Open access resource for cellular-resolution analyses of corticocortical connectivity in the marmoset monkey

Understanding the principles of neuronal connectivity requires tools for efficient quantification and visualization of large datasets. The primate cortex is particularly challenging due to its complex mosaic of areas, which in many cases lack clear boundaries. Here, we introduce a resource that allows exploration of results of 143 retrograde tracer injections in the marmoset neocortex. Data obtained in different animals are registered to a common stereotaxic space using an algorithm guided by expert delineation of histological borders, allowing accurate assignment of connections to areas despite interindividual variability. The resource incorporates tools for analyses relative to cytoarchitectural areas, including statistical properties such as the fraction of labeled neurons and the percentage of supragranular neurons. It also provides purely spatial (parcellation-free) data, based on the stereotaxic coordinates of 2 million labeled neurons. This resource helps bridge the gap between high-density cellular connectivity studies in rodents and imaging-based analyses of human brains. Understanding principles of neuronal connectivity requires tools for quantification and visualization of large datasets. Here, the authors introduce an online resource encompassing the coordinates of two million neurons labelled by tracer injections in the marmoset cortex, and analysis tools.

[1]  Bennett A Landman,et al.  Anatomical accuracy of standard-practice tractography algorithms in the motor system - A histological validation in the squirrel monkey brain. , 2019, Magnetic resonance imaging.

[2]  Elizabeth Jefferies,et al.  Situating the default-mode network along a principal gradient of macroscale cortical organization , 2016, Proceedings of the National Academy of Sciences.

[3]  Piotr Majka,et al.  Possum—A Framework for Three-Dimensional Reconstruction of Brain Images from Serial Sections , 2015, Neuroinformatics.

[4]  Cecil Chern-Chyi Yen,et al.  Anatomical and functional investigation of the marmoset default mode network , 2019, Nature Communications.

[5]  Partha P. Mitra,et al.  The Circuit Architecture of Whole Brains at the Mesoscopic Scale , 2014, Neuron.

[6]  Tristan A. Chaplin,et al.  Contrasting patterns of cortical input to architectural subdivisions of the area 8 complex: a retrograde tracing study in marmoset monkeys. , 2013, Cerebral cortex.

[7]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[8]  Allan R. Jones,et al.  A mesoscale connectome of the mouse brain , 2014, Nature.

[9]  Jon H. Kaas,et al.  The evolution of the complex sensory and motor systems of the human brain , 2008, Brain Research Bulletin.

[10]  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.

[11]  Arthur W. Toga,et al.  Neural Networks of the Mouse Neocortex , 2014, Cell.

[12]  M. Rosa,et al.  A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision , 2006, The European journal of neuroscience.

[13]  Yoshiro Shiba,et al.  A dimensional approach to modeling symptoms of neuropsychiatric disorders in the marmoset monkey , 2017, Developmental neurobiology.

[14]  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..

[15]  Olaf Sporns,et al.  Cerebral cartography and connectomics , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  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.

[17]  Randy L. Buckner,et al.  Parallel distributed networks resolved at high resolution reveal close juxtaposition of distinct regions , 2018, bioRxiv.

[18]  Piotr Majka,et al.  Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey , 2018, Brain Structure and Function.

[19]  Michael Petrides,et al.  The marmoset brain in stereotaxic coordinates , 2012 .

[20]  T. Preuss.  Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[21]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[22]  G. Luppino,et al.  Connectional heterogeneity of the ventral part of the macaque area 46. , 2013, Cerebral cortex.

[23]  Laurent Risser,et al.  In vivo localization of cortical areas using a 3D computerized atlas of the marmoset brain , 2019, Brain Structure and Function.

[24]  E T Bullmore,et al.  Trajectories and Milestones of Cortical and Subcortical Development of the Marmoset Brain From Infancy to Adulthood , 2018, Cerebral cortex.

[25]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[26]  Atsushi Iriki,et al.  The Brain/MINDS 3D digital marmoset brain atlas , 2018, Scientific Data.

[27]  David R. Haynor,et al.  Nonrigid multimodality image registration , 2001, SPIE Medical Imaging.

[28]  Hideyuki Okano,et al.  Investigation of brain science and neurological/psychiatric disorders using genetically modified non-human primates , 2018, Current Opinion in Neurobiology.

[29]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[30]  Markus Diesmann,et al.  CoCoMac 2.0 and the future of tract-tracing databases , 2012, Front. Neuroinform..

[31]  Marcello G P Rosa,et al.  Brain maps, great and small: lessons from comparative studies of primate visual cortical organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  Piotr Majka,et al.  Neuronal distribution across the cerebral cortex of the marmoset monkey (Callithrix jacchus) , 2018, bioRxiv.

[33]  Nikola T. Markov,et al.  Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex , 2013, The Journal of comparative neurology.

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

[35]  H. F. Song,et al.  Spatial embedding of structural similarity in the cerebral cortex , 2014, Proceedings of the National Academy of Sciences.

[36]  Ravi S. Menon,et al.  Frontoparietal Functional Connectivity in the Common Marmoset , 2016, Cerebral cortex.

[37]  C. Hilgetag,et al.  A blueprint of mammalian cortical connectomes , 2019, PLoS biology.

[38]  Steen Moeller,et al.  The Human Connectome Project: A data acquisition perspective , 2012, NeuroImage.

[39]  Sophia Bakola,et al.  Patterns of cortical input to the primary motor area in the marmoset monkey , 2014, The Journal of comparative neurology.

[40]  Lauretta Passarelli,et al.  Uniformity and Diversity of Cortical Projections to Precuneate Areas in the Macaque Monkey: What Defines Area PGm? , 2018, Cerebral cortex.

[41]  Nikola T. Markov,et al.  A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex , 2012, Cerebral cortex.

[42]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

[43]  Piotr Majka,et al.  Towards a comprehensive atlas of cortical connections in a primate brain: Mapping tracer injection studies of the common marmoset into a reference digital template , 2016, The Journal of comparative neurology.

[44]  Daniel S. Margulies,et al.  Gradients of connectivity distance in the cerebral cortex of the macaque monkey , 2018, Brain Structure and Function.

[45]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[46]  K. Saleem,et al.  Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey , 2008, The Journal of comparative neurology.

[47]  T. Kawecki,et al.  Behavior and neurobiology , 2009 .

[48]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[49]  Atsushi Iriki,et al.  A high-throughput neurohistological pipeline for brain-wide mesoscale connectivity mapping of the common marmoset , 2018, bioRxiv.

[50]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[51]  F. Arnaud,et al.  From core referencing to data re-use: two French national initiatives to reinforce paleodata stewardship (National Cyber Core Repository and LTER France Retro-Observatory) , 2017 .

[52]  H. Kuypers,et al.  Diamidino yellow dihydrochloride (DY·2HCl); a new fluorescent retrograde neuronal tracer, which migrates only very slowly out of the cell , 2004, Experimental Brain Research.

[53]  Lauretta Passarelli,et al.  Cortical Afferents and Myeloarchitecture Distinguish the Medial Intraparietal Area (MIP) from Neighboring Subdivisions of the Macaque Cortex , 2017, eNeuro.

[54]  Daniel S. Margulies,et al.  Macroscale cortical organization and a default-like apex transmodal network in the marmoset monkey , 2019, Nature Communications.

[55]  F. Condé.  Further studies on the use of the fluorescent tracers fast blue and diamidino yellow: Effective uptake area and cellular storage sites , 1987, Journal of Neuroscience Methods.

[56]  Piotr Majka,et al.  Common Atlas Format and 3D Brain Atlas Reconstructor: Infrastructure for Constructing 3D Brain Atlases , 2012, Neuroinformatics.

[57]  Kei Ito,et al.  Technical and Organizational Considerations for the Long-Term Maintenance and Development of Digital Brain Atlases and Web-Based Databases , 2010, Front. Syst. Neurosci..

[58]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[59]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[60]  Randy L. Buckner,et al.  The evolution of distributed association networks in the human brain , 2013, Trends in Cognitive Sciences.

[61]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[62]  J A Sethian,et al.  A fast marching level set method for monotonically advancing fronts. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Samuel G. Solomon,et al.  A simpler primate brain: the visual system of the marmoset monkey , 2014, Front. Neural Circuits..

[64]  M. Budde,et al.  Quantification of anisotropy and fiber orientation in human brain histological sections , 2012, Front. Integr. Neurosci..

[65]  H. Kennedy,et al.  A Large-Scale Circuit Mechanism for Hierarchical Dynamical Processing in the Primate Cortex , 2015, Neuron.

[66]  Erik Schultes,et al.  The FAIR Guiding Principles for scientific data management and stewardship , 2016, Scientific Data.

[67]  H. Gu,et al.  Large-Scale Brain Networks in the Awake, Truly Resting Marmoset Monkey , 2013, The Journal of Neuroscience.

[68]  Cory T. Miller,et al.  Marmoset vocal communication: Behavior and neurobiology , 2017, Developmental neurobiology.

[69]  Daniel S. Margulies,et al.  Gradients of connectivity distance are anchored in primary cortex , 2016, Brain Structure and Function.

[70]  Joseph S. Gati,et al.  Intrinsic Functional Boundaries of Lateral Frontal Cortex in the Common Marmoset Monkey , 2018, The Journal of Neuroscience.

[71]  Julian M. L. Budd,et al.  Communication and wiring in the cortical connectome , 2012, Front. Neuroanat..

[72]  Y. Temel,et al.  Serotonergic treatment normalizes midbrain dopaminergic neuron increase after periaqueductal gray stimulation , 2020, Brain Structure and Function.

[73]  Edward T. Bullmore,et al.  Statistical Analysis of Tract-Tracing Experiments Demonstrates a Dense, Complex Cortical Network in the Mouse , 2016, PLoS Comput. Biol..

[74]  David A. Leopold,et al.  A resource for detailed 3D mapping of white matter pathways in the marmoset brain , 2019, Nature Neuroscience.