Skip to main content
Erschienen in: Brain Structure and Function 3/2021

26.02.2021 | Original Article

Mapping the living mouse brain neural architecture: strain-specific patterns of brain structural and functional connectivity

verfasst von: Meltem Karatas, Vincent Noblet, Md Taufiq Nasseef, Thomas Bienert, Marco Reisert, Jürgen Hennig, Ipek Yalcin, Brigitte Lina Kieffer, Dominik von Elverfeldt, Laura-Adela Harsan

Erschienen in: Brain Structure and Function | Ausgabe 3/2021

Einloggen, um Zugang zu erhalten

Abstract

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.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat 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):61–73PubMedCrossRef 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):61–73PubMedCrossRef
Zurück zum Zitat 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):95–104PubMedCrossRef 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):95–104PubMedCrossRef
Zurück zum Zitat 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):2033–2044PubMedCrossRef 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):2033–2044PubMedCrossRef
Zurück zum Zitat 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):2841–2858PubMedPubMedCentralCrossRef 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):2841–2858PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):32060PubMedPubMedCentralCrossRef 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):32060PubMedPubMedCentralCrossRef
Zurück zum Zitat Barnett L, Seth AK (2014) The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference. J Neurosci Methods 15(223):50–68CrossRef Barnett L, Seth AK (2014) The MVGC multivariate Granger causality toolbox: a new approach to Granger-causal inference. J Neurosci Methods 15(223):50–68CrossRef
Zurück zum Zitat Belzung C, Barreau S (2000) Differences in drug-induced place conditioning between BALB/c and C57Bl/6 mice. Pharmacol Biochem Behav 65(3):419–423PubMedCrossRef Belzung C, Barreau S (2000) Differences in drug-induced place conditioning between BALB/c and C57Bl/6 mice. Pharmacol Biochem Behav 65(3):419–423PubMedCrossRef
Zurück zum Zitat Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125(1–2):141–149PubMedCrossRef Belzung C, Griebel G (2001) Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125(1–2):141–149PubMedCrossRef
Zurück zum Zitat 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):401–407PubMedCrossRef 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):401–407PubMedCrossRef
Zurück zum Zitat 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):537–541PubMedCrossRef 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):537–541PubMedCrossRef
Zurück zum Zitat Brodkin ES (2007) BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav Brain Res 176(1):53–65PubMedCrossRef Brodkin ES (2007) BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav Brain Res 176(1):53–65PubMedCrossRef
Zurück zum Zitat 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):151–157PubMedCrossRef 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):151–157PubMedCrossRef
Zurück zum Zitat 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):4628–4637PubMedPubMedCentralCrossRef 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):4628–4637PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):1259–1266PubMedCrossRef 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):1259–1266PubMedCrossRef
Zurück zum Zitat 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):286–296PubMedCrossRef 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):286–296PubMedCrossRef
Zurück zum Zitat 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):1111–1120PubMedCrossRef 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):1111–1120PubMedCrossRef
Zurück zum Zitat Chen C, Kim JJ, Thompson RF, Tonegawa S (1996) Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110(5):1177–1180PubMedCrossRef Chen C, Kim JJ, Thompson RF, Tonegawa S (1996) Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110(5):1177–1180PubMedCrossRef
Zurück zum Zitat Chuang K-H, Nasrallah FA (2017) Functional networks and network perturbations in rodents. NeuroImage 163:419–436PubMedCrossRef Chuang K-H, Nasrallah FA (2017) Functional networks and network perturbations in rodents. NeuroImage 163:419–436PubMedCrossRef
Zurück zum Zitat 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):718–730PubMedPubMedCentral 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):718–730PubMedPubMedCentral
Zurück zum Zitat 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):107–124PubMedCrossRef 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):107–124PubMedCrossRef
Zurück zum Zitat 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 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
Zurück zum Zitat Dennis EL, Thompson PM (2013) Typical and atypical brain development: a review of neuroimaging studies. Clin Res 15(3):26 Dennis EL, Thompson PM (2013) Typical and atypical brain development: a review of neuroimaging studies. Clin Res 15(3):26
Zurück zum Zitat 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):1423–1434PubMedCrossRef 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):1423–1434PubMedCrossRef
Zurück zum Zitat 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):1023–1029PubMedCrossRef 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):1023–1029PubMedCrossRef
Zurück zum Zitat 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):118–125PubMedCrossRef 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):118–125PubMedCrossRef
Zurück zum Zitat 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):211–217CrossRef 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):211–217CrossRef
Zurück zum Zitat 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):299–310PubMedCrossRef 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):299–310PubMedCrossRef
Zurück zum Zitat 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 237:338–347PubMedCrossRef 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 237:338–347PubMedCrossRef
Zurück zum Zitat 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):25–33PubMedCrossRef 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):25–33PubMedCrossRef
Zurück zum Zitat 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 153:382–398PubMedCrossRef 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 153:382–398PubMedCrossRef
Zurück zum Zitat Good CD, Ashburner J, Frackowiak RS (2001) Computational neuroanatomy: new perspectives for neuroradiology. Rev Neurol 157(8–9 Pt 1):797–806PubMed Good CD, Ashburner J, Frackowiak RS (2001) Computational neuroanatomy: new perspectives for neuroradiology. Rev Neurol 157(8–9 Pt 1):797–806PubMed
Zurück zum Zitat 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):8092–8101PubMedPubMedCentralCrossRef 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):8092–8101PubMedPubMedCentralCrossRef
Zurück zum Zitat Grange P (2020) Topology of the mesoscale connectome of the mouse brain. Comput Math Biophys 8(1):126–140CrossRef Grange P (2020) Topology of the mesoscale connectome of the mouse brain. Comput Math Biophys 8(1):126–140CrossRef
Zurück zum Zitat 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):363–372CrossRef 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):363–372CrossRef
Zurück zum Zitat Grubb SC, Churchill GA, Bogue MA (2004) A collaborative database of inbred mouse strain characteristics. Bioinformatics 20(16):2857–2859PubMedCrossRef Grubb SC, Churchill GA, Bogue MA (2004) A collaborative database of inbred mouse strain characteristics. Bioinformatics 20(16):2857–2859PubMedCrossRef
Zurück zum Zitat 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):1535–1551PubMedPubMedCentralCrossRef 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):1535–1551PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):117–124PubMedCrossRef 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):117–124PubMedCrossRef
Zurück zum Zitat 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):331–341PubMedCrossRef 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):331–341PubMedCrossRef
Zurück zum Zitat 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–E1806PubMedPubMedCentralCrossRef 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–E1806PubMedPubMedCentralCrossRef
Zurück zum Zitat Horsfield MA, Jones DK (2002) Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases—a review. NMR Biomed 15(7–8):570–577PubMedCrossRef Horsfield MA, Jones DK (2002) Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases—a review. NMR Biomed 15(7–8):570–577PubMedCrossRef
Zurück zum Zitat 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):1–18CrossRef 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):1–18CrossRef
Zurück zum Zitat 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):2696–2706PubMedCrossRef 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):2696–2706PubMedCrossRef
Zurück zum Zitat 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):393–400CrossRef 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):393–400CrossRef
Zurück zum Zitat Johnson GA, Wang N, Anderson RJ, Chen M, Cofer GP, Gee JC et al (2019) Whole mouse brain connectomics. J Comp Neurol 527(13):2146–2157CrossRef Johnson GA, Wang N, Anderson RJ, Chen M, Cofer GP, Gee JC et al (2019) Whole mouse brain connectomics. J Comp Neurol 527(13):2146–2157CrossRef
Zurück zum Zitat 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):807–815PubMedCrossRef 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):807–815PubMedCrossRef
Zurück zum Zitat 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):239–254CrossRef 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):239–254CrossRef
Zurück zum Zitat 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):951–961PubMedCrossRef 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):951–961PubMedCrossRef
Zurück zum Zitat 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):289–294PubMedPubMedCentralCrossRef 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):289–294PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):104–112PubMedCrossRef 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):104–112PubMedCrossRef
Zurück zum Zitat 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):217–236PubMedCrossRef 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):217–236PubMedCrossRef
Zurück zum Zitat 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 1455:56–67PubMedPubMedCentralCrossRef 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 1455:56–67PubMedPubMedCentralCrossRef
Zurück zum Zitat 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 318:12–21PubMedCrossRef 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 318:12–21PubMedCrossRef
Zurück zum Zitat Lassi G, Tucci V (2017) Gene-environment interaction influences attachment-like style in mice. Genes Brain Behav 16(6):612–618PubMedCrossRef Lassi G, Tucci V (2017) Gene-environment interaction influences attachment-like style in mice. Genes Brain Behav 16(6):612–618PubMedCrossRef
Zurück zum Zitat Lee H-L, Zahneisen B, Hugger T, LeVan P, Hennig J (2013) Tracking dynamic resting-state networks at higher frequencies using MR-encephalography. NeuroImage 65:216–222PubMedCrossRef Lee H-L, Zahneisen B, Hugger T, LeVan P, Hennig J (2013) Tracking dynamic resting-state networks at higher frequencies using MR-encephalography. NeuroImage 65:216–222PubMedCrossRef
Zurück zum Zitat 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):168–176PubMedCrossRef 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):168–176PubMedCrossRef
Zurück zum Zitat Liska A, Galbusera A, Schwarz AJ, Gozzi A (2015) Functional connectivity hubs of the mouse brain. NeuroImage 115:281–291PubMedCrossRef Liska A, Galbusera A, Schwarz AJ, Gozzi A (2015) Functional connectivity hubs of the mouse brain. NeuroImage 115:281–291PubMedCrossRef
Zurück zum Zitat 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):1349PubMedPubMedCentralCrossRef 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):1349PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):11603–11608PubMedPubMedCentralCrossRef 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):11603–11608PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):4–20PubMedCrossRef 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):4–20PubMedCrossRef
Zurück zum Zitat 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 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
Zurück zum Zitat 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):147–154PubMedCrossRef 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):147–154PubMedCrossRef
Zurück zum Zitat 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):12–20PubMedCrossRef 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):12–20PubMedCrossRef
Zurück zum Zitat 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):8PubMedPubMedCentralCrossRef 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):8PubMedPubMedCentralCrossRef
Zurück zum Zitat 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):185–190PubMedCrossRef 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):185–190PubMedCrossRef
Zurück zum Zitat 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 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
Zurück zum Zitat 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):5855–5864CrossRef 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):5855–5864CrossRef
Zurück zum Zitat Reisert M, Mader I, Anastasopoulos C, Weigel M, Schnell S, Kiselev V (2011) Global fiber reconstruction becomes practical. NeuroImage 54(2):955–962PubMedCrossRef Reisert M, Mader I, Anastasopoulos C, Weigel M, Schnell S, Kiselev V (2011) Global fiber reconstruction becomes practical. NeuroImage 54(2):955–962PubMedCrossRef
Zurück zum Zitat Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 25(1):230–242PubMedCrossRef Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 25(1):230–242PubMedCrossRef
Zurück zum Zitat Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14(9):609–625PubMedCrossRef Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14(9):609–625PubMedCrossRef
Zurück zum Zitat 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):415–423PubMedCrossRef 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):415–423PubMedCrossRef
Zurück zum Zitat 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):1–11CrossRef 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):1–11CrossRef
Zurück zum Zitat 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. 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.
Zurück zum Zitat 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):2368–2382PubMedCrossRef 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):2368–2382PubMedCrossRef
Zurück zum Zitat 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 125:571–577PubMedCrossRef 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 125:571–577PubMedCrossRef
Zurück zum Zitat 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):2041–2058PubMedCrossRef 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):2041–2058PubMedCrossRef
Zurück zum Zitat 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):16574–16579PubMedPubMedCentralCrossRef 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):16574–16579PubMedPubMedCentralCrossRef
Zurück zum Zitat Torgerson CM, Irimia A, Goh SYM, Horn JDV (2015) The DTI connectivity of the human claustrum. Hum Brain Mapp 36(3):827–838PubMedCrossRef Torgerson CM, Irimia A, Goh SYM, Horn JDV (2015) The DTI connectivity of the human claustrum. Hum Brain Mapp 36(3):827–838PubMedCrossRef
Zurück zum Zitat 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):1310–1320PubMedPubMedCentralCrossRef 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):1310–1320PubMedPubMedCentralCrossRef
Zurück zum Zitat van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17(12):683–696PubMedCrossRef van den Heuvel MP, Sporns O (2013) Network hubs in the human brain. Trends Cogn Sci 17(12):683–696PubMedCrossRef
Zurück zum Zitat Wahlsten D (1974) Heritable aspects of anomalous myelinated fibre tracts in the forebrain of the laboratory mouse. Brain Res 68(1):1–18PubMedCrossRef Wahlsten D (1974) Heritable aspects of anomalous myelinated fibre tracts in the forebrain of the laboratory mouse. Brain Res 68(1):1–18PubMedCrossRef
Zurück zum Zitat 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):116876CrossRef 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):116876CrossRef
Zurück zum Zitat 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):1363–1380PubMedCrossRef 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):1363–1380PubMedCrossRef
Zurück zum Zitat Weible AP (2013) Remembering to attend: the anterior cingulate cortex and remote memory. Behav Brain Res 245:63–75PubMedCrossRef Weible AP (2013) Remembering to attend: the anterior cingulate cortex and remote memory. Behav Brain Res 245:63–75PubMedCrossRef
Zurück zum Zitat Wu D, Zhang J (2016) In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI. NeuroImage 125:84–93PubMedCrossRef Wu D, Zhang J (2016) In vivo mapping of macroscopic neuronal projections in the mouse hippocampus using high-resolution diffusion MRI. NeuroImage 125:84–93PubMedCrossRef
Zurück zum Zitat 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):365–374PubMedCrossRef 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):365–374PubMedCrossRef
Zurück zum Zitat 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):37–42PubMedCrossRef 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):37–42PubMedCrossRef
Zurück zum Zitat 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 90:1–8PubMedCrossRef 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 90:1–8PubMedCrossRef
Zurück zum Zitat 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):116584CrossRef 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):116584CrossRef
Zurück zum Zitat 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):1–10CrossRef 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):1–10CrossRef
Metadaten
Titel
Mapping the living mouse brain neural architecture: strain-specific patterns of brain structural and functional connectivity
verfasst von
Meltem Karatas
Vincent Noblet
Md Taufiq Nasseef
Thomas Bienert
Marco Reisert
Jürgen Hennig
Ipek Yalcin
Brigitte Lina Kieffer
Dominik von Elverfeldt
Laura-Adela Harsan
Publikationsdatum
26.02.2021
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 3/2021
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02190-8

Weitere Artikel der Ausgabe 3/2021

Brain Structure and Function 3/2021 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.