Comparing structural and functional graph theory features in the human brain using multimodal MRI

Recent advances in magnetic resonance imaging (MRI) are allowing neuroscientists to gain critical insights into the neural networks mediating a variety of cognitive processes. This work investigates structural and functional connectivity in the human brain under different experimental conditions through multimodal MRI acquisitions. To define the nodes of a full-brain network, a set of regions was identified from resting-state functional MRI (fMRI) data using spatial independent component analysis (sICA) and a hierarchical clustering technique. Diffusion-weighted imaging (DWI) data were acquired from the same subjects and a probabilistic fiber tracking method was used to estimate the structure of this network. Using features originating from graph theory, such as small-world properties and network efficiency, we characterized the structural and functional connectivities of the full-brain network and we compared them quantitatively. We showed that structural and functional networks shared some properties in terms of topology as measured by the distribution of the node degrees, hence supporting the existence of an underlying anatomical substrate for functional networks.

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

[2]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

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

[4]  Rachid Deriche,et al.  Deterministic and Probabilistic Tractography Based on Complex Fibre Orientation Distributions , 2009, IEEE Transactions on Medical Imaging.

[5]  C. J. Stam,et al.  Functional connectivity patterns of human magnetoencephalographic recordings: a ‘small-world’ network? , 2004, Neuroscience Letters.

[6]  K. Sneppen,et al.  Specificity and Stability in Topology of Protein Networks , 2002, Science.

[7]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[8]  Habib Benali,et al.  NEDICA: Detection of group functional networks in FMRI using spatial independent component analysis , 2008, 2008 5th IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[9]  Geoff J. M. Parker,et al.  Characterizing function–structure relationships in the human visual system with functional MRI and diffusion tensor imaging , 2004, NeuroImage.

[10]  G. Schwarz Estimating the Dimension of a Model , 1978 .

[11]  Albert-László Barabási,et al.  Hierarchical organization in complex networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[13]  H E Stanley,et al.  Classes of small-world networks. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

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

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

[17]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[18]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

[19]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[20]  Martin Suter,et al.  Small World , 2002 .

[21]  C. Stam,et al.  Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis , 2006, Neuroscience Letters.

[22]  Liang Wang,et al.  Parcellation‐dependent small‐world brain functional networks: A resting‐state fMRI study , 2009, Human brain mapping.

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

[24]  John S. Duncan,et al.  Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo , 2003, NeuroImage.

[25]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[26]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[27]  Aapo Hyvärinen,et al.  Independent component analysis of fMRI group studies by self-organizing clustering , 2005, NeuroImage.

[28]  G. Edelman,et al.  Theoretical neuroanatomy and the connectivity of the cerebral cortex , 2002, Behavioural Brain Research.

[29]  Kyungsik Kim,et al.  Comparison of the small-world topology between anatomical and functional connectivity in the human brain , 2008 .

[30]  Guillaume Marrelec,et al.  Contribution of Exploratory Methods to the Investigation of Extended Large-Scale Brain Networks in Functional MRI: Methodologies, Results, and Challenges , 2008, Int. J. Biomed. Imaging.

[31]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  H. Berendse,et al.  The application of graph theoretical analysis to complex networks in the brain , 2007, Clinical Neurophysiology.

[33]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[34]  O. Sporns,et al.  Identification and Classification of Hubs in Brain Networks , 2007, PloS one.

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

[36]  Habib Benali,et al.  CORSICA: correction of structured noise in fMRI by automatic identification of ICA components. , 2007, Magnetic resonance imaging.

[37]  A. Luria,et al.  The functional organization of the brain. , 1970, Scientific American.

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

[39]  Stephen M. Smith,et al.  The future of FMRI connectivity , 2012, NeuroImage.

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

[41]  S Makeig,et al.  Analysis of fMRI data by blind separation into independent spatial components , 1998, Human brain mapping.

[42]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[43]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[44]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[45]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[46]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[47]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[48]  John A. Hartigan,et al.  Clustering Algorithms , 1975 .

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

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

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

[52]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[53]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[54]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[55]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

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