Skip to main content

Advertisement

SpringerLink
Log in

A diffusion tensor imaging atlas of white matter in tree shrew

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Tree shrews are small mammals now commonly classified in the order of Scandentia, but have relatively closer affinity to primates than rodents. The species has a high brain-to-body mass ratio and relatively well-differentiated neocortex, and thus has been frequently used in neuroscience research, especially for studies on vision and neurological/psychiatric diseases. The available atlases on tree shrew brain provided only limited information on white matter (WM) anatomy. In this study, diffusion tensor imaging (DTI) was used to study the WM anatomy of tree shrew, with the goal to establish an image-based WM atlas. DTI and T2-weighted anatomical images were acquired in vivo and from fixed brain samples. Deterministic tractography was used for three-dimensional reconstruction and rendering of major WM tracts. Myelin and neurofilaments staining were used to study the microstructural properties of certain WM tracts. Taking into account prior knowledge on tree shrew neuroanatomy, tractography results, and comparisons to the homologous structures in rodents and primates, an image-based WM atlas of tree shrew brain was constructed, which is available to research community upon request.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aboitiz F, Garcia VR (1997) The evolutionary origin of the language areas in the human brain. A neuroanatomical perspective. Brain Res Rev 25:381–396

    Article  CAS  PubMed  Google Scholar 

  • Adluru N, Zhang H, Fox AS et al (2012) A diffusion tensor brain template for rhesus macaques. Neuroimage 59:306–318

    Article  PubMed  Google Scholar 

  • Aggarwal M, Nauen DW, Troncoso JC et al (2015) Probing region-specific microstructure of human cortical areas using high angular and spatial resolution diffusion MRI. Neuroimage 105:198–207

    Article  PubMed  Google Scholar 

  • Atlan G, Terem A, Peretz-Rivlin N et al (2016) Mapping synaptic cortico-claustral connectivity in the mouse. J Comp Neurol. doi:10.1002/cne.23997

    PubMed  Google Scholar 

  • Avants BB, Tustison NJ, Song G et al (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54:2033–2044

    Article  PubMed  Google Scholar 

  • Bedwell SA, Billett EE, Crofts JJ et al (2015) The topology of connections between rat prefrontal and temporal cortices. Front Syst Neurosci 9:80

    Article  PubMed  PubMed Central  Google Scholar 

  • Behrens TE, Berg HJ, Jbabdi S et al (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144–155

    Article  CAS  PubMed  Google Scholar 

  • Benveniste H, Einstein G, Kim KR et al (1999) Detection of neuritic plaques in Alzheimer’s disease by magnetic resonance microscopy. Proc Natl Acad Sci USA 96:14079–14084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berke JJ (1960) The claustrum, the external capsule and the extreme capsule of Macaca mulatta. J Comp Neurol 115:297–331

    Article  PubMed  Google Scholar 

  • Bora E, Yucel M, Fornito A et al (2012) White matter microstructure in opiate addiction. Addict Biol 17:141–148

    Article  CAS  PubMed  Google Scholar 

  • Bosking WH, Zhang Y, Schofield B et al (1997) Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J Neurosci 17:2112–2127

    CAS  PubMed  Google Scholar 

  • Calabrese E, Badea A, Coe CL et al (2015) A diffusion tensor MRI atlas of the postmortem rhesus macaque brain. Neuroimage 117:408–416

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell CB, Jane JA, Yashon D (1967) The retinal projections of the tree shrew and hedgehog. Brain Res 5:406–418

    Article  CAS  PubMed  Google Scholar 

  • Cao J, Yang EB, Su JJ et al (2003) The tree shrews: adjuncts and alternatives to primates as models for biomedical research. J Med Primatol 32:123–130

    Article  CAS  PubMed  Google Scholar 

  • Carey RG, Neal TL (1986) Reciprocal connections between the claustrum and visual thalamus in the tree shrew (tupaia-glis). Brain Res 386:155–168

    Article  CAS  PubMed  Google Scholar 

  • Carey RG, Fitzpatrick D, Diamond IT (1979) Layer I of striate cortex of tupaia glis and galago senegalensis: projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 186:393–437

    Article  CAS  PubMed  Google Scholar 

  • Carey RG, Bear MF, Diamond IT (1980) Laminar organization of the reciprocal projections between the claustrum and striate cortex in the tree shrew, tupaia-glis. Brain Res 184:193–198

    Article  CAS  PubMed  Google Scholar 

  • Casseday HJ, Diamond IT, Harting JK (1976) Auditory pathways to the cortex in tupaia glis. J Comp Neurol 166:303–340

    Article  CAS  PubMed  Google Scholar 

  • Catani M, Howard RJ, Pajevic S et al (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94

    Article  PubMed  Google Scholar 

  • Chan E, Kovacevic N, Ho SK et al (2007) Development of a high resolution three-dimensional surgical atlas of the murine head for strains 129S1/SvImJ and C57Bl/6J using magnetic resonance imaging and micro-computed tomography. Neuroscience 144:604–615

    Article  CAS  PubMed  Google Scholar 

  • Chomsung RD, Petry HM, Bickford ME (2008) Ultrastructural examination of diffuse and specific tectopulvinar projections in the tree shrew. J Comp Neurol 510:24–46

    Article  PubMed  PubMed Central  Google Scholar 

  • Chomsung RD, Wei H, Day-Brown JD et al (2010) Synaptic organization of connections between the temporal cortex and pulvinar nucleus of the tree shrew. Cereb Cortex 20:997–1011

    Article  PubMed  Google Scholar 

  • Chuang N, Mori S, Yamamoto A et al (2011) An MRI-based atlas and database of the developing mouse brain. Neuroimage 54:80–89

    Article  PubMed  Google Scholar 

  • Conturo TE, Lori NF, Cull TS et al (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96:10422–10427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalby RB, Frandsen J, Chakravarty MM et al (2010) Depression severity is correlated to the integrity of white matter fiber tracts in late-onset major depression. Psychiatry Res 184:38–48

    Article  PubMed  Google Scholar 

  • Day-Brown JD, Wei H, Chomsung RD et al (2010) Pulvinar projections to the striatum and amygdala in the tree shrew. Front Neuroanat 4:143

    Article  PubMed  PubMed Central  Google Scholar 

  • Delatour B, Witter MP (2002) Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways. Eur J Neurosci 15:1400–1407

    Article  CAS  PubMed  Google Scholar 

  • Fan Y, Huang ZY, Cao CC et al (2013) Genome of the Chinese tree shrew. Nat Commun 4:1426

    Article  PubMed  CAS  Google Scholar 

  • Figini M, Zucca I, Aquino D et al (2015) In vivo DTI tractography of the rat brain: an atlas of the main tracts in Paxinos space with histological comparison. Magn Reson Imaging 33:296–303

    Article  PubMed  Google Scholar 

  • Fitzpatrick D (1996) The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. Cereb Cortex 6:329–341

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick D, Carey RG, Diamond IT (1980) The projection of the superior colliculus upon the lateral geniculate-body in tupaia-glis and galago-senegalensis. Brain Res 194:494–499

    Article  CAS  PubMed  Google Scholar 

  • Flugge G, Ahrens O, Fuchs E (1994) Monoamine receptors in the amygdaloid complex of the tree shrew (tupaia belangeri). J Comp Neurol 343:597–608

    Article  CAS  PubMed  Google Scholar 

  • Fox AS, Oler JA, do Tromp PM et al (2015) Extending the amygdala in theories of threat processing. Trends Neurosci 38:319–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foxley S, Jbabdi S, Clare S et al (2014) Improving diffusion-weighted imaging of post-mortem human brains: SSFP at 7 T. Neuroimage 102(Pt 2):579–589

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuchs E (2005) Social stress in tree shrews as an animal model of depression: an example of a behavioral model of a CNS disorder. CNS Spectr 10:182–190

    Article  PubMed  Google Scholar 

  • Fuchs E, Flugge G (2002) Social stress in tree shrews: effects on physiology, brain function, and behavior of subordinate individuals. Pharmacol Biochem Behav 73:247–258

    Article  CAS  PubMed  Google Scholar 

  • Glickstein M (1967) Laminar structure of the dorsal lateral geniculate nucleus in the tree shrew (tupaia glis). J Comp Neurol 131:93–102

    Article  CAS  PubMed  Google Scholar 

  • Hall WC, Lee P (1993) Interlaminar connections of the superior colliculus in the tree shrew. I. The superficial gray layer. J Comp Neurol 332:213–223

    Article  CAS  PubMed  Google Scholar 

  • Hall WC, Lee P (1997) Interlaminar connections of the superior colliculus in the tree shrew. III: The optic layer. Vis Neurosci 14:647–661

    Article  CAS  PubMed  Google Scholar 

  • Harting JK, Hall WC, Diamond IT et al (1973) Anterograde degeneration study of the superior colliculus in tupaia glis: evidence for a subdivision between superficial and deep layers. J Comp Neurol 148:361–386

    Article  CAS  PubMed  Google Scholar 

  • Harting JK, Huerta MF, Hashikawa T et al (1991) Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J Comp Neurol 304:275–306

    Article  CAS  PubMed  Google Scholar 

  • Hoover WB, Vertes RP (2011) Projections of the medial orbital and ventral orbital cortex in the rat. J Comp Neurol 519:3766–3801

    Article  PubMed  Google Scholar 

  • Jain N, Preuss TM, Kaas JH (1994) Subdivisions of the visual system labeled with the Cat-301 antibody in tree shrews. Vis Neurosci 11:731–741

    Article  CAS  PubMed  Google Scholar 

  • Jbabdi S, Johansen-Berg H (2011) Tractography: where do we go from here? Brain Connect 1:169–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaas JH (2011) The evolution of auditory cortex: the core areas. In: Jeffery A, Winer CES (eds) The auditory cortex. Springer, US, pp 407–427

    Chapter  Google Scholar 

  • Keuker JI, de Biurrun G, Luiten PG et al (2004) Preservation of hippocampal neuron numbers and hippocampal subfield volumes in behaviorally characterized aged tree shrews. J Comp Neurol 468:509–517

    Article  PubMed  Google Scholar 

  • Kowianski P, Dziewiatkowski J, Kowianska J et al (1999) Comparative anatomy of the claustrum in selected species: a morphometric analysis. Brain Behav Evol 53:44–54

    Article  CAS  PubMed  Google Scholar 

  • Lee P, Hall WC (1995) Interlaminar connections of the superior colliculus in the tree shrew. II: projections from the superficial gray to the optic layer. Vis Neurosci 12:573–588

    Article  CAS  PubMed  Google Scholar 

  • Lende RA (1970) Cortical localization in the tree shrew (tupaia). Brain Res 18:61–75

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Ni X (2016) An early Oligocene fossil demonstrates treeshrews are slowly evolving “living fossils”. Sci Rep 6:18627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu FG, Miyamoto MM, Freire NP et al (2001) Molecular and morphological supertrees for eutherian (placental) mammals. Science 291:1786–1789

    Article  CAS  PubMed  Google Scholar 

  • Luppino G, Matelli M, Carey RG et al (1988) New view of the organization of the pulvinar nucleus in tupaia as revealed by tectopulvinar and pulvinar-cortical projections. J Comp Neurol 273:67–86

    Article  CAS  PubMed  Google Scholar 

  • Lyon DC, Jain N, Kaas JH (2003a) The visual pulvinar in tree shrews I. Multiple subdivisions revealed through acetylcholinesterase and Cat-301 chemoarchitecture. J Comp Neurol 467:593–606

    Article  CAS  PubMed  Google Scholar 

  • Lyon DC, Jain N, Kaas JH (2003b) The visual pulvinar in tree shrews II. Projections of four nuclei to areas of visual cortex. J Comp Neurol 467:607–627

    Article  PubMed  Google Scholar 

  • Ma KL, Gao JH, Huang ZQ et al (2013) Motor function in MPTP-treated tree shrews (tupaia belangeri chinensis). Neurochem Res 38:1935–1940

    Article  CAS  Google Scholar 

  • Makris N, Pandya DN (2009) The extreme capsule in humans and rethinking of the language circuitry. Brain Struct Funct 213:343–358

    Article  PubMed  Google Scholar 

  • Marrocco RT, De Valois RL, Boles JI (1970) A stereotaxic atlas of the brain of the tree shrew (tupaia glis). J Hirnforsch 12:307–312

    PubMed  Google Scholar 

  • Mars RB, Foxley S, Verhagen L et al (2015) The extreme capsule fiber complex in humans and macaque monkeys: a comparative diffusion MRI tractography study. Brain Struct Funct. doi:10.1007/s00429-015-1146-0

    PubMed  PubMed Central  Google Scholar 

  • Mathur BN (2014) The claustrum in review. Front Syst Neurosci 8:48

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsuo K, Mizuno T, Yamada K et al (2008) Cerebral white matter damage in frontotemporal dementia assessed by diffusion tensor tractography. Neuroradiology 50:605–611

    Article  PubMed  Google Scholar 

  • May PJ (2006) The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 151:321–378

    Article  PubMed  Google Scholar 

  • McCollum LA, Roberts RC (2014) Ultrastructural localization of tyrosine hydroxylase in tree shrew nucleus accumbens core and shell. Neuroscience 271:23–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480

    Article  PubMed  Google Scholar 

  • Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539

    Article  CAS  PubMed  Google Scholar 

  • Mori S, Oishi K, Jiang H et al (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40:570–582

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy WJ, Eizirik E, O’Brien SJ et al (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351

    Article  CAS  PubMed  Google Scholar 

  • Ohl F, Kirschbaum C, Fuchs E (1999) Evaluation of hypothalamo-pituitary-adrenal activity in the tree shrew (tupaia belangeri) via salivary cortisol measurement. Lab Anim 33:269–274

    Article  CAS  PubMed  Google Scholar 

  • Ohl F, Michaelis T, Vollmann-Honsdorf GK et al (2000) Effect of chronic psychosocial stress and long-term cortisol treatment on hippocampus-mediated memory and hippocampal volume: a pilot-study in tree shrews. Psychoneuroendocrinology 25:357–363

    Article  CAS  PubMed  Google Scholar 

  • Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219

    Article  CAS  PubMed  Google Scholar 

  • Pajevic S, Pierpaoli C (1999) Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med 42:526–540

    Article  CAS  PubMed  Google Scholar 

  • Palchaudhuri M, Flugge G (2005) 5-HT1A receptor expression in pyramidal neurons of cortical and limbic brain regions. Cell Tissue Res 321:159–172

    Article  CAS  PubMed  Google Scholar 

  • Park S, Tyszka JM, Allman JM (2012) The claustrum and insula in microcebus murinus: a high resolution diffusion imaging study. Front Neuroanat 6:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Pawlik M, Fuchs E, Walker LC et al (1999) Primate-like amyloid-β sequence but no cerebral amyloidosis in aged tree shrews. Neurobiol Aging 20:47–51

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (2006) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, San Diego

    Google Scholar 

  • Peng Y, Ye Z, Zou R et al (1991) Biology of Chinese tree shrews. Yunnan Science and Technology Press, Kunming

    Google Scholar 

  • Petros TJ, Rebsam A, Mason CA (2008) Retinal axon growth at the optic chiasm: to cross or not to cross. Annu Rev Neurosci 31:295–315

    Article  CAS  PubMed  Google Scholar 

  • Poletti CE, Creswell G (1977) Fornix system efferent projections in the squirrel monkey: an experimental degeneration study. J Comp Neurol 175:101–128

    Article  CAS  PubMed  Google Scholar 

  • Pritzel M, Kretz R, Rager G (1988) Callosal projections between areas-17 in the adult tree shrew (tupaia-belangeri). Exp Brain Res 72:481–493

    Article  CAS  PubMed  Google Scholar 

  • Remple MS, Reed JL, Stepniewska I et al (2006) Organization of frontoparietal cortex in the tree shrew (tupaia belangeri). I. Architecture, microelectrode maps, and corticospinal connections. J Comp Neurol 497:133–154

    Article  PubMed  Google Scholar 

  • Remple MS, Reed JL, Stepniewska I et al (2007) The organization of frontoparietal cortex in the tree shrew (tupaia belangeri): II. Connectional evidence for a frontal-posterior parietal network. J Comp Neurol 501:121–149

    Article  PubMed  Google Scholar 

  • Rice MW, Roberts RC, Melendez-Ferro M et al (2011) Neurochemical characterization of the tree shrew dorsal striatum. Front Neuroanat 5:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Rilling JK, Glasser MF, Preuss TM et al (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:426–428

    Article  CAS  PubMed  Google Scholar 

  • Rilling JK, Glasser MF, Jbabdi S et al (2011) Continuity, divergence, and the evolution of brain language pathways. Front Evol Neurosci 3:11

    PubMed  Google Scholar 

  • Sati P, Silva AC, van Gelderen P et al (2012) In vivo quantification of T(2) anisotropy in white matter fibers in marmoset monkeys. Neuroimage 59:979–985

    Article  PubMed  Google Scholar 

  • Saur D, Kreher BW, Schnell S et al (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 105:18035–18040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmahmann JD, Pandya DN (2006) Fiber pathways of the brain. Oxford University Press, New York

    Book  Google Scholar 

  • Schmahmann JD, Pandya DN, Wang R et al (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130:630–653

    Article  PubMed  Google Scholar 

  • Shen F, Duan Y, Jin S et al (2014) Varied behavioral responses induced by morphine in the tree shrew: a possible model for human opiate addiction. Front Behav Neurosci 8:333

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shenton ME, Hamoda HM, Schneiderman JS et al (2012) A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav 6:137–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibata S, Komaki Y, Seki F et al (2015) Connectomics: comprehensive approaches for whole-brain mapping. Microscopy 64:57–67

    Article  PubMed  Google Scholar 

  • Sillitoe RV, Malz CR, Rockland K et al (2004) Antigenic compartmentation of the primate and tree shrew cerebellum: a common topography of zebrin II in macaca mulatta and tupaia belangeri. J Anat 204:257–269

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Dell’Acqua F, Valabregue R et al (2012) Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48:82–96

    Article  PubMed  Google Scholar 

  • Thomas C, Ye FQ, Irfanoglu MO et al (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci USA 111:16574–16579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tigges J, Shantha TR (1969) A stereotaxic brain atlas of the tree shrew (tupaia glis). Williams & Wilkins, Baltimore

    Google Scholar 

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

    Article  Google Scholar 

  • Wakana S, Jiang H, Nagae-Poetscher LM et al (2004) Fiber tract-based atlas of human white matter anatomy. Radiology 230:77–87

    Article  PubMed  Google Scholar 

  • Wang S, Shan D, Dai J et al (2013) Anatomical MRI templates of tree shrew brain for volumetric analysis and voxel-based morphometry. J Neurosci Methods 220:9–17

    Article  PubMed  Google Scholar 

  • Wong P, Kaas JH (2009) Architectonic subdivisions of neocortex in the tree shrew (tupaia belangeri). Anat Rec (Hoboken) 292:994–1027

    Article  PubMed Central  Google Scholar 

  • Yamashita A, Fuchs E, Taira M et al (2010) Amyloid beta (Abeta) protein- and amyloid precursor protein (APP)-immunoreactive structures in the brains of aged tree shrews. Curr Aging Sci 3:230–238

    Article  CAS  PubMed  Google Scholar 

  • Yamashita A, Fuchs E, Taira M et al (2012) Somatostatin-immunoreactive senile plaque-like structures in the frontal cortex and nucleus accumbens of aged tree shrews and Japanese macaques. J Med Primatol 41:147–157

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Liu J (1990) A stereotaxic atlas of the brain of tupaia belangeri and macaque monkey living in Guangxi. Guangxi Science and Technology Publishing House, Guangxi

    Google Scholar 

  • Zambello E, Fuchs E, Abumaria N et al (2010) Chronic psychosocial stress alters NPY system: different effects in rat and tree shrew. Prog Neuropsychopharmacol Biol Psychiatry 34:122–130

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Yushkevich PA, Rueckert D et al (2007) Unbiased white matter atlas construction using diffusion tensor images. Med Image Comput Comput Assist Interv 4792:211–218

    Google Scholar 

  • Zilles K (1978) A quantitative approach to cytoarchitectonics. I. The areal pattern of the cortex of tupaia belangeri. Anat Embryol (Berl) 153:195–212

    Article  CAS  Google Scholar 

  • Zuo N, Fang J, Lv X et al (2012) White matter abnormalities in major depression: a tract-based spatial statistics and rumination study. PLoS One 7:e37561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Yun-ling Gao for her assistance in histological staining. This work was supported by Grants from Chinese Ministry of Science and Technology (2011CB707800) and Natural Science Foundation of China (81171302 and 21221064).

Author information

Authors and Affiliations

  1. National Center for Magnetic Resonance in Wuhan, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences, Wuhan, 430071, China

    Jian-kun Dai, Shu-xia Wang, Dai Shan & Hao Lei

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Jian-kun Dai

  3. Xuzhou Medical University, Xuzhou, 221004, China

    Hai-chen Niu

Authors
  1. Jian-kun Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu-xia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dai Shan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hai-chen Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hao Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hao Lei.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dai, Jk., Wang, Sx., Shan, D. et al. A diffusion tensor imaging atlas of white matter in tree shrew. Brain Struct Funct 222, 1733–1751 (2017). https://doi.org/10.1007/s00429-016-1304-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1304-z

Keywords

Search

Navigation