Histology‐Based Average Template of the Marmoset Cortex With Probabilistic Localization of Cytoarchitectural Areas

The rapid adoption of marmosets in neuroscience has created a demand for three dimensional (3D) atlases of the brain of this species to facilitate data integration in a common reference space. We report on a new open access template of the marmoset cortex (the Nencki–Monash, or NM template), representing a morphological average of 20 brains of young adult individuals, obtained by 3D reconstructions generated from Nissl-stained serial sections. The method used to generate the template takes into account morphological features of the individual brains, as well as the borders of clearly defined cytoarchitectural areas. This has resulted in a resource which allows direct estimates of the most likely coordinates of each cortical area, as well as quantification of the margins of error involved in assigning voxels to areas, and preserves quantitative information about the laminar structure of the cortex. We provide spatial transformations between the NM and other available marmoset brain templates, thus enabling integration with magnetic resonance imaging (MRI) and tracer-based connectivity data. The NM template combines some of the main advantages of histology-based atlases (e.g. information about the cytoarchitectural structure) with features more commonly associated with MRI-based templates (isotropic nature of the dataset, and probabilistic analyses). The underlying workflow may be found useful in the future development of brain atlases that incorporate information about the variability of areas in species for which it may be impractical to ensure homogeneity of the sample in terms of age, sex and genetic background. Graphical abstract Highlights A 3D template of the marmoset cortex representing the average of 20 individuals. The template is based on Nissl stain and preserves information about cortical layers. Probabilistic mapping of areas, cortical thickness, and layer intensity profiles. Includes spatial transformations to other marmoset brain atlases. Abbreviations For a list of areas and their abbreviations see Table S2.

[1]  C. Galletti,et al.  Connections of the Dorsomedial Visual Area: Pathways for Early Integration of Dorsal and Ventral Streams in Extrastriate Cortex , 2009, The Journal of Neuroscience.

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

[3]  William J. Schroeder,et al.  Overview of Visualization , 2005, The Visualization Handbook.

[4]  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.

[5]  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.

[6]  Lisa A. de la Mothe,et al.  Thalamic connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[7]  Tristan A. Chaplin,et al.  A Conserved Pattern of Differential Expansion of Cortical Areas in Simian Primates , 2013, The Journal of Neuroscience.

[8]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[9]  D. Louis Collins,et al.  Brain templates and atlases , 2012, NeuroImage.

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

[11]  Elise G. Rowe,et al.  Rapid Adaptation Induces Persistent Biases in Population Codes for Visual Motion , 2016, The Journal of Neuroscience.

[12]  Barbara L. Finlay,et al.  Systematic, balancing gradients in neuron density and number across the primate isocortex , 2012, Front. Neuroanat..

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

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

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

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

[17]  Qinmu Peng,et al.  Population-averaged macaque brain atlas with high-resolution ex vivo DTI integrated into in vivo space , 2017, Brain Structure and Function.

[18]  Xia Li,et al.  Enhancement of histological volumes through averaging and their use for the analysis of magnetic resonance images. , 2009, Magnetic resonance imaging.

[19]  Hongkui Zeng,et al.  Neuroinformatics of the Allen Mouse Brain Connectivity Atlas. , 2015, Methods.

[20]  Marcello G P Rosa,et al.  Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications. , 2006, Cerebral cortex.

[21]  Kazuhiko Seki,et al.  Generation of transgenic marmosets using a tetracyclin-inducible transgene expression system as a neurodegenerative disease model† , 2017, Biology of Reproduction.

[22]  M. Poo,et al.  Local homogeneity of tonotopic organization in the primary auditory cortex of marmosets , 2019, Proceedings of the National Academy of Sciences.

[23]  A. Angelucci,et al.  Top-down feedback controls spatial summation and response amplitude in primate visual cortex , 2018, Nature Communications.

[24]  Hsin-Hao Yu,et al.  Cortical input to the frontal pole of the marmoset monkey. , 2011, Cerebral Cortex.

[25]  Ramón y Cajal,et al.  Histologie du système nerveux de l'homme & des vertébrés , 1909 .

[26]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[27]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

[28]  Daniel Glen,et al.  Three-Dimensional Digital Template Atlas of the Macaque Brain , 2016, Cerebral cortex.

[29]  F. Clascá,et al.  Cytoarchitecture and myeloarchitecture of the entorhinal cortex of the common marmoset monkey (Callithrix jacchus) , 2019, The Journal of comparative neurology.

[30]  Matthew L. Baker,et al.  Ab Initio Modeling of the Herpesvirus VP26 Core Domain Assessed by CryoEM Density , 2006, PLoS Comput. Biol..

[31]  Kathleen J. Burman,et al.  The cortical motor system of the marmoset monkey (Callithrix jacchus) , 2015, Neuroscience Research.

[32]  Stefan Everling,et al.  Electrical microstimulation evokes saccades in posterior parietal cortex of common marmosets. , 2019, Journal of neurophysiology.

[33]  Sophia Bakola,et al.  Cortical and thalamic projections to cytoarchitectural areas 6Va and 8C of the marmoset monkey: Connectionally distinct subdivisions of the lateral premotor cortex , 2015, The Journal of comparative neurology.

[34]  Matthew W Spitzer,et al.  Anatomical and physiological definition of the motor cortex of the marmoset monkey , 2008, The Journal of comparative neurology.

[35]  A. Iriki,et al.  Current models of the marmoset brain , 2015, Neuroscience Research.

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

[37]  Yoshinao Kajikawa,et al.  Cortical connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[38]  M. Keller,et al.  The main but not the accessory olfactory system is involved in the processing of socially relevant chemosignals in ungulates , 2012, Front. Neuroanat..

[39]  Jesper L. R. Andersson,et al.  A template for spatial normalisation of MR images of the rat brain , 2003, Journal of Neuroscience Methods.

[40]  Jeremy F. P. Ullmann,et al.  Robust methods to create ex vivo minimum deformation atlases for brain mapping. , 2015, Methods.

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

[42]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[43]  David A. Leopold,et al.  Functional magnetic resonance imaging of auditory cortical fields in awake marmosets , 2017, NeuroImage.

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

[45]  Hideyuki Okano,et al.  Mapping orbitofrontal-limbic maturation in non-human primates: A longitudinal magnetic resonance imaging study , 2017, NeuroImage.

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

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

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

[49]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  Partha P. Mitra,et al.  Open access resource for cellular-resolution analyses of corticocortical connectivity in the marmoset monkey , 2020, Nature Communications.

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

[52]  Sophia Bakola,et al.  Patterns of afferent input to the caudal and rostral areas of the dorsal premotor cortex (6DC and 6DR) in the marmoset monkey , 2014, The Journal of comparative neurology.

[53]  J R Wolff,et al.  Pre‐ and postnatal development of the primary visual cortex of the common marmoset. I. A changing space for synaptogenesis , 1993, The Journal of comparative neurology.

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

[55]  William Schroeder,et al.  The Visualization Toolkit: An Object-Oriented Approach to 3-D Graphics , 1997 .

[56]  Cory T. Miller,et al.  Optogenetic manipulation of neural circuits in awake marmosets. , 2016, Journal of neurophysiology.

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

[58]  Alan C. Evans,et al.  Mapping Cortical Laminar Structure in the 3D BigBrain , 2018, Cerebral cortex.

[59]  Douglas L. Rosene,et al.  Age-related effects on cortical thickness patterns of the Rhesus monkey brain , 2012, Neurobiology of Aging.

[60]  David A. Leopold,et al.  A digital 3D atlas of the marmoset brain based on multi-modal MRI , 2018, NeuroImage.

[61]  Matthew F. Glasser,et al.  Parcellating Cerebral Cortex: How Invasive Animal Studies Inform Noninvasive Mapmaking in Humans , 2018, Neuron.

[62]  Atsushi Iriki,et al.  Population-averaged standard template brain atlas for the common marmoset (Callithrix jacchus) , 2011, NeuroImage.

[63]  I. Aharon,et al.  Three‐dimensional mapping of cortical thickness using Laplace's Equation , 2000, Human brain mapping.

[64]  David Kulp,et al.  Innovations in Primate Interneuron Repertoire , 2019, bioRxiv.

[65]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

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

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

[68]  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.

[69]  J. Gee,et al.  Geodesic estimation for large deformation anatomical shape averaging and interpolation , 2004, NeuroImage.

[70]  K Amunts,et al.  A stereological approach to human cortical architecture: identification and delineation of cortical areas , 2000, Journal of Chemical Neuroanatomy.

[71]  David A. Leopold,et al.  A population MRI brain template and analysis tools for the macaque , 2017, NeuroImage.

[72]  David A. Leopold,et al.  Marmosets: A Neuroscientific Model of Human Social Behavior , 2016, Neuron.

[73]  Joseph S. Gati,et al.  Comparison of resting-state functional connectivity in marmosets with tracer-based cellular connectivity , 2020, NeuroImage.

[74]  Akiya Watakabe,et al.  Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks , 2018, Nature Communications.

[75]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..