Abstract
The recently released Allen Mouse Brain Connectivity Atlas provides a comprehensive mouse brain neuronal connectivity map from brain-wide injection sites via anterograde tracers coupled with serial two-photon tomography. In addition, the Allen Mouse Brain Atlas offers a genome-wide gene expression database built upon a series of in situ hybridization images, covering comprehensive expression energy of over 4,000 genes in coronal sections and over 20,000 genes in sagittal sections across the whole mouse brain. These concurrent and co-registered datasets provide an unparalleled opportunity for systematically analyzing and characterizing spatial neuronal connectivity and gene expression patterns. Inspired by our recent macroscale neuroimaging results showing that there are significantly different structural and functional connectivity patterns on the gyri and sulci of cerebral cortex in primate brains, the present work systematically examines the axonal connectivity and gene expression patterns on gyri and sulci of the cerebellum. Our results demonstrate that the cerebellum gyri and sulci of rodent brains are significantly different in both axonal connectivity and gene expression patterns. This discovery enriches and extends our prior findings in macroscale neuroimaging studies in primates. Additionally, this work offers novel insights on the molecular and structural architectures of the cerebellum in particular and the brain in general.
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References
Allen Institute for Brain Science (2012a) Allen Brain Atlas API. http://www.brain-map.org/api/index.html
Allen Institute for Brain Science (2012b) Allen Mouse Brain Altas. http://mouse.brain-map.org
Allen Institute for Brain Science (2013a) Allen Mouse Brain Connectivity Atlas. http://connectivity.brain-map.org/
Allen Institute for Brain Science (2013b) Allen mouse brain connectivity atlas: technical white paper: informatics data processing
Bonnici HM, William T, Moorhead J, Stanfield AC, Harris JM, Owens DG, Johnstone EC, Lawrie SM (2007) Pre-frontal lobe gyrification index in schizophrenia, mental retardation and comorbid groups: an automated study. NeuroImage 35(2):648–654. doi:10.1016/j.neuroimage.2006.11.031
Budde MD, Frank JA (2012) Examining brain microstructure using structure tensor analysis of histological sections. Neuroimage 63(1):1–10
Calamante F, Tournier JD, Kurniawan ND, Yang ZY, Gyengesi E, Galloway GJ, Reutens DC, Connelly A (2012) Super-resolution track-density imaging studies of mouse brain: comparison to histology. Neuroimage 59(1):286–296
Callaway EM (2008) Transneuronal circuit tracing with neurotropic viruses. Curr Opin Neurobiol 18(6):617–623
Chen H, Zhang T, Guo L, Li K, Yu X, Li L, Hu X, Han J, Liu T (2013) Coevolution of gyral folding and structural connection patterns in primate brains. Cereb Cortex 23(5):1208–1217. doi:10.1093/cercor/bhs113
Deng F, Jiang X, Zhu D, Zhang T, Li K, Guo L, Liu T (2013) A functional model of cortical gyri and sulci. Brain structure and function
Dong H (2009) The Allen reference atlas: a digital brain atlas of the C57BL/6 J male mouse. Willey, New York
Fan RE, Chang KW, Hsieh CJ, Wang XR, Lin CJ (2008) LIBLINEAR: a library for large linear classification. J Mach Learn Res 9:1871–1874
Hansen B, Flint JJ, Heon-Lee C, Fey M, Vincent F, King MA, Vestergaard-Poulsen P, Blackband SJ (2011) Diffusion tensor microscopy in human nervous tissue with quantitative correlation based on direct histological comparison. Neuroimage 57(4):1458–1465
Hardan AY, Jou RJ, Keshavan MS, Varma R, Minshew NJ (2004) Increased frontal cortical folding in autism: a preliminary MRI study. Psychiatry Res 131(3):263–268. doi:10.1016/j.pscychresns.2004.06.001
Ji S, Fakhry A, Deng H (2014) Integrative analysis of the connectivity and gene expression atlases in the mouse brain. Neuroimage 84(1):245–253
Jones AR, Overly CC, Sunkin SM (2009) The Allen brain atlas: 5 years and beyond. Nat Rev Neurosci 10(11):821–828
Kaufman A, Dror G, Meilijson I, Ruppin E (2006) Gene expression of Caenorhabditis elegans neurons carries information on their synaptic connectivity. PLoS Comput Biol 2(12):1561–1567
Kobbert C, Apps R, Bechmann I, Lanciego JL, Mey J, Thanos S (2000) Current concepts in neuroanatomical tracing. Prog Neurobiol 62(4):327–351
Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445(7124):168–176
Meinshausen N, Buhlmann P (2010) Stability selection. J Roy Stat Soc Ser B Stat Methodol 72:417–473
Neal J, Takahashi M, Silva M, Tiao G, Walsh CA, Sheen VL (2007) Insights into the gyrification of developing ferret brain by magnetic resonance imaging. J Anat 210(1):66–77. doi:10.1111/j.1469-7580.2006.00674.x
Nie J, Guo L, Li K, Wang Y, Chen G, Li L, Chen H, Deng F, Jiang X, Zhang T, Huang L, Faraco C, Zhang D, Guo C, Yap PT, Hu X, Li G, Lv J, Yuan Y, Zhu D, Han J, Sabatinelli D, Zhao Q, Miller LS, Xu B, Shen P, Platt S, Shen D, Liu T (2012) Axonal fiber terminations concentrate on gyri. Cereb Cortex 22(12):2831–2839
Osten P, Margrie TW (2013) Mapping brain circuitry with a light microscope. Nat Methods 10(6):515–523
Rash BG, Rakic P (2014) Neuroscience. Genetic resolutions of brain convolutions. Science 343(6172):744–745. doi:10.1126/science.1250246
Rettmann ME, Kraut MA, Prince JL, Resnick SM (2006) Cross-sectional and longitudinal analyses of anatomical sulcal changes associated with aging. Cereb Cortex 16(11):1584–1594. doi:10.1093/cercor/bhj095
Schaer M, Schmitt JE, Glaser B, Lazeyras F, Delavelle J, Eliez S (2006) Abnormal patterns of cortical gyrification in velo-cardio-facial syndrome (deletion 22q11.2): an MRI study. Psychiatry Res 146(1):1–11. doi:10.1016/j.pscychresns.2005.10.002
Sereno MI, Tootell RBH (2005) From monkeys to humans: what do we now know about brain homologies? Curr Opin Neurobiol 15(2):135–144
Sotiropoulos SN, Jbabdi S, Xu J, Andersson JL, Moeller S, Auerbach EJ, Glasser MF, Hernandez M, Sapiro G, Jenkinson M, Feinberg DA, Yacoub E, Lenglet C, Van Essen DC, Ugurbil K, Behrens TE, Consortium WU-MH (2013) Advances in diffusion MRI acquisition and processing in the human connectome project. Neuroimage 80:125–143
Sunkin SM, Hohmann JG (2007) Insights from spatially mapped gene expression in the mouse brain. Hum Mol Genet 16 Spec No(2):R209–R219
Takahashi E, Folkerth RD, Galaburda AM, Grant PE (2012) Emerging cerebral connectivity in the human fetal brain: an MR tractography study. Cereb Cortex 22(2):455–464. doi:10.1093/cercor/bhr126
Thompson RH, Swanson LW (2010) Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc Natl Acad Sci USA 107(34):15235–15239
Tibshirani R (1996) Regression shrinkage and selection via the Lasso. J Roy Statist Soc Ser B Methodol 58(1):267–288
Ugolini G (2010) Advances in viral transneuronal tracing. J Neurosci Methods 194(1):2–20
Vercelli A, Repici M, Garbossa D, Grimaldi A (2000) Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51(1):11–28
Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong HW (2014) Neural networks of the mouse neocortex. Cell 156(5):1096–1111
Acknowledgments
We thank the Allen Institute for Brain Science for making the Allen Brain Atlas data available and Dr. Stephen Landowne for the editorial support. T. Liu was supported by NIH R01 DA-033393, NIH R01 AG-042599, NSF CAREER Award IIS-1149260, and NSF BME-1302089. S. Ji was supported by NSF DBI-1147134 and NSF DBI-1356621.
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429_2014_821_MOESM1_ESM.pdf
Joint visualization of connectivity from an injection site (colored volume) and reconstructed cerebella cortex (white surface). Connectivity energy is rescaled by logarithm and the color bar is on the right. As highlighted by purple arrows, stronger connection to the gyri on cerebellum can be observed in comparison with sulci (magenta arrow). Connectivity from an injection site mapped to the reconstructed cerebellum cortex. The energy has been rescaled by logarithm and the color bar is on the right. The injection site is the same as supplemental figure 1. As highlighted by yellow arrows, more connections can be observed on gyri than sulci (red arrows). (PDF 196 kb)
429_2014_821_MOESM2_ESM.xlsx
Gyrus and sulcus abbreviations and the numbers of voxels in each gyrus and sulcus. The numbers of connected viral tracer injection sites are also given. (XLSX 10 kb)
429_2014_821_MOESM3_ESM.xlsx
Correspondence among structure abbreviations used in manuscript, structure full names used in the ARA, and the acronyms used in the ARA. (XLSX 10 kb)
429_2014_821_MOESM4_ESM.xlsx
Ordered injection sites to all gyri and sulci. The overall neuronal connectivity strength from 1019 injection sites to all gyri and sulci were ordered for each gyrus and sulcus, and the names of corresponding brain structures are given. (XLSX 138 kb)
429_2014_821_MOESM5_ESM.xlsx
Three lists of marker genes that identify gyri from sulci, gyri from negative, and sulci from negative. In each list, the top 200 genes are provided. (XLSX 16 kb)
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Zeng, T., Chen, H., Fakhry, A. et al. Allen mouse brain atlases reveal different neural connection and gene expression patterns in cerebellum gyri and sulci. Brain Struct Funct 220, 2691–2703 (2015). https://doi.org/10.1007/s00429-014-0821-x
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DOI: https://doi.org/10.1007/s00429-014-0821-x