning is associated with gray matter changes in healthy human individuals: A tensor-based morphometry study , 2009, NeuroImage.

[11]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

[12]  R. Beaglehole,et al.  Recovery of motor function after stroke. , 1988, Stroke.

[13]  Rory Stewart The Places in Between , 2004 .

[14]  R. Nudo Functional and structural plasticity in motor cortex: implications for stroke recovery. , 2003, Physical medicine and rehabilitation clinics of North America.

[15]  R. Nudo,et al.  Cortical plasticity after stroke: implications for rehabilitation. , 1999, Revue neurologique.

[16]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[17]  R. Nudo Remodeling of cortical motor representations after stroke: implications for recovery from brain damage , 1997, Molecular Psychiatry.

[18]  E. Luders,et al.  Voxel-Based Morphometry , 2015 .

[19]  D. Pandya,et al.  Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey , 2009, PLoS biology.

[20]  L. Cohen,et al.  Reorganization of the human ipsilesional premotor cortex after stroke. , 2004, Brain : a journal of neurology.

[21]  Liang Wang,et al.  Dynamic brain structural changes after left hemisphere subcortical stroke , 2013, Human Brain Mapping.

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

[23]  Pélagie M. Beeson,et al.  Cost function masking during normalization of brains with focal lesions: Still a necessity? , 2010, NeuroImage.

[24]  John W Krakauer,et al.  Arm function after stroke: from physiology to recovery. , 2005, Seminars in neurology.

[25]  J. Ashburner,et al.  Progression of structural neuropathology in preclinical Huntington’s disease: a tensor based morphometry study , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[26]  A E Hillis,et al.  Crossed Cerebellar Diaschisis in Acute Stroke Detected by Dynamic Susceptibility Contrast MR Perfusion Imaging , 2009, American Journal of Neuroradiology.

[27]  U. Castiello The neuroscience of grasping , 2005, Nature Reviews Neuroscience.

[28]  D C Thomas,et al.  Excavations at Jam, Afghanistan , 2004 .

[29]  V. Mathiowetz,et al.  Reliability and validity of grip and pinch strength evaluations. , 1984, The Journal of hand surgery.

[30]  Katrin Amunts,et al.  Broca’s area: Nomenclature, anatomy, typology and asymmetry , 2009, Brain and Language.

[31]  Angela R. Laird,et al.  Is There “One” DLPFC in Cognitive Action Control? Evidence for Heterogeneity From Co-Activation-Based Parcellation , 2012, Cerebral cortex.

[32]  C. Plastaras,et al.  Electrodiagnostic challenges in the evaluation of lumbar spinal stenosis. , 2003, Physical medicine and rehabilitation clinics of North America.

[33]  Lynne V. Gauthier,et al.  Remodeling the Brain: Plastic Structural Brain Changes Produced by Different Motor Therapies After Stroke , 2008, Stroke.

[34]  J. Krakauer,et al.  Neurorehabilitation and Neural Repair Inter-individual Variability in the Capacity for Motor Recovery after Ischemic Stroke Neurorehabilitation and Neural Repair Additional Services and Information for Inter-individual Variability in the Capacity for Motor Recovery after Ischemic Stroke , 2022 .

[35]  Josep Marco-Pallarés,et al.  Analysis of automated methods for spatial normalization of lesioned brains , 2012, NeuroImage.

[36]  T. Murphy,et al.  In Vivo Calcium Imaging Reveals Functional Rewiring of Single Somatosensory Neurons after Stroke , 2008, The Journal of Neuroscience.

[37]  J. Marler,et al.  Measurements of acute cerebral infarction: a clinical examination scale. , 1989, Stroke.

[38]  Stefan Geyer,et al.  Prologue: Toward the Concept of a Cortical Control of Voluntary Movements , 2004 .

[39]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[40]  L. Ostergaard,et al.  Changes in regional brain volume three months after stroke , 2012, Journal of the Neurological Sciences.

[41]  C. Stinear,et al.  Prediction of recovery of motor function after stroke , 2010, The Lancet Neurology.

[42]  R Turner,et al.  Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T , 2004, NeuroImage.

[43]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[44]  Mark D. Huffman,et al.  Heart disease and stroke statistics--2013 update: a report from the American Heart Association. , 2013, Circulation.

[45]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[46]  J. Krakauer,et al.  Medial Premotor Cortex Shows a Reduction in Inhibitory Markers and Mediates Recovery in a Mouse Model of Focal Stroke , 2013, Stroke.

[47]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[48]  Gereon R. Fink,et al.  Supramodal Representation of Objects and Actions in the Human Inferior Temporal and Ventral Premotor Cortex , 2004, Cortex.

[49]  S. Carmichael,et al.  New Patterns of Intracortical Projections after Focal Cortical Stroke , 2001, Neurobiology of Disease.

[50]  J. Ashburner,et al.  Atrophy progression in semantic dementia with asymmetric temporal involvement: A tensor-based morphometry study , 2009, Neurobiology of Aging.

[51]  Steven C Cramer,et al.  Motor Cortex Stimulation for the Enhancement of Recovery from Stroke: A Prospective, Multicenter Safety Study , 2006, Neurosurgery.

[52]  Katherine L. Perdue,et al.  Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. , 2008, Cerebral cortex.

[53]  Matthew Petoe,et al.  The PREP algorithm predicts potential for upper limb recovery after stroke. , 2012, Brain : a journal of neurology.

[54]  M. Filippi,et al.  Motor Learning in Healthy Humans Is Associated to Gray Matter Changes: A Tensor-Based Morphometry Study , 2010, PloS one.

[55]  F. Flood Ghurid monuments and Muslim identities , 2005 .

[56]  Guozhi Tao,et al.  Deep gray matter atrophy in multiple sclerosis: A tensor based morphometry , 2009, Journal of the Neurological Sciences.

[57]  S Senn,et al.  Analysis of serial measurements in medical research. , 1990, BMJ.

[58]  Massimo Filippi,et al.  Longitudinal assessment of grey matter contraction in amyotrophic lateral sclerosis: A tensor based morphometry study , 2009, Amyotrophic lateral sclerosis : official publication of the World Federation of Neurology Research Group on Motor Neuron Diseases.

[59]  Wei Liao,et al.  Preferential networks of the mediodorsal nucleus and centromedian–parafascicular complex of the thalamus—A DTI tractography study , 2012, Human brain mapping.

[60]  M F Chesselet,et al.  Anatomical and functional evidence for lesion‐specific sprouting of corticostriatal input in the adult rat , 1996, The Journal of comparative neurology.

[61]  H. Forssberg,et al.  Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. , 2001, Journal of neurophysiology.

[62]  Rick M Dijkhuizen,et al.  Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. , 2006, Brain : a journal of neurology.

[63]  Karl J. Friston,et al.  Distributional Assumptions in Voxel-Based Morphometry , 2002, NeuroImage.

[64]  Sterling C. Johnson,et al.  Longitudinal Volumetric Changes following Traumatic Brain Injury: A Tensor-Based Morphometry Study , 2012, Journal of the International Neuropsychological Society.

[65]  D. Louis Collins,et al.  Sensitivity of voxel-based morphometry analysis to choice of imaging protocol at 3 T , 2009, NeuroImage.

[66]  Simon B. Eickhoff,et al.  Activation likelihood estimation meta-analysis of motor-related neural activity after stroke , 2012, NeuroImage.

[67]  Sébastien Ourselin,et al.  Issues with threshold masking in voxel-based morphometry of atrophied brains , 2009, NeuroImage.

[68]  Nikolaus R. McFarland,et al.  The Place of the Thalamus in Frontal Cortical-Basal Ganglia Circuits , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[69]  Dr. Stefan Geyer The Microstructural Border Between the Motor and the Cognitive Domain in the Human Cerebral Cortex , 2004, Advances in Anatomy Embryology and Cell Biology.

[70]  Andrea Federspiel,et al.  Lesions to Primary Sensory and Posterior Parietal Cortices Impair Recovery from Hand Paresis after Stroke , 2012, PloS one.

[71]  F. Binkofski,et al.  Motor functions of the Broca’s region , 2004, Brain and Language.

[72]  R. Seitz,et al.  Learning of Sequential Finger Movements in Man: A Combined Kinematic and Positron Emission Tomography (PET) Study , 1992, The European journal of neuroscience.

[73]  J. Wojczal,et al.  Quantitative evaluation of crossed cerebellar diaschisis, using voxel-based analysis of Tc-99m ECD brain SPECT. , 2013, Nuclear medicine review. Central & Eastern Europe.

[74]  R. H. Jebsen,et al.  An objective and standardized test of hand function. , 1969, Archives of physical medicine and rehabilitation.

[75]  K. Amunts,et al.  Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. , 2008, Cerebral cortex.

[76]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[77]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[78]  E B Stern,et al.  Stability of the Jebsen-Taylor Hand Function Test across three test sessions. , 1992, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[79]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[80]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

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

[82]  R. Passingham,et al.  Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity , 2001, NeuroImage.

[83]  E. Hogg,et al.  Synapse replacement in the striatum of the adult rat following unilateral cortex ablation , 2003, The Journal of comparative neurology.

[84]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[85]  Guy Marchal,et al.  Multi-modality image registration by maximization of mutual information , 1996, Proceedings of the Workshop on Mathematical Methods in Biomedical Image Analysis.

[86]  Angela R. Laird,et al.  Tackling the multifunctional nature of Broca's region meta-analytically: Co-activation-based parcellation of area 44 , 2013, NeuroImage.

[87]  Ravi S. Menon,et al.  Imaging at high magnetic fields: initial experiences at 4 T. , 1993, Magnetic resonance quarterly.