Enhanced and unified anatomical labeling for a common mouse brain atlas

Anatomical atlases in standard coordinates are necessary for the interpretation and integration of research findings in a common spatial context. However, the two most-used mouse brain atlases, the Franklin-Paxinos (FP) and the common coordinate framework (CCF) from the Allen Institute for Brain Science, have accumulated inconsistencies in anatomical delineations and nomenclature, creating confusion among neuroscientists. To overcome these issues, we adopt here the FP labels into the CCF to merge the labels in the single atlas framework. We use cell type-specific transgenic mice and an MRI atlas to adjust and further segment our labels. Moreover, detailed segmentations are added to the dorsal striatum using cortico-striatal connectivity data. Lastly, we digitize our anatomical labels based on the Allen ontology, create a web-interface for visualization, and provide tools for comprehensive comparisons between the CCF and FP labels. Our open-source labels signify a key step towards a unified mouse brain atlas. Anatomical brain atlases elucidate the anatomical and functional organisation across species but different atlases have conflicting anatomical border and 3D coordinates. The authors integrated two atlases into a unified and highly segmented anatomical labelling system of the mouse brain.

[1]  Cheuk Y. Tang,et al.  Mapping of Brain Activity by Automated Volume Analysis of Immediate Early Genes , 2016, Cell.

[2]  Markus Aswendt,et al.  Processing Pipeline for Atlas-Based Imaging Data Analysis of Structural and Functional Mouse Brain MRI (AIDAmri) , 2019, Front. Neuroinform..

[3]  Arthur W. Toga,et al.  Digital Atlases as a Framework for Data Sharing , 2008, Front. Neurosci..

[4]  Marc Modat,et al.  aMAP is a validated pipeline for registration and segmentation of high-resolution mouse brain data , 2016, Nature Communications.

[5]  Hong-wei Dong,et al.  Topography of projections from amygdala to bed nuclei of the stria terminalis , 2001, Brain Research Reviews.

[6]  H. Schröder,et al.  The Mouse Cerebral Cortex , 2020 .

[7]  James G. King,et al.  Reconstruction and Simulation of Neocortical Microcircuitry , 2015, Cell.

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

[9]  Nicholas N. Foster,et al.  Integration of gene expression and brain-wide connectivity reveals the multiscale organization of mouse hippocampal networks , 2018, Nature Neuroscience.

[10]  W. Węglarz,et al.  A three-dimensional stereotaxic atlas of the gray short-tailed opossum (Monodelphis domestica) brain , 2017, Brain Structure and Function.

[11]  Brian S. Eastwood,et al.  Topographic precision in sensory and motor corticostriatal projections varies across cell type and cortical area , 2018, Nature Communications.

[12]  Tianyi Mao,et al.  A comprehensive excitatory input map of the striatum reveals novel functional organization , 2016, eLife.

[13]  Jack R Glaser,et al.  Automatic navigation system for the mouse brain , 2018, bioRxiv.

[14]  E. G. Jones.  Cerebral Cortex , 1987, Cerebral Cortex.

[15]  J. Coyle,et al.  Developmental expression of somatostatin in mouse brain. I. Immunocytochemical studies. , 1990, Brain research. Developmental brain research.

[16]  Yoav Freund,et al.  An active texture-based digital atlas enables automated mapping of structures and markers across brains , 2019, Nature Methods.

[17]  Richard A. Baldock,et al.  Cyberinfrastructure for the digital brain: spatial standards for integrating rodent brain atlases , 2014, Front. Neuroinform..

[18]  Miao He,et al.  Brain-wide Maps Reveal Stereotyped Cell-Type-Based Cortical Architecture and Subcortical Sexual Dimorphism , 2017, Cell.

[19]  Henry Markram,et al.  A Cell Atlas for the Mouse Brain , 2018, Front. Neuroinform..

[20]  James W. Phillips,et al.  A repeated molecular architecture across thalamic pathways , 2019, Nature Neuroscience.

[21]  P. Hof.  Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains , 2000 .

[22]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[23]  L. Puelles,et al.  Molecular anatomy of the thalamic complex and the underlying transcription factors , 2015, Brain Structure and Function.

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

[25]  James E. Fitzgerald,et al.  Whole-brain activity mapping onto a zebrafish brain atlas , 2015, Nature Methods.

[26]  Trygve B. Leergaard,et al.  Navigating the Murine Brain: Toward Best Practices for Determining and Documenting Neuroanatomical Locations in Experimental Studies , 2018, Front. Neuroanat..

[27]  Brian S. Eastwood,et al.  Whole mouse brain reconstruction and registration to a reference atlas with standard histochemical processing of coronal sections , 2019, The Journal of comparative neurology.

[28]  Brian Zingg,et al.  Inhibitory gain modulation of defense behaviors by zona incerta , 2018, Nature Communications.

[29]  Mapping gene expression in the CNS: Tools and data from the Allen Institute for Brain Science , 2010, Neuroscience Research.

[30]  Larry W. Swanson,et al.  Brain Maps: Structure of the Rat Brain , 1992 .

[31]  Smadar Shiffman,et al.  An automated mapping method for Nissl-stained mouse brain histologic sections , 2018, Journal of Neuroscience Methods.

[32]  G. Allan Johnson,et al.  Digital Atlasing and Standardization in the Mouse Brain , 2011, PLoS Comput. Biol..

[33]  K. Hsu,et al.  Conditional Deletion of Hippocampal CA2/CA3a Oxytocin Receptors Impairs the Persistence of Long-Term Social Recognition Memory in Mice , 2017, The Journal of Neuroscience.

[34]  Paul H. E. Tiesinga,et al.  The Scalable Brain Atlas: Instant Web-Based Access to Public Brain Atlases and Related Content , 2013, Neuroinformatics.

[35]  A. Lüthi,et al.  Neuronal circuits for fear and anxiety , 2015, Nature Reviews Neuroscience.

[36]  Nicholas N. Foster,et al.  The mouse cortico-striatal projectome , 2016, Nature Neuroscience.

[37]  Staci A. Sorensen,et al.  Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation , 2014, Front. Neural Circuits.

[38]  Andrew L. Janke,et al.  An ontologically consistent MRI-based atlas of the mouse diencephalon , 2017, NeuroImage.

[39]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

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

[41]  S. Nelson,et al.  A Resource of Cre Driver Lines for Genetic Targeting of GABAergic Neurons in Cerebral Cortex , 2011, Neuron.

[42]  Hong Wei Dong,et al.  Allen reference atlas : a digital color brain atlas of the C57Black/6J male mouse , 2008 .

[43]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[44]  Max A. Viergever,et al.  elastix: A Toolbox for Intensity-Based Medical Image Registration , 2010, IEEE Transactions on Medical Imaging.

[45]  Harry B. M. Uylings,et al.  Comparison of (stereotactic) parcellations in mouse prefrontal cortex , 2014, Brain Structure and Function.

[46]  Andrew L. Janke,et al.  A segmentation protocol and MRI atlas of the C57BL/6J mouse neocortex , 2013, NeuroImage.

[47]  Karl Deisseroth,et al.  An interactive framework for whole-brain maps at cellular resolution , 2017, Nature Neuroscience.

[48]  Nima Azimi,et al.  Discrepancies in stereotaxic coordinate publications and improving precision using an animal-specific atlas , 2017, Journal of Neuroscience Methods.

[49]  Laszlo Zaborszky,et al.  The Input-Output Relationship of the Cholinergic Basal Forebrain. , 2017, Cell reports.

[50]  Ian R. Wickersham,et al.  The BRAIN Initiative Cell Census Consortium: Lessons Learned toward Generating a Comprehensive Brain Cell Atlas , 2017, Neuron.

[51]  Anders M. Dale,et al.  Three-Dimensional Atlas System for Mouse and Rat Brain Imaging Data , 2007, Frontiers Neuroinformatics.

[52]  G. Allan Johnson,et al.  Waxholm Space: An image-based reference for coordinating mouse brain research , 2010, NeuroImage.

[53]  Gary F. Egan,et al.  Segmentation of the C57BL/6J mouse cerebellum in magnetic resonance images , 2012, NeuroImage.

[54]  A. Keller,et al.  Zona incerta: a role in central pain. , 2009, Journal of neurophysiology.

[55]  M. Ananth,et al.  Basal Forebrain Cholinergic Circuits and Signaling in Cognition and Cognitive Decline , 2016, Neuron.

[56]  Srinivas C. Turaga,et al.  Mapping social behavior-induced brain activation at cellular resolution in the mouse. , 2014, Cell reports.

[57]  R. Mark Henkelman,et al.  High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice , 2008, NeuroImage.

[58]  L. Swanson,et al.  Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: I. cytoarchitecture , 1989, The Journal of comparative neurology.

[59]  Partha P. Mitra,et al.  Comparative three-dimensional connectome map of motor cortical projections in the mouse brain , 2016, Scientific Reports.

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

[61]  Jason Tucciarone,et al.  Strategies and Tools for Combinatorial Targeting of GABAergic Neurons in Mouse Cerebral Cortex , 2016, Neuron.

[62]  Lydia Ng,et al.  Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system , 2012, Nucleic Acids Res..