Structural Connectivity Fingerprints Predict Cortical Selectivity for Multiple Visual Categories across Cortex.

A fundamental and largely unanswered question in neuroscience is whether extrinsic connectivity and function are closely related at a fine spatial grain across the human brain. Using a novel approach, we found that the anatomical connectivity of individual gray-matter voxels (determined via diffusion-weighted imaging) alone can predict functional magnetic resonance imaging (fMRI) responses to 4 visual categories (faces, objects, scenes, and bodies) in individual subjects, thus accounting for both functional differentiation across the cortex and individual variation therein. Furthermore, this approach identified the particular anatomical links between voxels that most strongly predict, and therefore plausibly define, the neural networks underlying specific functions. These results provide the strongest evidence to date for a precise and fine-grained relationship between connectivity and function in the human brain, raise the possibility that early-developing connectivity patterns may determine later functional organization, and offer a method for predicting fine-grained functional organization in populations who cannot be functionally scanned.

[1]  Elinor McKone,et al.  Are Faces Special , 2011 .

[2]  R Clay Reid,et al.  From Functional Architecture to Functional Connectomics , 2012, Neuron.

[3]  Daniel D. Dilks,et al.  Differential selectivity for dynamic versus static information in face-selective cortical regions , 2011, NeuroImage.

[4]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

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

[6]  N. Kanwisher Functional specificity in the human brain: A window into the functional architecture of the mind , 2010, Proceedings of the National Academy of Sciences.

[7]  Nancy Kanwisher,et al.  An algorithmic method for functionally defining regions of interest in the ventral visual pathway , 2012, NeuroImage.

[8]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[9]  Alessandro Vespignani,et al.  Large scale networks fingerprinting and visualization using the k-core decomposition , 2005, NIPS.

[10]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[11]  M. Rushworth,et al.  Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks. , 2012, Cerebral cortex.

[12]  Lindsey L. Glickfeld,et al.  Cortico-cortical projections in mouse visual cortex are functionally target specific , 2013, Nature Neuroscience.

[13]  Adam G. Thomas,et al.  The Organization of Dorsal Frontal Cortex in Humans and Macaques , 2013, The Journal of Neuroscience.

[14]  K. Grill-Spector,et al.  The functional architecture of the ventral temporal cortex and its role in categorization , 2014, Nature Reviews Neuroscience.

[15]  Zeynep M. Saygin,et al.  Anatomical connectivity patterns predict face-selectivity in the fusiform gyrus , 2011, Nature Neuroscience.

[16]  Nancy Kanwisher,et al.  Divide and conquer: A defense of functional localizers , 2006, NeuroImage.

[17]  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.

[18]  Klaas E. Stephan,et al.  The anatomical basis of functional localization in the cortex , 2002, Nature Reviews Neuroscience.

[19]  N. Kanwisher,et al.  New method for fMRI investigations of language: defining ROIs functionally in individual subjects. , 2010, Journal of neurophysiology.

[20]  Kevin L. Briggman,et al.  Wiring specificity in the direction-selectivity circuit of the retina , 2011, Nature.

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

[22]  Saad Jbabdi,et al.  Long-range connectomics , 2013, Annals of the New York Academy of Sciences.

[23]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[24]  L. Regolin,et al.  Faces are special for newly hatched chicks: evidence for inborn domain-specific mechanisms underlying spontaneous preferences for face-like stimuli. , 2009, Developmental science.

[25]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[26]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

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

[28]  Robert Tibshirani,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction, 2nd Edition , 2001, Springer Series in Statistics.

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

[30]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[32]  Stephen B. Seidman,et al.  Network structure and minimum degree , 1983 .

[33]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[34]  Bruce Fischl,et al.  Improved tractography alignment using combined volumetric and surface registration , 2010, NeuroImage.

[35]  H. Sebastian Seung,et al.  Neuroscience: Towards functional connectomics , 2011, Nature.

[36]  Y. Sugita Face perception in monkeys reared with no exposure to faces , 2008, Proceedings of the National Academy of Sciences.

[37]  J. Budd,et al.  A numerical analysis of the geniculocortical input to striate cortex in the monkey. , 1994, Cerebral cortex.

[38]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[39]  E. Warrington,et al.  An Experimental Investigation of Facial Recognition in Patients with Unilateral Cerebral Lesions , 1967 .

[40]  Rainer Goebel,et al.  Measuring structural–functional correspondence: Spatial variability of specialised brain regions after macro-anatomical alignment , 2012, NeuroImage.

[41]  Bruce Fischl,et al.  Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography , 2011, NeuroImage.

[42]  D. R. Lick,et al.  k-Degenerate Graphs , 1970, Canadian Journal of Mathematics.

[43]  Katrin Amunts,et al.  The mid-fusiform sulcus: A landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex , 2014, NeuroImage.

[44]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[45]  Bruce Fischl,et al.  Combined Volumetric and Surface Registration , 2009, IEEE Transactions on Medical Imaging.

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

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

[48]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[49]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Parietal Cortex and Comparison with Human and Macaque Resting-State Functional Connectivity , 2011, The Journal of Neuroscience.

[50]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[51]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  F. Simion,et al.  Newborns’ face recognition over changes in viewpoint , 2008, Cognition.

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

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

[55]  R. Reid,et al.  Specificity and randomness: structure–function relationships in neural circuits , 2011, Current Opinion in Neurobiology.

[56]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[57]  Daniel D. Dilks,et al.  The Functional Organization of the Ventral Visual Pathway in Humans , 2012 .

[58]  Timothy E. J. Behrens,et al.  The topographic connectome , 2013, Current Opinion in Neurobiology.

[59]  Doris Y. Tsao,et al.  Neurons that keep a straight face , 2014, Proceedings of the National Academy of Sciences.

[60]  M. Sur,et al.  Experimentally induced visual projections into auditory thalamus and cortex. , 1988, Science.

[61]  T. V. Sewards Neural structures and mechanisms involved in scene recognition: A review and interpretation , 2011, Neuropsychologia.

[62]  Rogier B Mars,et al.  Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex , 2013, Proceedings of the National Academy of Sciences.

[63]  V. Wedeen,et al.  Reduction of eddy‐current‐induced distortion in diffusion MRI using a twice‐refocused spin echo , 2003, Magnetic resonance in medicine.

[64]  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.

[65]  Timothy E. J. Behrens,et al.  Human and Monkey Ventral Prefrontal Fibers Use the Same Organizational Principles to Reach Their Targets: Tracing versus Tractography , 2013, The Journal of Neuroscience.