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Published in: Brain Structure and Function 1/2018

01-01-2018 | Original Article

Nanoscale structural mapping as a measure of maturation in the murine frontal cortex

Authors: G. Smolyakov, E. Dague, C. Roux, M. H. Seguelas, C. Galés, J. M. Senard, D. N. Arvanitis

Published in: Brain Structure and Function | Issue 1/2018

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Abstract

Atomic force microscopy (AFM) is emerging as an innovative tool to phenotype the brain. This study demonstrates the utility of AFM to determine nanomechanical and nanostructural features of the murine dorsolateral frontal cortex from weaning to adulthood. We found an increase in tissue stiffness of the primary somatosensory cortex with age, along with an increased cortical mechanical heterogeneity. To characterize the features potentially responsible for this heterogeneity, we applied AFM scan mode to directly image the topography of thin sections of the primary somatosensory cortical layers II/III, IV and V/VI. Topographical mapping of the cortical layers at successive ages showed progressive smoothing of the surface. Topographical images were also compared with histochemically derived morphological information, which demonstrated the deposition of perineuronal nets, important extracellular components and markers of maturity. Our work demonstrates that high-resolution AFM images can be used to determine the nanostructural properties of cortical maturation, well beyond embryonic and postnatal development. Furthermore, it may offer a new method for brain phenotyping and screening to uncover topographical changes in early stages of neurodegenerative diseases.
Literature
go back to reference Antunes A, Gozzo FV, Borella MI, Nakamura M, Safatle MV, Barros PSM, Toma HE (2007) Atomic Force Imaging of Ocular Tissues: morphological study of healthy and cataract lenses. Mod Res Educ Top Microsc. Mendez-Villas et Diaz, Spain, pp 29–36 Antunes A, Gozzo FV, Borella MI, Nakamura M, Safatle MV, Barros PSM, Toma HE (2007) Atomic Force Imaging of Ocular Tissues: morphological study of healthy and cataract lenses. Mod Res Educ Top Microsc. Mendez-Villas et Diaz, Spain, pp 29–36
go back to reference Beaussart A, El-Kirat-Chatel S, Sullan RMA, Alsteens D, Herman P, Derclaye S, Dufrêne YF (2014) Quantifying the forces guiding microbial cell adhesion using single-cell force spectroscopy. Nat Protoc 9:1049–1055. doi:10.1038/nprot.2014.066 CrossRefPubMed Beaussart A, El-Kirat-Chatel S, Sullan RMA, Alsteens D, Herman P, Derclaye S, Dufrêne YF (2014) Quantifying the forces guiding microbial cell adhesion using single-cell force spectroscopy. Nat Protoc 9:1049–1055. doi:10.​1038/​nprot.​2014.​066 CrossRefPubMed
go back to reference Burnham NA, Colton RJ (1998) Measuring the nanomechanical properties and surface forces of materials using an atomic force microscope. J Vac Sci Technol Vac Surf Film. doi:10.1116/1.576168 Burnham NA, Colton RJ (1998) Measuring the nanomechanical properties and surface forces of materials using an atomic force microscope. J Vac Sci Technol Vac Surf Film. doi:10.​1116/​1.​576168
go back to reference Carulli D, Rhodes KE, Fawcett JW (2007) Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J Comp Neurol 501:83–94. doi:10.1002/cne.21231 CrossRefPubMed Carulli D, Rhodes KE, Fawcett JW (2007) Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J Comp Neurol 501:83–94. doi:10.​1002/​cne.​21231 CrossRefPubMed
go back to reference Di Cristo G, Chattopadhyaya B, Kuhlman SJ, Fu Y, Bélanger M-C, Wu CZ, Rutishauser U, Maffei L, Huang ZJ (2007) Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat Neurosci 10:1569–1577. doi:10.1038/nn2008 CrossRefPubMed Di Cristo G, Chattopadhyaya B, Kuhlman SJ, Fu Y, Bélanger M-C, Wu CZ, Rutishauser U, Maffei L, Huang ZJ (2007) Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat Neurosci 10:1569–1577. doi:10.​1038/​nn2008 CrossRefPubMed
go back to reference Formosa C, Schiavone M, Martin-Yken H, François JM, Duval RE, Dague E (2013) Nanoscale effects of caspofungin against two yeast species, Saccharomyces Cerevisiae and Candida albicans. Antimicrob Agent Chemother 57:3498–3506. doi:10.1128/AAC.00105-13 CrossRef Formosa C, Schiavone M, Martin-Yken H, François JM, Duval RE, Dague E (2013) Nanoscale effects of caspofungin against two yeast species, Saccharomyces Cerevisiae and Candida albicans. Antimicrob Agent Chemother 57:3498–3506. doi:10.​1128/​AAC.​00105-13 CrossRef
go back to reference Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861–863. doi:10.1038/13158 CrossRefPubMed Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861–863. doi:10.​1038/​13158 CrossRefPubMed
go back to reference Hertz H (1882) Uber die beruhrung fester elastischer korper (on the contact of elastic solids). J Reine Angew Math 92:156–171 Hertz H (1882) Uber die beruhrung fester elastischer korper (on the contact of elastic solids). J Reine Angew Math 92:156–171
go back to reference Iwashita M, Kataoka N, Toida K, Kosodo Y (2014) Systematic profiling of spatiotemporal tissue and cellular stiffness in the developing brain. Dev Camb Engl 141:3793–3798. doi:10.1242/dev.109637 Iwashita M, Kataoka N, Toida K, Kosodo Y (2014) Systematic profiling of spatiotemporal tissue and cellular stiffness in the developing brain. Dev Camb Engl 141:3793–3798. doi:10.​1242/​dev.​109637
go back to reference Li Q, Bozek K, Xu C, Guo Y, Sun J, Pääbo S, Sherwood CC, Hof PR, Ely JJ, Li Y, Willmitzer L, Giavalisco P, Khaitovich P (2017) Changes in lipidome composition during brain development in humans, chimpanzees, and macaque monkeys. Mol Biol Evol 34:1155. doi:10.1093/molbev/msx065 CrossRefPubMedPubMedCentral Li Q, Bozek K, Xu C, Guo Y, Sun J, Pääbo S, Sherwood CC, Hof PR, Ely JJ, Li Y, Willmitzer L, Giavalisco P, Khaitovich P (2017) Changes in lipidome composition during brain development in humans, chimpanzees, and macaque monkeys. Mol Biol Evol 34:1155. doi:10.​1093/​molbev/​msx065 CrossRefPubMedPubMedCentral
go back to reference Litinetsky L, Barkay Z, Kalicharan D, Rosenzweig E, Ishay JS (2002) AFM study of microstructures on the cornea of the compound eye and ocelli of the hornet Vespa orientalis (Insecta, Hymenoptera). Physiol Chem Phys Med NMR 34:61–69PubMed Litinetsky L, Barkay Z, Kalicharan D, Rosenzweig E, Ishay JS (2002) AFM study of microstructures on the cornea of the compound eye and ocelli of the hornet Vespa orientalis (Insecta, Hymenoptera). Physiol Chem Phys Med NMR 34:61–69PubMed
go back to reference MacGregor DG, Chesler M, Rice ME (2001) HEPES prevents edema in rat brain slices. Neurosci Lett 303:141–144CrossRefPubMed MacGregor DG, Chesler M, Rice ME (2001) HEPES prevents edema in rat brain slices. Neurosci Lett 303:141–144CrossRefPubMed
go back to reference Moeendarbary E, Weber IP, Sheridan GK, Koser DE, Soleman S, Haenzi B, Bradbury EJ, Fawcett J, Franze K (2017) The soft mechanical signature of glial scars in the central nervous system. Nat Commun. doi:10.1038/ncomms14787 Moeendarbary E, Weber IP, Sheridan GK, Koser DE, Soleman S, Haenzi B, Bradbury EJ, Fawcett J, Franze K (2017) The soft mechanical signature of glial scars in the central nervous system. Nat Commun. doi:10.​1038/​ncomms14787
go back to reference Schiavone M, Vax A, Formosa C, Martin-Yken H, Dague E, François JM (2014) A combined chemical and enzymatic method to determine quantitatively the polysaccharide components in the cell wall of yeasts. FEMS Yeast Res 14:933–947. doi:10.1111/1567-1364.12182 CrossRefPubMed Schiavone M, Vax A, Formosa C, Martin-Yken H, Dague E, François JM (2014) A combined chemical and enzymatic method to determine quantitatively the polysaccharide components in the cell wall of yeasts. FEMS Yeast Res 14:933–947. doi:10.​1111/​1567-1364.​12182 CrossRefPubMed
go back to reference Thalhammer S, Heckl WM, Zink A, Nerlich AG (2001) Atomic force microscopy for high resolution imaging of collagen fibrils—a new technique to investigate collagen structure in historic bone tissues. J Archaeol Sci 28:1061–1068. doi:10.1006/jasc.2000.0644 CrossRef Thalhammer S, Heckl WM, Zink A, Nerlich AG (2001) Atomic force microscopy for high resolution imaging of collagen fibrils—a new technique to investigate collagen structure in historic bone tissues. J Archaeol Sci 28:1061–1068. doi:10.​1006/​jasc.​2000.​0644 CrossRef
go back to reference Ungureanu A-A, Benilova I, Krylychkina O, Braeken D, De Strooper B, Van Haesendonck C, Dotti CG, Bartic C (2016) Amyloid beta oligomers induce neuronal elasticity changes in age-dependent manner: a force spectroscopy study on living hippocampal neurons. Sci Rep 6:25841. doi:10.1038/srep25841 CrossRefPubMedPubMedCentral Ungureanu A-A, Benilova I, Krylychkina O, Braeken D, De Strooper B, Van Haesendonck C, Dotti CG, Bartic C (2016) Amyloid beta oligomers induce neuronal elasticity changes in age-dependent manner: a force spectroscopy study on living hippocampal neurons. Sci Rep 6:25841. doi:10.​1038/​srep25841 CrossRefPubMedPubMedCentral
go back to reference Zhang P, Yang Y, Candiello J, Thorn TL, Gray N, Halfter WM, Hu H (2013) Biochemical and biophysical changes underlie the mechanisms of basement membrane disruptions in a mouse model of dystroglycanopathy. Matrix Biol J Int Soc Matrix Biol 32:196–207. doi:10.1016/j.matbio.2013.02.002 CrossRef Zhang P, Yang Y, Candiello J, Thorn TL, Gray N, Halfter WM, Hu H (2013) Biochemical and biophysical changes underlie the mechanisms of basement membrane disruptions in a mouse model of dystroglycanopathy. Matrix Biol J Int Soc Matrix Biol 32:196–207. doi:10.​1016/​j.​matbio.​2013.​02.​002 CrossRef
Metadata
Title
Nanoscale structural mapping as a measure of maturation in the murine frontal cortex
Authors
G. Smolyakov
E. Dague
C. Roux
M. H. Seguelas
C. Galés
J. M. Senard
D. N. Arvanitis
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1486-z

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