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01-07-2014 | Original Article

An MRI atlas of the mouse basal ganglia

Authors: Jeremy F. P. Ullmann, Charles Watson, Andrew L. Janke, Nyoman D. Kurniawan, George Paxinos, David C. Reutens

Published in: Brain Structure and Function | Issue 4/2014

Abstract

The basal ganglia are a group of subpallial nuclei that play an important role in motor, emotional, and cognitive functions. Morphological changes and disrupted afferent/efferent connections in the basal ganglia have been associated with a variety of neurological disorders including psychiatric and movement disorders. While high-resolution magnetic resonance imaging has been used to characterize changes in brain structure in mouse models of these disorders, no systematic method for segmentation of the C57BL/6 J mouse basal ganglia exists. In this study we have used high-resolution MR images of ex vivo C57BL/6 J mouse brain to create a detailed protocol for segmenting the basal ganglia. We created a three-dimensional minimum deformation atlas, which includes the segmentation of 35 striatal, pallidal, and basal ganglia-related structures. In addition, we provide mean volumes, mean T₂ contrast intensities and mean FA and ADC values for each structure. This MR atlas is available for download, and enables researchers to perform automated segmentation in genetic models of basal ganglia disorders.

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Ahsan RL, Allom R, Gousias IS, Habib H, Turkheimer FE, Free S, Lemieux L, Myers R, Duncan JS, Brooks DJ, Koepp MJ, Hammers A (2007) Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus. NeuroImage 38(2):261–270PubMedCrossRef

Antonsen BT, Jiang Y, Veraart J, Qu H, Nguyen HP, Sijbers J, von Horsten S, Johnson GA, Leergaard TB (2013) Altered diffusion tensor imaging measurements in aged transgenic Huntington disease rats. Brain Struct Funct 218:767–778PubMedCentralPubMedCrossRef

Bear M, Conners B, Paradiso M (2007) Neuroscience. Exploring the brain, 3rd edn. Lippincott Williams & Wilkins, Baltimore

Boska MD, Hasan KM, Kibuule D, Banerjee R, McIntyre E, Nelson JA, Hahn T, Gendelman HE, Mosley RL (2007) Quantitative diffusion tensor imaging detects dopaminergic neuronal degeneration in a murine model of Parkinson’s disease. Neurobiol Dis 26(3):590–596PubMedCentralPubMedCrossRef

Brodal P (2004) The central nervous system, 4th edn. Oxford University Press, New York

Capecchi MR (1989) The new mouse genetics: altering the genome by gene targeting. Trends Genet 5(3):70–76PubMedCrossRef

Carroll JB, Lerch JP, Franciosi S, Spreeuw A, Bissada N, Henkelman RM, Hayden MR (2011) Natural history of disease in the YAC128 mouse reveals a discrete signature of pathology in Huntington disease. Neurobiol Dis 43(1):257–265PubMedCrossRef

Cepeda-Prado E, Popp S, Khan U, Stefanov D, Rodriguez J, Menalled LB, Dow-Edwards D, Small SA, Moreno H (2012) R6/2 Huntington’s disease mice develop early and progressive abnormal brain metabolism and seizures. J Neurosci 32(19):6456–6467PubMedCentralPubMedCrossRef

Chakravarty MM, Bedell BJ, Zehntner SP, Evans AC, Collins DL (2008) Three-dimensional reconstruction of serial histological mouse brain sections. In: 2008 IEEE international symposium on biomedical imaging: from nano to macro, vol 1–4, pp 987–990

Cheng Y, Peng Q, Hou Z, Aggarwal M, Zhang J, Mori S, Ross CA, Duan W (2011) Structural MRI detects progressive regional brain atrophy and neuroprotective effects in N171–82Q Huntington’s disease mouse model. Neuroimage 56(3):1027–1034PubMedCentralPubMedCrossRef

Choe AS, Gao YR, Li X, Compton KB, Stepniewska I, Anderson AW (2011) Accuracy of image registration between MRI and light microscopy in the ex vivo brain. Magn Reson Imaging 29(5):683–692PubMedCentralPubMedCrossRef

Chuang N, Mori S, Yamamoto A, Jiang H, Ye X, Xu X, Richards LJ, Nathans J, Miller MI, Toga AW, Sidman RL, Zhang J (2011) An MRI-based atlas and database of the developing mouse brain. NeuroImage 54(1):80–89PubMedCentralPubMedCrossRef

Collins DL, Holmes CJ, Peters TM, Evans AC (1995) Automatic 3-D model-based neuroanatomical segmentation. Hum Brain Mapp 3(3):190–208CrossRef

Cyr M, Caron MG, Johnson GA, Laakso A (2005) Magnetic resonance imaging at microscopic resolution reveals subtle morphological changes in a mouse model of dopaminergic hyperfunction. NeuroImage 26(1):83–90PubMedCrossRef

Deogaonkar M, Heers M, Mahajan S, Brummer M, Subramanian T (2005) Method of construction of a MRI-based tabular database of 3D stereotaxic co-ordinates for individual structures in the basal ganglia of Macaca mulatta. J Neurosci Meth 149(2):154–163CrossRef

Flinn L, Bretaud S, Lo C, Ingham PW, Bandmann O (2008) Zebrafish as a new animal model for movement disorders. J Neurochem 106(5):1991–1997PubMedCrossRef

Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL (2011) Unbiased average age-appropriate atlases for pediatric studies. NeuroImage 54(1):313–327PubMedCentralPubMedCrossRef

Francois C, Yelnik J, Percheron G (1996) A stereotaxic atlas of the basal ganglia in macaques. Brain Res Bull 41(3):151–158PubMedCrossRef

Gerfen CR (2004) Basal Ganglia. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic Press, San Diego, pp 455–508

Heimer L, Switzer RD, Van Hoesen GW (1982) Ventral striatum and ventral pallidum components of the motor system? Trends Neurosci 5(3):83–87CrossRef

Hertel N, Krishna K, Nuernberger M, Redies C (2008) A cadherin-based code for the divisions of the mouse basal ganglia. J Comp Neurol 508(4):511–528PubMedCrossRef

Janke AL, Ullmann JFP, Kurniawan ND, Paxinos G, Keller M, Yang Z, Richards K, Egan G, Petrou S, Galloway G, Reutens D (2012) 15 μm average mouse models in Waxholm space from 16.4T 30 μm images. In: 20th annual ISMRM scientific meeting and exhibition, Melbourne, Australia

Jiang Y, Johnson GA (2011) Microscopic diffusion tensor atlas of the mouse brain. NeuroImage 56(3):1235–1243PubMedCentralPubMedCrossRef

Johnson GA, Badea A, Brandenburg J, Cofer G, Fubara B, Liu S, Nissanov J (2010) Waxholm space: an image-based reference for coordinating mouse brain research. NeuroImage 53(2):365–372PubMedCentralPubMedCrossRef

Johnson GA, Calabrese E, Badea A, Paxinos G, Watson C (2012) A multidimensional magnetic resonance histology atlas of the Wistar rat brain. NeuroImage 62(3):1848–1856PubMedCentralPubMedCrossRef

Kerbler GM, Hamlin AS, Pannek K, Kurniawan ND, Keller MD, Rose SE, Coulson EJ (2012) Diffusion-weighted magnetic resonance imaging detection of basal forebrain cholinergic degeneration in a mouse model. NeuroImage 66C:133–141PubMed

Lanciego JL, Vazquez A (2012) The basal ganglia and thalamus of the long-tailed macaque in stereotaxic coordinates. A template atlas based on coronal, sagittal and horizontal brain sections. Brain Struct Funct 217(2):613–666PubMedCentralPubMedCrossRef

Lerch JP, Carroll JB, Dorr A, Spring S, Evans AC, Hayden MR, Sled JG, Henkelman RM (2008a) Cortical thickness measured from MRI in the YAC128 mouse model of Huntington’s disease. NeuroImage 41(2):243–251PubMedCrossRef

Lerch JP, Carroll JB, Spring S, Bertram LN, Schwab C, Hayden MR, Henkelman RM (2008b) Automated deformation analysis in the YAC128 Huntington disease mouse model. NeuroImage 39(1):32–39PubMedCrossRef

MacKenzie-Graham A, Boline J, Toga AW (2007) Brain atlases and neuroanatomic imaging. Methods Mol Biol 401:183–194PubMedCrossRef

Martinez-Garcia G, Novejarque A, Gutierrez-Castellanos N, Lanuza E (2012) Piriform cortex and amygdala. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system, vol 1. Elsevier Academic Press, San Diego, pp 140–172CrossRef

Medina L, Abellan A (2012) Subpallial structures. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system, vol 1. Elsevier Academic Press, San Diego, pp 173–220CrossRef

Meredith GE, Pattiselanno A, Groenewegen HJ, Haber SN (1996) Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin-D28 k. J Comp Neurol 365(4):628–639PubMedCrossRef

Oorschot DE (2010) Cell types in the different nuclei of the basal ganglia. In: Steiner H, Tseng KY (eds) Handbook of basal ganglia structure and function. Elsevier Inc., San Diego, pp 63–74CrossRef

Panula P, Chen YC, Priyadarshini M, Kudo H, Semenova S, Sundvik M, Sallinen V (2010) The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiol Dis 40(1):46–57PubMedCrossRef

Paxinos G, Franklin K (2013) The mouse brain in stereotaxic coordinates, vol 4. Academic Press, San Diego

Paxinos G, Watson C, Carrive P, Kirkcaldie MT, Ashwell K (2009) Chemoarchitectonic atlas of the rat brain. Elsevier Academic Press, San Diego

Pelled G, Bergman H, Ben-Hur T, Goelman G (2007) Manganese-enhanced MRI in a rat model of Parkinson’s disease. J Magn Reson Imaging 26(4):863–870PubMedCrossRef

Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martinez S (2007) The chick brain in stereotaxic coordinates. An atlas featuring neuromeres and mammalian homologies. Elsevier Academic Press, San Diego

Puelles E, Martinez-de-la-Torre M, Watson C, Puelles L (2012) Midbrain. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system, vol 1. Elsevier Academic Press, San Diego, pp 337–359CrossRef

Sadikot AF, Chakravarty MM, Bertrand G, Rymar VV, Al-Subaie F, Collins DL (2011) Creation of computerized 3D MRI-integrated atlases of the human basal ganglia and thalamus. Front Syst Neurosci 5:71PubMedCentralPubMedCrossRef

Saleem K, Logothetis N (2007) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego

Sawiak SJ, Wood NI, Williams GB, Morton AJ, Carpenter TA (2009a) Use of magnetic resonance imaging for anatomical phenotyping of the R6/2 mouse model of Huntington’s disease. Neurobiol Dis 33(1):12–19PubMedCrossRef

Sawiak SJ, Wood NI, Williams GB, Morton AJ, Carpenter TA (2009b) Voxel-based morphometry in the R6/2 transgenic mouse reveals differences between genotypes not seen with manual 2D morphometry. Neurobiol Dis 33(1):20–27PubMedCrossRef

Song SK, Kim JH, Lin SJ, Brendza RP, Holtzman DM (2004) Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition. Neurobiol Dis 15(3):640–647PubMedCrossRef

Soria G, Aguilar E, Tudela R, Mullol J, Planas AM, Marin C (2011) In vivo magnetic resonance imaging characterization of bilateral structural changes in experimental Parkinson’s disease: a T2 relaxometry study combined with longitudinal diffusion tensor imaging and manganese-enhanced magnetic resonance imaging in the 6-hydroxydopamine rat model. Eur J Neurosci 33(8):1551–1560PubMedCrossRef

Swanson LW (2000) Cerebral hemisphere regulation of motivated behavior. Brain Res 886(1–2):113–164PubMedCrossRef

Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21(8):323–331PubMedCrossRef

Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 35(4):1459–1472PubMedCrossRef

Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Tech 22(1):53–66CrossRef

Ullmann JF, Keller MD, Watson C, Janke AL, Kurniawan ND, Yang Z, Richards K, Paxinos G, Egan GF, Petrou S, Bartlett P, Galloway GJ, Reutens DC (2012) Segmentation of the C57BL/6 J mouse cerebellum in magnetic resonance images. NeuroImage 62(3):1408–1414PubMedCrossRef

Watson C, Paxinos G (2010) Chemoarchitectonic atlas of the mouse brain. Elsevier Academic Press, San Diego

Watson C, Kirkcaldie MT, Paxinos G (2010) The brain: an introduction to functional neuroanatomy. Academic Press, San Diego

Yang SH, Chan AW (2011) Transgenic animal models of Huntington’s disease. Curr Top Behav Neurosci 7:61–85PubMedCrossRef

Yang Z, Richards K, Kurniawan ND, Petrou S, Reutens DC (2012) MRI-guided volume reconstruction of mouse brain from histological sections. J Neurosci Meth 211(2):210–217CrossRef

Yelnik J, Bardinet E, Dormont D, Malandain G, Ourselin S, Tande D, Karachi C, Ayache N, Cornu P, Agid Y (2007) A three-dimensional, histological and deformable atlas of the human basal ganglia. I. Atlas construction based on immunohistochemical and MRI data. NeuroImage 34(2):618–638PubMedCrossRef

Zahm DS, Brog JS (1992) On the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience 50(4):751–767PubMedCrossRef

Zhang J, Richards LJ, Yarowsky P, Huang H, van Zijl PCM, Mori S (2003) Three-dimensional anatomical characterization of the developing mouse brain by diffusion tensor microimaging. NeuroImage 20(3):1639–1648PubMedCrossRef

Zhang JY, Peng Q, Li Q, Jahanshad N, Hou ZP, Jiang ML, Masuda N, Langbehn DR, Miller MI, Mori S, Ross CA, Duan WZ (2010) Longitudinal characterization of brain atrophy of a Huntington’s disease mouse model by automated morphological analyses of magnetic resonance images. Neuroimage 49(3):2340–2351PubMedCentralPubMedCrossRef

Title: An MRI atlas of the mouse basal ganglia
Authors: Jeremy F. P. Ullmann
Charles Watson
Andrew L. Janke
Nyoman D. Kurniawan
George Paxinos
David C. Reutens
Publication date: 01-07-2014
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2014
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-013-0572-0

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An MRI atlas of the mouse basal ganglia

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