Transcallosal connectivity of the human cortical motor network

The organisational and architectural configuration of white matter pathways connecting brain regions has ramifications for all facets of the human condition, including manifestations of incipient neurodegeneration. Although diffusion tensor imaging (DTI) has been used extensively to visualise white matter connectivity, due to the widespread presence of crossing fibres, the lateral projections of the corpus callosum are not normally detected using this methodology. Detailed knowledge of the transcallosal connectivity of the human cortical motor network has, therefore, remained elusive. We employed constrained spherical deconvolution (CSD) tractography—an approach that is much less susceptible to the influence of crossing fibres, in order to derive complete in vivo characterizations of white matter pathways connecting specific motor cortical regions to their counterparts and other loci in the opposite hemisphere. The revealed patterns of connectivity closely resemble those derived from anatomical tracing in primates. It was established that dorsal premotor cortex (PMd) and supplementary motor area (SMA) have extensive interhemispheric connectivity—exhibiting both dense homologous projections, and widespread structural relations with every other region in the contralateral motor network. Through this in vivo portrayal, the importance of non-primary motor regions for interhemispheric communication is emphasised. Additionally, distinct connectivity profiles were detected for the anterior and posterior subdivisions of primary motor cortex. The present findings provide a comprehensive representation of transcallosal white matter projections in humans, and have the potential to inform the development of models and hypotheses relating structural and functional brain connectivity.

[1]  G. Gerig,et al.  Fractional anisotropy distributions in 2- to 6-year-old children with autism. , 2012, Journal of intellectual disability research : JIDR.

[2]  M. A. Jeeves,et al.  Bimanual co-ordination in callosal agenesis and partial commissurotomy , 1988, Neuropsychologia.

[3]  James C. Gee,et al.  Spatial transformations of diffusion tensor magnetic resonance images , 2001, IEEE Transactions on Medical Imaging.

[4]  M. Catani,et al.  Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true‐tract specific index to characterize white matter diffusion , 2013, Human brain mapping.

[5]  J. Attems,et al.  White matter connections of the supplementary motor area in humans , 2014, Journal of Neurology, Neurosurgery & Psychiatry.

[6]  N Filippini,et al.  Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis , 2010, Neurology.

[7]  Michael S. Gazzaniga,et al.  Direction information coordinated via the posterior third of the corpus callosum during bimanual movements , 1999, Experimental Brain Research.

[8]  Philip G. F. Browning,et al.  Causal effect of disconnection lesions on interhemispheric functional connectivity in rhesus monkeys , 2013, Proceedings of the National Academy of Sciences.

[9]  M. Corbetta,et al.  Evolutionarily Novel Functional Networks in the Human Brain? , 2013, The Journal of Neuroscience.

[10]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

[11]  Dinggang Shen,et al.  Axonal fiber terminations concentrate on gyri. , 2012, Cerebral cortex.

[12]  P. Roland,et al.  Fields in human motor areas involved in preparation for reaching, actual reaching, and visuomotor learning: a positron emission tomography study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  J. Villemure,et al.  Sensory and Motor Interhemispheric Integration after Section of Different Portions of the Anterior Corpus Callosum in Nonepileptic Patients , 2005, Neurosurgery.

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

[15]  R. Carson.  Neural pathways mediating bilateral interactions between the upper limbs , 2005, Brain Research Reviews.

[16]  Derek K. Jones,et al.  Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging , 2013, Human brain mapping.

[17]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

[18]  Max A. Viergever,et al.  Recursive calibration of the fiber response function for spherical deconvolution of diffusion MRI data , 2014, NeuroImage.

[19]  Jan Sijbers,et al.  Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution , 2011, Human brain mapping.

[20]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations , 2007, The Journal of Neuroscience.

[21]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[22]  Jan Sijbers,et al.  Weighted linear least squares estimation of diffusion MRI parameters: Strengths, limitations, and pitfalls , 2013, NeuroImage.

[23]  C. Büchel,et al.  White matter asymmetry in the human brain: a diffusion tensor MRI study. , 2004, Cerebral cortex.

[24]  J. Kaas,et al.  Corpus callosum connections of subdivisions of motor and premotor cortex, and frontal eye field in a prosimian primate, Otolemur garnetti , 2008, The Journal of comparative neurology.

[25]  Max A. Viergever,et al.  elastix: A Toolbox for Intensity-Based Medical Image Registration , 2010, IEEE Transactions on Medical Imaging.

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

[27]  Alexander Leemans,et al.  The B‐matrix must be rotated when correcting for subject motion in DTI data , 2009, Magnetic resonance in medicine.

[28]  Jan Sijbers,et al.  ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data , 2009 .

[29]  U. Jürgens,et al.  The efferent and afferent connections of the supplementary motor area , 1984, Brain Research.

[30]  M S Gazzaniga,et al.  Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers. , 2000, Brain : a journal of neurology.

[31]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.

[32]  B. Preilowski,et al.  Possible contribution of the anterior forebrain commissures to bilateral motor coordination. , 1972, Neuropsychologia.

[33]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[34]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[35]  Walter Schneider,et al.  In vivo quantification of global connectivity in the human corpus callosum , 2012, NeuroImage.

[36]  Olaf Sporns,et al.  Can structure predict function in the human brain? , 2010, NeuroImage.

[37]  M. Petrides,et al.  Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas. , 2014, Cerebral cortex.

[38]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[39]  Alan Connelly,et al.  Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution , 2007, NeuroImage.

[40]  Shenmin Zhang,et al.  Resting-state functional connectivity of the medial superior frontal cortex. , 2012, Cerebral cortex.

[41]  Scott Barbay,et al.  Interhemispheric connections of the ventral premotor cortex in a new world primate , 2007, The Journal of comparative neurology.

[42]  Stuart Crozier,et al.  Apparent Fibre Density: A novel measure for the analysis of diffusion-weighted magnetic resonance images , 2012, NeuroImage.

[43]  T. Johnson,et al.  Diffusion tensor MRI of the corpus callosum in amyotrophic lateral sclerosis , 2014, Journal of magnetic resonance imaging : JMRI.

[44]  C. Brinkman.  Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  K. Muller,et al.  Approximating the Geisser-Greenhouse sphericity estimator and its applications to diffusion tensor imaging. , 2010, Statistics and its Interface.

[46]  D. Boussaoud,et al.  Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study , 2005, BMC Neuroscience.

[47]  R. Caminiti,et al.  Callosal connections of dorso‐lateral premotor cortex , 2003, The European journal of neuroscience.

[48]  Thierry Wannier,et al.  Origins of callosal projections to the supplementary motor area (SMA): A direct comparison between pre‐SMA and SMA‐proper in macaque monkeys , 2002, The Journal of comparative neurology.

[49]  Xiaoping P. Hu,et al.  Coevolution of gyral folding and structural connection patterns in primate brains. , 2013, Cerebral cortex.

[50]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[51]  Chun-Hung Yeh,et al.  Probabilistic topography of human corpus callosum using cytoarchitectural parcellation and high angular resolution diffusion imaging tractography , 2009, Human brain mapping.

[52]  N. Makris,et al.  High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity , 2002, Magnetic resonance in medicine.

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

[54]  Nikola T. Markov,et al.  A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex , 2012, Cerebral cortex.

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