MR connectomics: Principles and challenges

MR connectomics is an emerging framework in neuro-science that combines diffusion MRI and whole brain tractography methodologies with the analytical tools of network science. In the present work we review the current methods enabling structural connectivity mapping with MRI and show how such data can be used to infer new information of both brain structure and function. We also list the technical challenges that should be addressed in the future to achieve high-resolution maps of structural connectivity. From the resulting tremendous amount of data that is going to be accumulated soon, we discuss what new challenges must be tackled in terms of methods for advanced network analysis and visualization, as well data organization and distribution. This new framework is well suited to investigate key questions on brain complexity and we try to foresee what fields will most benefit from these approaches.

[1]  Kalvis M. Jansons,et al.  Persistent angular structure: new insights from diffusion magnetic resonance imaging data , 2003 .

[2]  Manuel Casanova,et al.  Radial cytoarchitecture and patterns of cortical connectivity in autism , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  Bernhard Ø Palsson,et al.  Understanding human metabolic physiology: a genome-to-systems approach. , 2009, Trends in biotechnology.

[4]  V. Wedeen,et al.  Halving imaging time of whole brain diffusion spectrum imaging and diffusion tractography using simultaneous image refocusing in EPI , 2009, Journal of magnetic resonance imaging : JMRI.

[5]  V. Wedeen,et al.  Fiber crossing in human brain depicted with diffusion tensor MR imaging. , 2000, Radiology.

[6]  M. Fox,et al.  Intrinsic functional relations between human cerebral cortex and thalamus. , 2008, Journal of neurophysiology.

[7]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[8]  S. Clarke,et al.  Thalamic projections of the fusiform gyrus in man , 1999, The European journal of neuroscience.

[9]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[10]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[11]  O. Sporns,et al.  Motifs in Brain Networks , 2004, PLoS biology.

[12]  N. Zečević,et al.  Oligodendrocyte Development and the Onset of Myelination in the Human Fetal Brain , 2009, Front. Neuroanat..

[13]  M. Adams,et al.  How many genes in the human genome? , 1994, Nature Genetics.

[14]  Jacob Jelsing,et al.  Validation of in vitro probabilistic tractography , 2007, NeuroImage.

[15]  J. Kurhanewicz,et al.  Diffusion-weighted MR imaging of acute stroke: correlation with T2-weighted and magnetic susceptibility-enhanced MR imaging in cats. , 1990, AJNR. American journal of neuroradiology.

[16]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[17]  Akira Ishida,et al.  Plasticity and injury in the developing brain , 2009, Brain and Development.

[18]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[19]  Jean-Francois Mangin,et al.  Fiber Tracking in q-Ball Fields Using Regularized Particle Trajectories , 2005, IPMI.

[20]  A. Alexander,et al.  White matter tractography using diffusion tensor deflection , 2003, Human brain mapping.

[21]  M. Young,et al.  Advanced database methodology for the Collation of Connectivity data on the Macaque brain (CoCoMac). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  Jelliffe.  Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[23]  P. Thiran,et al.  Mapping Human Whole-Brain Structural Networks with Diffusion MRI , 2007, PloS one.

[24]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .

[25]  V. Wedeen,et al.  Mapping fiber orientation spectra in cerebral white matter with Fourier-transform diffusion MRI , 2000 .

[26]  Christopher A Walsh,et al.  Genetic basis of developmental malformations of the cerebral cortex. , 2004, Archives of neurology.

[27]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[28]  Lester Melie-García,et al.  Characterizing brain anatomical connections using diffusion weighted MRI and graph theory , 2007, NeuroImage.

[29]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

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

[31]  Yaniv Assaf,et al.  Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain , 2005, NeuroImage.

[32]  H. L. Dryden,et al.  Investigations on the Theory of the Brownian Movement , 1957 .

[33]  P. Thompson,et al.  Computational anatomical methods as applied to ageing and dementia. , 2007, The British journal of radiology.

[34]  Jun Li,et al.  Brain Anatomical Network and Intelligence , 2009, NeuroImage.

[35]  J. Gore,et al.  Theoretical Model for Water Diffusion in Tissues , 1995, Magnetic resonance in medicine.

[36]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[37]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[38]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.

[39]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[40]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[41]  David G. Norris,et al.  An Investigation of Functional and Anatomical Connectivity Using Magnetic Resonance Imaging , 2002, NeuroImage.

[42]  D. Botstein,et al.  Comparing whole genomes using DNA microarrays , 2008, Nature Reviews Genetics.

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

[44]  D. Alexander.  A general framework for experiment design in diffusion MRI and its application in measuring direct tissue‐microstructure features , 2008, Magnetic resonance in medicine.

[45]  P. Hagmann.  From diffusion MRI to brain connectomics , 2005 .

[46]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Daniel C Alexander,et al.  Probabilistic anatomical connectivity derived from the microscopic persistent angular structure of cerebral tissue , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Geoffrey J M Parker,et al.  A framework for a streamline‐based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements , 2003, Journal of magnetic resonance imaging : JMRI.

[49]  S. Clarke,et al.  Intrinsic connectivity of human auditory areas: a tracing study with DiI , 2001, The European journal of neuroscience.

[50]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[51]  Daniel C. Alexander,et al.  Chapter 4 – Multiple Fibers: Beyond the Diffusion Tensor , 2009 .

[52]  V. Kiselev,et al.  Gibbs tracking: A novel approach for the reconstruction of neuronal pathways , 2008, Magnetic resonance in medicine.

[53]  Timothy Edward John Behrens,et al.  A Bayesian framework for global tractography , 2007, NeuroImage.

[54]  Jeremy D. Schmahmann,et al.  A Proposal for a Coordinated Effort for the Determination of Brainwide Neuroanatomical Connectivity in Model Organisms at a Mesoscopic Scale , 2009, PLoS Comput. Biol..

[55]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[56]  K. Brodmann.  Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[57]  D. Le Bihan.  Molecular diffusion, tissue microdynamics and microstructure. , 1995, NMR in biomedicine.

[58]  H. Moser,et al.  Imaging cortical association tracts in the human brain using diffusion‐tensor‐based axonal tracking , 2002, Magnetic resonance in medicine.

[59]  Thomas Schaffner,et al.  Cortical regions contributing to the anterior commissure in man , 1999, Experimental Brain Research.

[60]  Bruce R. Rosen,et al.  Diffusion anisotropy and white matter tracts , 1996, NeuroImage.

[61]  Gareth J. Barker,et al.  Estimating distributed anatomical connectivity using fast marching methods and diffusion tensor imaging , 2002, IEEE Transactions on Medical Imaging.

[62]  Scott N. Hwang,et al.  An image‐based finite difference model for simulating restricted diffusion , 2003, Magnetic resonance in medicine.

[63]  Colin Blakemore,et al.  Development of the human cerebral cortex: Boulder Committee revisited , 2008, Nature Reviews Neuroscience.

[64]  A. R. McIntosh,et al.  The effects of physiologically plausible connectivity structure on local and global dynamics in large scale brain models , 2009, Journal of Neuroscience Methods.

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

[66]  J. L. Conel,et al.  The postnatal development of the human cerebral cortex , 1960 .

[67]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[68]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Olaf Sporns,et al.  The small world of the cerebral cortex , 2007, Neuroinformatics.

[70]  C. Frith,et al.  Is autism a disconnection disorder? , 2004, The Lancet Neurology.

[71]  V. Wedeen,et al.  Diffusion MRI of Complex Neural Architecture , 2003, Neuron.

[72]  J. Thiran,et al.  Understanding diffusion MR imaging techniques: from scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. , 2006, Radiographics : a review publication of the Radiological Society of North America, Inc.

[73]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[74]  V. Menon,et al.  White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. , 2005, Cerebral cortex.

[75]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[76]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[77]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[78]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

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

[80]  Michael Jünger,et al.  Graph Drawing Software , 2003, Graph Drawing Software.

[81]  Edward T. Bullmore,et al.  Age-related changes in modular organization of human brain functional networks , 2009, NeuroImage.

[82]  P. Hagmann,et al.  Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[83]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[84]  H. Pfeifer.  Principles of Nuclear Magnetic Resonance Microscopy , 1992 .

[85]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[86]  Giorgio M. Innocenti,et al.  Exuberance in the development of cortical networks , 2005, Nature Reviews Neuroscience.

[87]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[88]  J. Pekar,et al.  MR color mapping of myelin fiber orientation. , 1991, Journal of computer assisted tomography.

[89]  Peter Boesiger,et al.  Resolving fiber crossing using advanced fast marching tractography based on diffusion tensor imaging , 2006, NeuroImage.

[90]  D. Cory,et al.  Measurement of translational displacement probabilities by NMR: An indicator of compartmentation , 1990, Magnetic resonance in medicine.

[91]  Jean-Philippe Thiran,et al.  DTI mapping of human brain connectivity: statistical fibre tracking and virtual dissection , 2003, NeuroImage.

[92]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[93]  A. Anwander,et al.  Connectivity-Based Parcellation of Broca's Area. , 2006, Cerebral cortex.

[94]  M. P. van den Heuvel,et al.  Microstructural Organization of the Cingulum Tract and the Level of Default Mode Functional Connectivity , 2008, The Journal of Neuroscience.

[95]  J. Brian,et al.  Decreased brain coordinated activity in autism spectrum disorders during executive tasks: reduced long-range synchronization in the fronto-parietal networks. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[96]  Larry W Swanson,et al.  From gene networks to brain networks , 2003, Nature Neuroscience.

[97]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[98]  Isabelle Bloch,et al.  Towards inference of human brain connectivity from MR diffusion tensor data , 2001, Medical Image Anal..

[99]  E. Bullmore,et al.  Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia , 2008, The Journal of Neuroscience.

[100]  Maria Argyropoulou,et al.  Myelination process in preterm subjects with periventricular leucomalacia assessed by magnetization transfer ratio , 2006, Pediatric Radiology.

[101]  Denis Le Bihan,et al.  Looking into the functional architecture of the brain with diffusion MRI , 2003, Nature Reviews Neuroscience.

[102]  G Tononi,et al.  Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. , 2000, Cerebral cortex.

[103]  S. Strogatz.  Exploring complex networks , 2001, Nature.

[104]  O. Sporns,et al.  Dynamical consequences of lesions in cortical networks , 2008, Human brain mapping.

[105]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[106]  D. Geschwind,et al.  Autism spectrum disorders: developmental disconnection syndromes , 2007, Current Opinion in Neurobiology.

[107]  R. McCarley,et al.  A review of MRI findings in schizophrenia , 2001, Schizophrenia Research.

[108]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[109]  F. Crick,et al.  Backwardness of human neuroanatomy , 1993, Nature.

[110]  C. Hutchison.  DNA sequencing: bench to bedside and beyond , 2007, Nucleic acids research.

[111]  Gareth J. Barker,et al.  Diffusion tensor imaging in schizophrenia , 2008, European Psychiatry.

[112]  Vladimir Batagelj,et al.  Pajek - Analysis and Visualization of Large Networks , 2001, Graph Drawing Software.

[113]  J. Polimeni,et al.  96‐Channel receive‐only head coil for 3 Tesla: Design optimization and evaluation , 2009, Magnetic resonance in medicine.

[114]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.