A Template and Probabilistic Atlas of the Human Sensorimotor Tracts using Diffusion MRI

The purpose of this study was to develop a high-resolution sensorimotor area tract template (SMATT) which segments corticofugal tracts based on 6 cortical regions in primary motor cortex, dorsal premotor cortex, ventral premotor cortex, supplementary motor area (SMA), pre-supplementary motor area (preSMA), and primary somatosensory cortex using diffusion tensor imaging. Individual probabilistic tractography analyses were conducted in 100 subjects using the highest resolution data currently available. Tractography results were refined using a novel algorithm to objectively determine slice level thresholds that best minimized overlap between tracts while preserving tract volume. Consistent with tracing studies in monkey and rodent, our observations show that cortical topography is generally preserved through the internal capsule, with the preSMA tract remaining most anterior and the primary somatosensory tract remaining most posterior. We combine our results into a freely available white matter template named the SMATT. We also provide a probabilistic SMATT that quantifies the extent of overlap between tracts. Finally, we assess how the SMATT operates at the individual subject level in another independent data set, and in an individual after stroke. The SMATT and probabilistic SMATT provide new tools that segment and label sensorimotor tracts at a spatial resolution not previously available.

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

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

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

[4]  Nicole Varnerin,et al.  Rethinking Stimulation of the Brain in Stroke Rehabilitation , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[5]  I. Darian‐Smith,et al.  Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. , 1994, Cerebral cortex.

[6]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[7]  R. Nudo,et al.  Descending pathways to the spinal cord, III: Sites of origin of the corticospinal tract , 1990, The Journal of comparative neurology.

[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]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  R. Lemon,et al.  Comparing the function of the corticospinal system in different species: Organizational differences for motor specialization? , 2005, Muscle & nerve.

[11]  W. Byblow,et al.  Functional potential in chronic stroke patients depends on corticospinal tract integrity. , 2006, Brain : a journal of neurology.

[12]  Heffner Rs,et al.  The Role of the Corticospinal Tract in the Evolution of Human Digital Dexterity , 1983 .

[13]  V. Muggeo Estimating regression models with unknown break‐points , 2003, Statistics in medicine.

[14]  S. Lehéricy,et al.  3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. , 2004, Cerebral cortex.

[15]  Nick S. Ward,et al.  Assessing a standardised approach to measuring corticospinal integrity after stroke with DTI☆ , 2013, NeuroImage: Clinical.

[16]  S. Swinnen,et al.  Brain‐behavior relationships in young traumatic brain injury patients: DTI metrics are highly correlated with postural control , 2009, Human brain mapping.

[17]  Stephen A Coombes,et al.  Pain‐Related Suppression of Beta Oscillations Facilitates Voluntary Movement , 2016, Cerebral cortex.

[18]  Peter A. Calabresi,et al.  Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification , 2008, NeuroImage.

[19]  A. Travis,et al.  Neurological deficiencies after ablation of the precentral motor area in Macaca mulatta. , 1955, Brain : a journal of neurology.

[20]  Derek B Archer,et al.  Microstructural properties of premotor pathways predict visuomotor performance in chronic stroke , 2016, Human brain mapping.

[21]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[22]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[23]  Sung Ho Jang,et al.  Injury of the Corticospinal Tract in Patients with Mild Traumatic Brain Injury: A Diffusion Tensor Tractography Study. , 2016, Journal of neurotrauma.

[24]  Timothy Edward John Behrens,et al.  Effects of image reconstruction on fiber orientation mapping from multichannel diffusion MRI: Reducing the noise floor using SENSE , 2013, Magnetic resonance in medicine.

[25]  Jeremy D. Schmahmann,et al.  Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers , 2008, NeuroImage.

[26]  Heidi Johansen-Berg,et al.  Probabilistic tractography of the optic radiations—An automated method and anatomical validation , 2010, NeuroImage.

[27]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[28]  J. Schaechter,et al.  Corticospinal Tract Diffusion Abnormalities Early After Stroke Predict Motor Outcome , 2014, Neurorehabilitation and neural repair.

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

[30]  Mark Jenkinson,et al.  A consistent relationship between local white matter architecture and functional specialisation in medial frontal cortex , 2006, NeuroImage.

[31]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  G. Schlaug,et al.  Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke , 2010, Neurology.

[33]  Nicole Wenderoth,et al.  The Corticospinal Tract: A Biomarker to Categorize Upper Limb Functional Potential in Unilateral Cerebral Palsy , 2016, Front. Pediatr..

[34]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[35]  G Rizzolatti,et al.  Corticospinal projections from mesial frontal and cingulate areas in the monkey. , 1994, Neuroreport.

[36]  S. Swinnen,et al.  Disturbed cortico‐subcortical interactions during motor task switching in traumatic brain injury , 2013, Human brain mapping.

[37]  Steen Moeller,et al.  Advances in diffusion MRI acquisition and processing in the Human Connectome Project , 2013, NeuroImage.

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

[39]  S. Rauch,et al.  Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. , 2005, The American journal of psychiatry.

[40]  N. Makris,et al.  Hypothalamic Abnormalities in Schizophrenia: Sex Effects and Genetic Vulnerability , 2007, Biological Psychiatry.

[41]  M Wiesendanger,et al.  Dexterity in adult monkeys following early lesion of the motor cortical hand area: the role of cortex adjacent to the lesion , 1998, The European journal of neuroscience.

[42]  R B Masterton,et al.  Descending pathways to the spinal cord, IV: Some factors related to the amount of cortex devoted to the corticospinal tract , 1990, The Journal of comparative neurology.

[43]  J. Polimeni,et al.  Blipped‐controlled aliasing in parallel imaging for simultaneous multislice echo planar imaging with reduced g‐factor penalty , 2012, Magnetic resonance in medicine.

[44]  C. Woolsey,et al.  A study of localization in the corticospinal tracts of monkey and rat , 1956, The Journal of comparative neurology.

[45]  Sungyoung Auh,et al.  Diffuse and Focal Corticospinal Tract Disease and Its Impact on Patient Disability in Multiple Sclerosis , 2015, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[46]  Stephen A Coombes,et al.  Neuroimaging Evidence of Motor Control and Pain Processing in the Human Midcingulate Cortex. , 2015, Cerebral cortex.

[47]  Stamatios N. Sotiropoulos,et al.  A probabilistic atlas of the cerebellar white matter , 2016, NeuroImage.

[48]  W. Fries,et al.  Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. , 1993, Brain : a journal of neurology.

[49]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[50]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  Randy L. Gollub,et al.  Reproducibility of quantitative tractography methods applied to cerebral white matter , 2007, NeuroImage.

[52]  Vishwanath Sankarasubramanian,et al.  Influence of Corticospinal Tracts from Higher Order Motor Cortices on Recruitment Curve Properties in Stroke , 2016, Front. Neurosci..

[53]  S. Jang,et al.  Aging of corticospinal tract fibers according to the cerebral origin in the human brain: A diffusion tensor imaging study , 2015, Neuroscience Letters.

[54]  H. Kuypers,et al.  Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in monkey (Macaca fascicularis) , 2004, Experimental Brain Research.

[55]  David W. McNeal,et al.  Vulnerability of the medial frontal corticospinal projection accompanies combined lateral frontal and parietal cortex injury in rhesus monkey , 2015, The Journal of comparative neurology.

[56]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[57]  D. Vaillancourt,et al.  Maintaining Force Control Despite Changes in Emotional Context Engages Dorsomedial Prefrontal and Premotor Cortex , 2011, Cerebral cortex.

[58]  Timothy E. J. Behrens,et al.  Measuring macroscopic brain connections in vivo , 2015, Nature Neuroscience.

[59]  Stephen M. Smith,et al.  Multiplexed Echo Planar Imaging for Sub-Second Whole Brain FMRI and Fast Diffusion Imaging , 2010, PloS one.

[60]  David E Vaillancourt,et al.  Selective regions of the visuomotor system are related to gain-induced changes in force error. , 2010, Journal of neurophysiology.

[61]  Nikos Makris,et al.  Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients , 2009, Human brain mapping.

[62]  Robert Lindenberg,et al.  Predicting functional motor potential in chronic stroke patients using diffusion tensor imaging , 2012, Human brain mapping.

[63]  Bong Soo Kim,et al.  Evaluation of the Somatotopic Organization of Corticospinal Tracts in the Internal Capsule and Cerebral Peduncle: Results of Diffusion-Tensor MR Tractography , 2008, Korean journal of radiology.

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

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

[66]  G. Baker,et al.  Topography of fibre organisation in the corticofugal pathways of rats , 1997, The Journal of comparative neurology.

[67]  N. Makris,et al.  Decreased volume of left and total anterior insular lobule in schizophrenia , 2006, Schizophrenia Research.

[68]  Karl J. Friston,et al.  Non-invasive mapping of corticofugal fibres from multiple motor areas--relevance to stroke recovery. , 2006, Brain : a journal of neurology.

[69]  Jian Wang,et al.  Motor recovery at 6 months after admission is related to structural and functional reorganization of the spine and brain in patients with spinal cord injury , 2016, Human brain mapping.

[70]  Manuel Graña,et al.  Model‐based analysis of multishell diffusion MR data for tractography: How to get over fitting problems , 2012, Magnetic resonance in medicine.

[71]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

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

[73]  Robert Lindenberg,et al.  Lesion Load of the Corticospinal Tract Predicts Motor Impairment in Chronic Stroke , 2010, Stroke.

[74]  R. Lemon,et al.  Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. , 2002, Cerebral cortex.

[75]  R B Masterton,et al.  The role of the corticospinal tract in the evolution of human digital dexterity. , 1983, Brain, behavior and evolution.

[76]  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.

[77]  Max A. Viergever,et al.  Partial volume effect as a hidden covariate in DTI analyses , 2011, NeuroImage.

[78]  Volkmar Glauche,et al.  Diffusion tensor MRI of early upper motor neuron involvement in amyotrophic lateral sclerosis. , 2004, Brain : a journal of neurology.

[79]  Heidi Johansen-Berg,et al.  Using diffusion imaging to study human connectional anatomy. , 2009, Annual review of neuroscience.

[80]  Stephen A. Coombes,et al.  Spatiotemporal tuning of brain activity and force performance , 2011, NeuroImage.

[81]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[82]  Ruopeng Wang,et al.  Structural damage to the corticospinal tract correlates with bilateral sensorimotor cortex reorganization in stroke patients , 2008, NeuroImage.

[83]  Sung Ho Jang,et al.  The role of the corticospinal tract in motor recovery in patients with a stroke: a review. , 2009, NeuroRehabilitation.

[84]  Chang-Hyun Park,et al.  Assessing the Integrity of Corticospinal Pathways From Primary and Secondary Cortical Motor Areas After Stroke , 2012, Stroke.