Connectivity precedes function in the development of the visual word form area

What determines the cortical location where a given functionally specific region will arise in development? Here we test the hypothesis that functionally specific regions develop in their characteristic locations because of pre-existing differences in the extrinsic connectivity of that region to the rest of the brain. We exploit the Visual Word Form Area (VWFA) as a test case, scanning children with diffusion and functional imaging at age five, before they learned to read, and at age 8, after they learned to read. We find the VWFA develops functionally in this interval and that its location in a particular child at age 8 can be predicted from that child’s connectivity fingerprints (but not functional responses) at age 5. These results suggest that early connectivity instructs the functional development of the VWFA, possibly reflecting a general mechanism of cortical development. Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms Correspondence should be addressed to Z.M.S. (zsaygin@mit.edu). AUTHOR CONTRIBUTIONS Z.M.S., D.E.O., and N.K designed the experiments. Z.M.S., E.S.N, D.A.Y., S.D.B., N.G., J.D.E.G. and N.K. conducted the experiments or supplied data. Z.M.S., D.E.O., D.A.Y., and J.F. analyzed the data. Z.M.S., D.E.O., and N.K. wrote the manuscript. COMPETING FINANCIAL INTERESTS The authors declare no competing financial interests. A Supplementary Methods Checklist is available. HHS Public Access Author manuscript Nat Neurosci. Author manuscript; available in PMC 2017 March 01. Published in final edited form as: Nat Neurosci. 2016 September ; 19(9): 1250–1255. doi:10.1038/nn.4354. A uhor M anscript

[1]  Amir Amedi,et al.  Origins of the specialization for letters and numbers in ventral occipitotemporal cortex , 2015, Trends in Cognitive Sciences.

[2]  D. Plaut,et al.  Distributed circuits, not circumscribed centers, mediate visual recognition , 2013, Trends in Cognitive Sciences.

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

[4]  Brian A. Wandell,et al.  Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections , 2013, Brain and Language.

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

[6]  David E. Osher,et al.  Tracking the Roots of Reading Ability: White Matter Volume and Integrity Correlate with Phonological Awareness in Prereading and Early-Reading Kindergarten Children , 2013, The Journal of Neuroscience.

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

[8]  Bruce Fischl,et al.  Highly accurate inverse consistent registration: A robust approach , 2010, NeuroImage.

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

[10]  Bruce Fischl,et al.  Volumetric navigators for prospective motion correction and selective reacquisition in neuroanatomical MRI , 2012, Magnetic resonance in medicine.

[11]  Hiroyuki Kidokoro,et al.  Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different neonatal intensive care unit environments. , 2014, The Journal of pediatrics.

[12]  Satrajit S. Ghosh,et al.  Nipype: A Flexible, Lightweight and Extensible Neuroimaging Data Processing Framework in Python , 2011, Front. Neuroinform..

[13]  B. Avants,et al.  Longitudinal reproducibility and accuracy of pseudo-continuous arterial spin-labeled perfusion MR imaging in typically developing children. , 2012, Radiology.

[14]  Alessandra Angelucci,et al.  Induction of visual orientation modules in auditory cortex , 2000, Nature.

[15]  Gabriel Kreiman,et al.  Differential Gene Expression in the Developing Lateral Geniculate Nucleus and Medial Geniculate Nucleus Reveals Novel Roles for Zic4 and Foxp2 in Visual and Auditory Pathway Development , 2009, The Journal of Neuroscience.

[16]  M. Sur,et al.  A map of visual space induced in primary auditory cortex. , 1990, Science.

[17]  Cyril Poupon,et al.  Anatomical Connections of the Visual Word Form Area , 2014, The Journal of Neuroscience.

[18]  Paul A. Yushkevich,et al.  Multi-atlas segmentation with joint label fusion and corrective learning—an open source implementation , 2013, Front. Neuroinform..

[19]  Arno Klein,et al.  Large-scale evaluation of ANTs and FreeSurfer cortical thickness measurements , 2014, NeuroImage.

[20]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.

[21]  Maximilian Riesenhuber,et al.  Adding Words to the Brain's Visual Dictionary: Novel Word Learning Selectively Sharpens Orthographic Representations in the VWFA , 2015, The Journal of Neuroscience.

[22]  R. Woodcock Woodcock Reading Mastery Tests-Revised , 1987 .

[23]  Bruce Fischl,et al.  Avoiding asymmetry-induced bias in longitudinal image processing , 2011, NeuroImage.

[24]  Timothy Edward John Behrens,et al.  Task-free MRI predicts individual differences in brain activity during task performance , 2016, Science.

[25]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

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

[27]  A W Roe,et al.  Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  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.

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

[30]  K. Grill-Spector,et al.  Two New Cytoarchitectonic Areas on the Human Mid‐Fusiform Gyrus , 2015, Cerebral cortex.

[31]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

[32]  Philippe Pinel,et al.  Cortical representations of symbols, objects, and faces are pruned back during early childhood. , 2011, Cerebral cortex.

[33]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[34]  André J. W. van der Kouwe,et al.  Brain morphometry with multiecho MPRAGE , 2008, NeuroImage.

[35]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[36]  Maximilian Riesenhuber,et al.  Individual Variability in Location Impacts Orthographic Selectivity in the “Visual Word Form Area” , 2013, The Journal of Neuroscience.

[37]  Bradford Z. Mahon,et al.  What drives the organization of object knowledge in the brain? , 2011, Trends in Cognitive Sciences.

[38]  Justin L. Vincent,et al.  Novel domain formation reveals proto-architecture in inferotemporal cortex , 2014, Nature Neuroscience.

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

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

[41]  Nicolas Langer,et al.  White Matter Alterations in Infants at Risk for Developmental Dyslexia , 2015, Cerebral cortex.

[42]  Brian B. Avants,et al.  The Multimodal Brain Tumor Image Segmentation Benchmark (BRATS) , 2015, IEEE Transactions on Medical Imaging.

[43]  Laurie S. Glezer,et al.  Evidence for Highly Selective Neuronal Tuning to Whole Words in the “Visual Word Form Area” , 2009, Neuron.

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

[45]  Nancy Kanwisher,et al.  Structural Connectivity Fingerprints Predict Cortical Selectivity for Multiple Visual Categories across Cortex. , 2016, Cerebral cortex.

[46]  Thomas L. Griffiths,et al.  Supplementary Information for Natural Speech Reveals the Semantic Maps That Tile Human Cerebral Cortex , 2022 .

[47]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[48]  J. Gee,et al.  The Insight ToolKit image registration framework , 2014, Front. Neuroinform..

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

[50]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[51]  N. Kanwisher,et al.  Visual word processing and experiential origins of functional selectivity in human extrastriate cortex , 2007, Proceedings of the National Academy of Sciences.

[52]  S Thesen,et al.  Prospective acquisition correction for head motion with image‐based tracking for real‐time fMRI , 2000, Magnetic resonance in medicine.

[53]  Jeffrey T Duda,et al.  Associations between children's socioeconomic status and prefrontal cortical thickness. , 2013, Developmental science.

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