دورية أكاديمية
Mapping the living mouse brain neural architecture: strain-specific patterns of brain structural and functional connectivity.
العنوان: | Mapping the living mouse brain neural architecture: strain-specific patterns of brain structural and functional connectivity. |
---|---|
المؤلفون: | Karatas M; Department of Radiology, Medical Physics, Medical Center, Faculty of Medicine, University of Freiburg, Breisacher Straße 60a, 79106, Freiburg, Germany.; Laboratory of Engineering, Informatics and Imaging (ICube), Integrative Multimodal Imaging in Healthcare (IMIS), UMR 7357, University of Strasbourg, 4 Rue Kirschleger, 67000, Strasbourg, France.; Institut de Neurosciences Cellulaires et Intégratives (INCI), CNRS UPR 3212, University of Strasbourg, 8 Allée du Général Rouvillois, 67000, Strasbourg, France., Noblet V; Laboratory of Engineering, Informatics and Imaging (ICube), Images-Modelling-Learning-Geometry and Statistics (IMAGeS), UMR 7357, University of Strasbourg, 300 Bd Sébastien Brant, BP 10413, 67412, Illkirch Cedex, France., Nasseef MT; Department of Psychiatry, School of Medicine, Douglas Hospital Research Center, McGill University, Montreal, QC, Canada., Bienert T; Department of Radiology, Medical Physics, Medical Center, Faculty of Medicine, University of Freiburg, Breisacher Straße 60a, 79106, Freiburg, Germany., Reisert M; Department of Radiology, Medical Physics, Medical Center, Faculty of Medicine, University of Freiburg, Breisacher Straße 60a, 79106, Freiburg, Germany., Hennig J; Department of Radiology, Medical Physics, Medical Center, Faculty of Medicine, University of Freiburg, Breisacher Straße 60a, 79106, Freiburg, Germany., Yalcin I; Institut de Neurosciences Cellulaires et Intégratives (INCI), CNRS UPR 3212, University of Strasbourg, 8 Allée du Général Rouvillois, 67000, Strasbourg, France., Kieffer BL; Department of Psychiatry, School of Medicine, Douglas Hospital Research Center, McGill University, Montreal, QC, Canada., von Elverfeldt D; Department of Radiology, Medical Physics, Medical Center, Faculty of Medicine, University of Freiburg, Breisacher Straße 60a, 79106, Freiburg, Germany., Harsan LA; Department of Radiology, Medical Physics, Medical Center, Faculty of Medicine, University of Freiburg, Breisacher Straße 60a, 79106, Freiburg, Germany. harsan@unistra.fr.; Laboratory of Engineering, Informatics and Imaging (ICube), Integrative Multimodal Imaging in Healthcare (IMIS), UMR 7357, University of Strasbourg, 4 Rue Kirschleger, 67000, Strasbourg, France. harsan@unistra.fr.; Department of Biophysics and Nuclear Medicine, University Hospitals of Strasbourg, 1 Avenue Molière, 67098, Strasbourg Cedex, France. harsan@unistra.fr. |
المصدر: | Brain structure & function [Brain Struct Funct] 2021 Apr; Vol. 226 (3), pp. 647-669. Date of Electronic Publication: 2021 Feb 26. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 101282001 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1863-2661 (Electronic) Linking ISSN: 18632653 NLM ISO Abbreviation: Brain Struct Funct Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Berlin : Springer-Verlag, c2007- |
مواضيع طبية MeSH: | Brain Mapping*/methods, Brain/*pathology , Brain/*physiology , Nerve Net/*pathology, Animals ; Connectome/methods ; Diffusion Magnetic Resonance Imaging/methods ; Magnetic Resonance Imaging/methods ; Mice ; Nerve Net/physiopathology ; Neural Pathways/pathology ; Neural Pathways/physiology ; Reward |
مستخلص: | Mapping brain structural and functional connectivity (FC) became an essential approach in neuroscience as network properties can underlie behavioral phenotypes. In mouse models, revealing strain-related patterns of brain wiring is crucial, since these animals are used to answer questions related to neurological or neuropsychiatric disorders. C57BL/6 and BALB/cJ strains are two of the primary "genetic backgrounds" for modeling brain disease and testing therapeutic approaches. However, extensive literature describes basal differences in the behavioral, neuroanatomical and neurochemical profiles of the two strains, which raises questions on whether the observed effects are pathology specific or depend on the genetic background of each strain. Here, we performed a systematic comparative exploration of brain structure and function of C57BL/6 and BALB/cJ mice using Magnetic Resonance Imaging (MRI). We combined deformation-based morphometry (DBM), diffusion MRI and high-resolution fiber mapping (hrFM) along with resting-state functional MRI (rs-fMRI) and demonstrated brain-wide differences in the morphology and "connectome" features of the two strains. Essential inter-strain differences were depicted regarding the size and the fiber density (FD) within frontal cortices, along cortico-striatal, thalamic and midbrain pathways as well as genu and splenium of corpus callosum. Structural dissimilarities were accompanied by specific FC patterns, emphasizing strain differences in frontal and basal forebrain functional networks as well as hubness characteristics. Rs-fMRI data further indicated differences of reward-aversion circuitry and default mode network (DMN) patterns. The inter-hemispherical FC showed flexibility and strain-specific adjustment of their patterns in agreement with the structural characteristics. |
References: | Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR et al (2007) Diffusion tensor imaging of the corpus callosum in autism. Neuroimage 34(1):61–73. (PMID: 17023185) Anderzhanova EA, Bächli H, Buneeva OA, Narkevich VB, Medvedev AE, Thoeringer CK et al (2013) Strain differences in profiles of dopaminergic neurotransmission in the prefrontal cortex of the BALB/C vs. C57Bl/6 mice: consequences of stress and afobazole. Eur J Pharmacol. 708(3):95–104. (PMID: 23524098) Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 54(3):2033–2044. (PMID: 20851191) Aydogan DB, Jacobs R, Dulawa S, Thompson SL, Francois MC, Toga AW et al (2018) When tractography meets tracer injections: a systematic study of trends and variation sources of diffusion-based connectivity. Brain Struct Funct 223(6):2841–2858. (PMID: 296631355997540) Bardella G, Bifone A, Gabrielli A, Gozzi A, Squartini T (2016) Hierarchical organization of functional connectivity in the mouse brain: a complex network approach. Sci Rep 6(1):32060. (PMID: 275347084989195) Barnett L, Seth AK (2014) The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference. J Neurosci Methods 15(223):50–68. Belzung C, Barreau S (2000) Differences in drug-induced place conditioning between BALB/c and C57Bl/6 mice. Pharmacol Biochem Behav 65(3):419–423. (PMID: 10683481) Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125(1–2):141–149. (PMID: 11682105) Bihan DL, Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E et al (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161(2):401–407. Biswal B, Zerrin Yetkin F, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar mri. Magn Reson Med 34(4):537–541. (PMID: 8524021) Brodkin ES (2007) BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav Brain Res 176(1):53–65. (PMID: 16890300) Brodkin ES, Hagemann A, Nemetski SM, Silver LM (2004) Social approach-avoidance behavior of inbred mouse strains towards DBA/2 mice. Brain Res 1002(1–2):151–157. (PMID: 14988045) Calabrese E, Badea A, Cofer G, Qi Y, Johnson GA (2015) A diffusion MRI tractography connectome of the mouse brain and comparison with neuronal tracer data. Cereb Cortex 25(11):4628–4637. (PMID: 260489514715247) Calamante F, Tournier J-D, Heidemann RM, Anwander A, Jackson GD, Connelly A (2011) Track density imaging (TDI): validation of super resolution property. NeuroImage 56(3):1259–1266. (PMID: 21354314) Calamante F, Tournier J-D, Kurniawan ND, Yang Z, Gyengesi E, Galloway GJ et al (2012) Super-resolution track-density imaging studies of mouse brain: comparison to histology. NeuroImage 59(1):286–296. (PMID: 21777683) Calcagno E, Canetta A, Guzzetti S, Cervo L, Invernizzi RW (2007) Strain differences in basal and post-citalopram extracellular 5-HT in the mouse medial prefrontal cortex and dorsal hippocampus: relation with tryptophan hydroxylase-2 activity. J Neurochem 103(3):1111–1120. (PMID: 17666043) Chen C, Kim JJ, Thompson RF, Tonegawa S (1996) Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110(5):1177–1180. (PMID: 8919020) Chuang K-H, Nasrallah FA (2017) Functional networks and network perturbations in rodents. NeuroImage 163:419–436. (PMID: 28942060) Clipperton-Allen AE, Ingrao JC, Ruggiero L, Batista L, Ovari J, Hammermueller J et al (2015) Long-term provision of environmental resources alters behavior but not physiology or neuroanatomy of male and female BALB/c and C57BL/6 mice. J Am Assoc Lab Anim Sci 54(6):718–730. (PMID: 266327814671787) Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N et al (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132(2):107–124. (PMID: 9266608) de Sá-Calçada D, Roque S, Branco C, Monteiro S, Cerqueira-Rodrigues B, Sousa N, et al. Exploring Female Mice Interstrain Differences Relevant for Models of Depression. Front Behav Neurosci [Internet]. 2015. [cited 2020 May 19];9. Available from: http://journal.frontiersin.org/Article/ https://doi.org/10.3389/fnbeh.2015.00335/abstract. Dennis EL, Thompson PM (2013) Typical and atypical brain development: a review of neuroimaging studies. Clin Res 15(3):26. Draganski B, Ashburner J, Hutton C, Kherif F, Frackowiak RSJ, Helms G et al (2011) Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ). Neuroimage 55(4):1423–1434. (PMID: 212773753093621) Ellegood J, Pacey LK, Hampson DR, Lerch JP, Mark HR (2010) Anatomical phenotyping in a mouse model of fragile X syndrome with magnetic resonance imaging. NeuroImage 53(3):1023–1029. (PMID: 20304074) Ellegood J, Anagnostou E, Babineau BA, Crawley JN, Lin L, Genestine M et al (2015) Clustering autism: using neuroanatomical differences in 26 mouse models to gain insight into the heterogeneity. Mol Psychiatry 20(1):118–125. (PMID: 25199916) Fairless AH, Dow HC, Toledo MM, Malkus KA, Edelmann M, Li H et al (2008) Low sociability is associated with reduced size of the corpus callosum in the BALB/cJ inbred mouse strain. Brain Res 16(1230):211–217. Fairless AH, Dow HC, Kreibich AS, Torre M, Kuruvilla M, Gordon E et al (2012) Sociability and brain development in BALB/cJ and C57BL/6J mice. Behav Brain Res 228(2):299–310. (PMID: 22178318) Fairless AH, Katz JM, Vijayvargiya N, Dow HC, Kreibich AS, Berrettini WH et al (2013) Development of home cage social behaviors in BALB/cJ vs. C57BL/6J mice. Behav Brain Res 237:338–347. (PMID: 22982070) Fontaine DA, Davis DB (2016) Attention to background strain is essential for metabolic research: C57BL/6 and the international knockout mouse consortium. Diabetes 65(1):25–33. (PMID: 26696638) Gao Y-R, Ma Y, Zhang Q, Winder AT, Liang Z, Antinori L et al (2017) Time to wake up: studying neurovascular coupling and brain-wide circuit function in the un-anesthetized animal. Neuroimage 153:382–398. (PMID: 27908788) Goense J, Bohraus Y, Logothetis NK. fMRI at High Spatial Resolution: Implications for BOLD-Models. Front Comput Neurosci [Internet]. 2016 [cited 2020];10. Available from: https://www.frontiersin.org/articles/ https://doi.org/10.3389/fncom.2016.00066/full. Good CD, Ashburner J, Frackowiak RS (2001) Computational neuroanatomy: new perspectives for neuroradiology. Rev Neurol 157(8–9 Pt 1):797–806. (PMID: 11677400) Grandjean J, Zerbi V, Balsters JH, Wenderoth N, Rudin M (2017) Structural basis of large-scale functional connectivity in the mouse. J Neurosci 37(34):8092–8101. (PMID: 287169616596781) Grange P (2020) Topology of the mesoscale connectome of the mouse brain. Comput Math Biophys 8(1):126–140. Griesemer JR, Gerson EM (2006) Of mice and men and low unit cost. Stud Hist Philos Sci Part C Stud Hist Philos Biol Biomed Sci 37(2):363–372. Grubb SC, Churchill GA, Bogue MA (2004) A collaborative database of inbred mouse strain characteristics. Bioinformatics 20(16):2857–2859. (PMID: 15130929) Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE, Adhikari A et al (2014) Natural neural projection dynamics underlying social behavior. Cell 157(7):1535–1551. (PMID: 249499674123133) Guzzetti S, Calcagno E, Canetta A, Sacchetti G, Fracasso C, Caccia S et al (2008) Strain differences in paroxetine-induced reduction of immobility time in the forced swimming test in mice: role of serotonin. Eur J Pharmacol 594(1–3):117–124. (PMID: 18691569) Hägele C, Schlagenhauf F, Rapp M, Sterzer P, Beck A, Bermpohl F et al (2015) Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacology 232(2):331–341. (PMID: 24973896) Harsan L-A, David C, Reisert M, Schnell S, Hennig J, von Elverfeldt D et al (2013) Mapping remodeling of thalamocortical projections in the living reeler mouse brain by diffusion tractography. Proc Natl Acad Sci 110(19):E1797–E1806. (PMID: 23610438) Horsfield MA, Jones DK (2002) Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases—a review. NMR Biomed 15(7–8):570–577. (PMID: 12489103) Hübner NS, Mechling AE, Lee H-L, Reisert M, Bienert T, Hennig J et al (2017) The connectomics of brain demyelination: functional and structural patterns in the cuprizone mouse model. Neuroimage 1(146):1–18. Ingalhalikar M, Parker D, Ghanbari Y, Smith A, Hua K, Mori S et al (2015) Connectome and maturation profiles of the developing mouse brain using diffusion tensor imaging. Cereb Cortex 25(9):2696–2706. (PMID: 24711485) Jacome LF, Burket JA, Herndon AL, Deutsch SI (2011) Genetically inbred Balb/c mice differ from outbred Swiss Webster mice on discrete measures of sociability: relevance to a genetic mouse model of autism spectrum disorders. Autism Res Off J Int Soc Autism Res 4(6):393–400. Johnson GA, Wang N, Anderson RJ, Chen M, Cofer GP, Gee JC et al (2019) Whole mouse brain connectomics. J Comp Neurol 527(13):2146–2157. Jones DK (2004) The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med 51(4):807–815. (PMID: 15065255) Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 1(73):239–254. Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ (2007) Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex 17(4):951–961. (PMID: 16772313) Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B et al (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477(7364):289–294. (PMID: 219219103276836) Kim S, Pickup S, Fairless AH, Ittyerah R, Dow HC, Abel T et al (2012) Association between sociability and diffusion tensor imaging in BALB/cJ mice: diffusion tensor imaging and sociability. NMR Biomed 25(1):104–112. (PMID: 21618305) Knox JE, Harris KD, Graddis N, Whitesell JD, Zeng H, Harris JA et al (2019) High-resolution data-driven model of the mouse connectome. Netw Neurosci 3(1):217–236. (PMID: 30793081) Kumar M, Kim S, Pickup S, Chen R, Fairless AH, Ittyerah R et al (2012) Longitudinal in-vivo diffusion tensor imaging for assessing brain developmental changes in BALB/cJ mice, a model of reduced sociability relevant to autism. Brain Res 1455:56–67. (PMID: 225131033340503) Lai JKY, Lerch JP, Doering LC, Foster JA, Ellegood J (2016) Regional brain volumes changes in adult male FMR1-KO mouse on the FVB strain. Neuroscience 318:12–21. (PMID: 26794591) Lassi G, Tucci V (2017) Gene-environment interaction influences attachment-like style in mice. Genes Brain Behav 16(6):612–618. (PMID: 28421709) Le Bihan D (2014) Diffusion MRI: what water tells us about the brain. EMBO Mol Med 6(5):569–573. (PMID: 247058764023879) Lee H-L, Zahneisen B, Hugger T, LeVan P, Hennig J (2013) Tracking dynamic resting-state networks at higher frequencies using MR-encephalography. NeuroImage 65:216–222. (PMID: 23069810) 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. (PMID: 17151600) Liska A, Gozzi A. Can mouse imaging studies bring order to autism connectivity chaos? Front Neurosci [Internet]. 2016Nov 10 [cited 2020 May 19];10. Available from: http://journal.frontiersin.org/article/ https://doi.org/10.3389/fnins.2016.00484/full. Liska A, Galbusera A, Schwarz AJ, Gozzi A (2015) Functional connectivity hubs of the mouse brain. NeuroImage 115:281–291. (PMID: 25913701) Maier-Hein KH, Neher PF, Houde J-C, Côté M-A, Garyfallidis E, Zhong J et al (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8(1):1349. (PMID: 291160935677006) Mechling AE, Arefin T, Lee H-L, Bienert T, Reisert M, Ben Hamida S et al (2016) Deletion of the mu opioid receptor gene in mice reshapes the reward–aversion connectome. Proc Natl Acad Sci 113(41):11603–11608. (PMID: 27671662) Moy SS, Nadler JJ, Young NB, Perez A, Holloway LP, Barbaro RP et al (2007) Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 176(1):4–20. (PMID: 16971002) Naeyaert M, Aelterman J, Audekerke JV, Golkov V, Cremers D, Pižurica A, et al. Accelerating in vivo fast spin echo high angular resolution diffusion imaging with an isotropic resolution in mice through compressed sensing. Magn Reson Med [Internet]. 2020 [cited 2020 Nov 14];n/a(n/a). Available from: https://onlinelibrary.wiley.com/doi/abs/ https://doi.org/10.1002/mrm.28520. Neher PF, Stieltjes B, Wolf I, Meinzer H-P, Fritzsche KH (2013) Analysis of tractography biases introduced by anisotropic voxels. Proc Intl Soc Mag Reson Med [Internet]. [cited 2020 Sep 21];21. Available from: https://www.researchgate.net/publication/236022704_Analysis_of_tractography_biases_introduced_by_anisotropic_voxels. Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S et al (2014) A mesoscale connectome of the mouse brain. Nature 508(7495):207–214. (PMID: 246952285102064) Ohl F, Sillaber I, Binder E, Keck ME, Holsboer F (2001) Differential analysis of behavior and diazepam-induced alterations in C57BL/6N and BALB/c mice using the modified hole board test. J Psychiatr Res 35(3):147–154. (PMID: 11461710) Palumbo ML, Canzobre MC, Pascuan CG, Ríos H, Wald M, Genaro AM (2010) Stress induced cognitive deficit is differentially modulated in BALB/c and C57Bl/6 mice: correlation with Th1/Th2 balance after stress exposure. J Neuroimmunol 218(1–2):12–20. (PMID: 19942299) Panksepp JB, Lahvis GP (2007) Social reward among juvenile mice. Genes Brain Behav 6(7):661–671. (PMID: 172126482040181) Pervolaraki E, Tyson AL, Pibiri F, Poulter SL, Reichelt AC, Rodgers RJ et al (2019) The within-subject application of diffusion tensor MRI and CLARITY reveals brain structural changes in Nrxn2 deletion mice. Mol Autism 10(1):8. (PMID: 308589646394023) Pilz LK, Quiles CL, Dallegrave E, Levandovski R, Hidalgo MPL, Elisabetsky E (2015) Differential susceptibility of BALB/c, C57BL/6N, and CF1 mice to photoperiod changes. Braz J Psychiatry 37(3):185–190. (PMID: 25806472) Potter M (1985) History of the BALB/c family. In: Potter M (ed) The BALB/c mouse [Internet]. Berlin: Springer; [cited 2020]. p 1–5. (Clarke A, Compans RW, Cooper M, Eisen H, Goebel W, Koprowski H et al (eds) Current topics in microbiology and immunology, vol. 122). Available from: http://link.springer.com/ https://doi.org/10.1007/978-3-642-70740-7_1. Qiu S, Anderson CT, Levitt P, Shepherd GMG (2011) Circuit-specific intracortical hyperconnectivity in mice with deletion of the autism-associated Met receptor tyrosine kinase. J Neurosci Off J Soc Neurosci 31(15):5855–5864. Reisert M, Mader I, Anastasopoulos C, Weigel M, Schnell S, Kiselev V (2011) Global fiber reconstruction becomes practical. NeuroImage 54(2):955–962. (PMID: 20854913) Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 25(1):230–242. (PMID: 15734358) Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14(9):609–625. (PMID: 23942470) Sankoorikal GMV, Kaercher KA, Boon CJ, Lee JK, Brodkin ES (2006) A mouse model system for genetic analysis of sociability: C57BL/6J versus BALB/cJ inbred mouse strains. Biol Psychiatry 59(5):415–423. (PMID: 16199013) Schilling KG, Nath V, Hansen C, Parvathaneni P, Blaber J, Gao Y et al (2019) Limits to anatomical accuracy of diffusion tractography using modern approaches. NeuroImage 15(185):1–11. Schilling KG, Rheault F, Petit L, Hansen CB, Nath V, Yeh F-C et al (2020) Tractography dissection variability: what happens when 42 groups dissect 14 white matter bundles on the same dataset? bioRxiv 2020.10.07.321083. Schroeter A, Grandjean J, Schlegel F, Saab BJ, Rudin M (2017) Contributions of structural connectivity and cerebrovascular parameters to functional magnetic resonance imaging signals in mice at rest and during sensory paw stimulation. J Cereb Blood Flow Metab 37(7):2368–2382. (PMID: 27596833) Shah D, Deleye S, Verhoye M, Staelens S, Van der Linden A (2016) Resting-state functional MRI and [18F]-FDG PET demonstrate differences in neuronal activity between commonly used mouse strains. NeuroImage 125:571–577. (PMID: 26520769) Shepherd GMG (2013) Corticostriatal connectivity and its role in disease. Nat Rev Neurosci 14(4):278–291. (PMID: 235119084096337) Smith JB, Liang Z, Watson GDR, Alloway KD, Zhang N (2017) Interhemispheric resting-state functional connectivity of the claustrum in the awake and anesthetized states. Brain Struct Funct 222(5):2041–2058. (PMID: 27714529) Stouffer SA (1949) A study of attitudes. Sci Am 180(5):11–15. (PMID: 18138375) Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA et al (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci 111(46):16574–16579. (PMID: 25368179) Torgerson CM, Irimia A, Goh SYM, Horn JDV (2015) The DTI connectivity of the human claustrum. Hum Brain Mapp 36(3):827–838. (PMID: 25339630) Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA et al (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29(6):1310–1320. (PMID: 30718553071855) van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17(12):683–696. (PMID: 24231140) Wahlsten D (1974) Heritable aspects of anomalous myelinated fibre tracts in the forebrain of the laboratory mouse. Brain Res 68(1):1–18. (PMID: 4470444) Wang N, White LE, Qi Y, Cofer G, Johnson GA (2020) Cytoarchitecture of the mouse brain by high resolution diffusion magnetic resonance imaging. NeuroImage 1(216):116876. Watson GDR, Smith JB, Alloway KD (2017) Interhemispheric connections between the infralimbic and entorhinal cortices: the endopiriform nucleus has limbic connections that parallel the sensory and motor connections of the claustrum: circuitry of dorsal endopiriform nucleus. J Comp Neurol 525(6):1363–1380. (PMID: 26860547) Weible AP (2013) Remembering to attend: the anterior cingulate cortex and remote memory. Behav Brain Res 245:63–75. (PMID: 23453992) Wu D, Zhang J (2016) In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI. NeuroImage 125:84–93. (PMID: 26499812) Wu G-R, Liao W, Stramaglia S, Ding J-R, Chen H, Marinazzo D (2013) A blind deconvolution approach to recover effective connectivity brain networks from resting state fMRI data. Med Image Anal 17(3):365–374. (PMID: 23422254) Yoshida M, Goto K, Watanabe S (2001) Task-dependent strain difference of spatial learning in C57BL/6N and BALB/c mice. Physiol Behav 73(1–2):37–42. (PMID: 11399292) Zhang WQ, Smolik CM, Barba-Escobedo PA, Gamez M, Sanchez JJ, Javors MA et al (2015) Acute dietary tryptophan manipulation differentially alters social behavior, brain serotonin and plasma corticosterone in three inbred mouse strains. Neuropharmacology 90:1–8. (PMID: 25445490) Zhang C, Arefin TM, Nakarmi U, Lee CH, Li H, Liang D et al (2020) Acceleration of three-dimensional diffusion magnetic resonance imaging using a kernel low-rank compressed sensing method. NeuroImage 15(210):116584. Zhou IY, Liang Y-X, Chan RW, Gao PP, Cheng JS, Hu Y et al (2014) Brain resting-state functional MRI connectivity: morphological foundation and plasticity. Neuroimage 1(84):1–10. |
معلومات مُعتمدة: | NeuroTime Erasmus+; 16658 United States AA NIAAA NIH HHS; 16658 United States AA NIAAA NIH HHS |
فهرسة مساهمة: | Keywords: BALB/cJ; C57BL6/N; Diffusion tensor imaging; Inbred strains; Mouse brain connectivity; Resting-state functional magnetic resonance imaging |
تواريخ الأحداث: | Date Created: 20210226 Date Completed: 20211102 Latest Revision: 20211102 |
رمز التحديث: | 20221213 |
DOI: | 10.1007/s00429-020-02190-8 |
PMID: | 33635426 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1863-2661 |
---|---|
DOI: | 10.1007/s00429-020-02190-8 |