Cytoarchitectonic similarity is a wiring principle of the human connectome

Understanding the wiring diagram of the human cerebral cortex is a fundamental challenge in neuroscience. Elemental aspects of its organization remain elusive. Here we examine which structural traits of cortical regions, particularly their cytoarchitecture and thickness, relate to the existence and strength of inter-regional connections. We use the architecture data from the classic work of von Economo and Koskinas and state-of-the-art diffusion-based connectivity data from the Human Connectome Project. Our results reveal a prominent role of the cytoarchitectonic similarity of supragranular layers for predicting the existence and strength of connections. In contrast, cortical thickness similarity was not related to the existence or strength of connections. These results are in line with findings for non-human mammalian cerebral cortices, suggesting overarching wiring principles of the mammalian cerebral cortex. The results invite hypotheses about evolutionary conserved neurobiological mechanisms that give rise to the relation of cytoarchitecture and connectivity in the human cerebral cortex.

[1]  G. Smith,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. , 1927 .

[2]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[3]  Claus C. Hilgetag,et al.  Principles of ipsilateral and contralateral cortico-cortical connectivity in the mouse , 2015, Brain Structure and Function.

[4]  Claus C. Hilgetag,et al.  Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex , 2010, NeuroImage.

[5]  Michael Petrides,et al.  Distinct Parietal and Temporal Connectivity Profiles of Ventrolateral Frontal Areas Involved in Language Production , 2013, The Journal of Neuroscience.

[6]  J. Rapoport,et al.  Simple models of human brain functional networks , 2012, Proceedings of the National Academy of Sciences.

[7]  Gustavo Deco,et al.  Rich club organization supports a diverse set of functional network configurations , 2014, NeuroImage.

[8]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[9]  C C Hilgetag,et al.  Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. , 2001, Cerebral cortex.

[10]  C. Hilgetag,et al.  A predictive model of the cat cortical connectome based on cytoarchitecture and distance , 2014, Brain Structure and Function.

[11]  D. Leopold,et al.  Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited , 2014, Proceedings of the National Academy of Sciences.

[12]  H. Barbas,et al.  Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure , 2006, The European journal of neuroscience.

[13]  H. Barbas General cortical and special prefrontal connections: principles from structure to function. , 2015, Annual review of neuroscience.

[14]  P. B. Cipolloni,et al.  Cerebral Cortex: Architecture, Connections, and the Dual Origin Concept , 2015 .

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

[16]  P. Rakic Progress: Neurogenesis in adult primate neocortex: an evaluation of the evidence , 2002, Nature Reviews Neuroscience.

[17]  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.

[18]  Chad J. Donahue,et al.  Using Diffusion Tractography to Predict Cortical Connection Strength and Distance: A Quantitative Comparison with Tracers in the Monkey , 2016, The Journal of Neuroscience.

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

[20]  F. Sanides Die Architektonik des Menschlichen Stirnhirns , 1962 .

[21]  M. P. van den Heuvel,et al.  Linking contemporary high resolution magnetic resonance imaging to the von economo legacy: A study on the comparison of MRI cortical thickness and histological measurements of cortical structure , 2015, Human brain mapping.

[22]  R. Caminiti,et al.  Areal differences in diameter and length of corticofugal projections. , 2012, Cerebral Cortex.

[23]  Thomas Nowotny,et al.  Influence of Wiring Cost on the Large-Scale Architecture of Human Cortical Connectivity , 2014, PLoS Comput. Biol..

[24]  Luciano da Fontoura Costa,et al.  Predicting the connectivity of primate cortical networks from topological and spatial node properties , 2007, BMC Systems Biology.

[25]  Claus C Hilgetag,et al.  Bridging Cytoarchitectonics and Connectomics in Human Cerebral Cortex , 2015, The Journal of Neuroscience.

[26]  Ruben Schmidt,et al.  Linking Macroscale Graph Analytical Organization to Microscale Neuroarchitectonics in the Macaque Connectome , 2014, The Journal of Neuroscience.

[27]  A. Campbell Histological Studies on the Localisation of Cerebral Function , 2009 .

[28]  Martijn P. van den Heuvel,et al.  Estimating false positives and negatives in brain networks , 2013, NeuroImage.

[29]  Gorka Zamora-López,et al.  Cortical Hubs Form a Module for Multisensory Integration on Top of the Hierarchy of Cortical Networks , 2009, Front. Neuroinform..

[30]  Claus C. Hilgetag,et al.  A Predictive Structural Model of the Primate Connectome , 2015, Scientific Reports.

[31]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[33]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

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

[35]  D. Pandya,et al.  Prefrontal cortex in relation to other cortical areas in rhesus monkey: architecture and connections. , 1990, Progress in brain research.

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

[37]  Alan C. Evans,et al.  BigBrain: An Ultrahigh-Resolution 3D Human Brain Model , 2013, Science.

[38]  Paul H. E. Tiesinga,et al.  The missing link: Predicting connectomes from noisy and partially observed tract tracing data , 2016, bioRxiv.

[39]  E. Bullmore,et al.  Wiring cost and topological participation of the mouse brain connectome , 2015, Proceedings of the National Academy of Sciences.

[40]  Edward T. Bullmore,et al.  Neuroinformatics Original Research Article , 2022 .

[41]  Xiaoping Hu,et al.  The effects of connection reconstruction method on the interregional connectivity of brain networks via diffusion tractography , 2012, Human brain mapping.

[42]  Jon H Kaas Cortical Areas and Patterns of Cortico-Cortical Connections , 2002 .

[43]  J. Rilling,et al.  Comparison of diffusion tractography and tract‐tracing measures of connectivity strength in rhesus macaque connectome , 2015, Human brain mapping.

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

[45]  Olaf Sporns,et al.  Generative models of the human connectome , 2015, NeuroImage.

[46]  H. Barbas,et al.  Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey , 2005, BMC Neuroscience.

[47]  Marcus Kaiser,et al.  Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems , 2006, PLoS Comput. Biol..

[48]  M. A. Macconaill Die Architektonik des menschlichen Stirnhirns , 1963 .

[49]  Barbara L Finlay,et al.  Systematic, cross-cortex variation in neuron numbers in rodents and primates. , 2015, Cerebral cortex.

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

[51]  E. Bullmore,et al.  The hubs of the human connectome are generally implicated in the anatomy of brain disorders , 2014, Brain : a journal of neurology.

[52]  C. Economo,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen , 1925 .