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01-07-2018 | Original Article

Age, sex, and puberty related development of the corpus callosum: a multi-technique diffusion MRI study

Authors: Sila Genc, Charles B. Malpas, Gareth Ball, Timothy J. Silk, Marc L. Seal

Published in: Brain Structure and Function | Issue 6/2018

Abstract

The corpus callosum is integral to the central nervous system, and continually develops with age by virtue of increasing axon diameter and ongoing myelination. Magnetic resonance imaging (MRI) techniques offer a means to disentangle these two aspects of white matter development. We investigate the profile of microstructural metrics across the corpus callosum, and assess the impact of age, sex and pubertal development on these processes. This study made use of two independent paediatric populations. Multi-shell diffusion MRI data were analysed to produce a suite of diffusion tensor imaging, neurite orientation dispersion and density imaging, and apparent fibre density (AFD) metrics. A multivariate profile analysis was performed for each diffusion metric across ten subdivisions of the corpus callosum. All diffusion metrics significantly varied across the length of the corpus callosum. AFD exhibited a strong relationship with age across the corpus callosum (partial η² = 0.65), particularly in the posterior body of the corpus callosum (partial η² = 0.72). In addition, females had significantly higher AFD compared with males, most markedly in the anterior splenium (partial η² = 0.14) and posterior genu (partial η² = 0.13). Age-matched pubertal group differences were localised to the splenium. We present evidence of a strong relationship between apparent fibre density and age, sex, and puberty during development. These results are consistent with ex vivo studies of fibre morphology, providing insights into the dynamics of axonal development in childhood and adolescence using diffusion MRI.

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Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Res 598(1–2):143–153CrossRefPubMed

Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJM, Dyrby TB (2010) Orientationally invariant indices of axon diameter and density from diffusion MRI. Neuroimage 52(4):1374–1389. https://doi.org/10.1016/j.neuroimage.2010.05.043 CrossRefPubMed

Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15(7–8):435–455. https://doi.org/10.1002/nbm.782 CrossRefPubMed

Benjamin DJ, Berger JO, Johannesson M, Nosek BA, Wagenmakers EJ, Berk R, Bollen KA, Brembs B, Brown L, Camerer C, Cesarini D, Chambers CD, Clyde M, Cook TD, De Boeck P, Dienes Z, Dreber A, Easwaran K, Efferson C, Fehr E, Fidler F, Field AP, Forster M, George EI, Gonzalez R, Goodman S, Green E, Green DP, Greenwald AG, Hadfield JD, Hedges LV, Held L, Hua Ho T, Hoijtink H, Hruschka DJ, Imai K, Imbens G, Ioannidis JPA, Jeon M, Jones JH, Kirchler M, Laibson D, List J, Little R, Lupia A, Machery E, Maxwell SE, McCarthy M, Moore DA, Morgan SL, Munafó M, Nakagawa S, Nyhan B, Parker TH, Pericchi L, Perugini M, Rouder J, Rousseau J, Savalei V, Schönbrodt FD, Sellke T, Sinclair B, Tingley D, Van Zandt T, Vazire S, Watts DJ, Winship C, Wolpert RL, Xie Y, Young C, Zinman J, Johnson VE (2018) Redefine statistical significance. Nat Hum Behav 2(1):6–10. https://doi.org/10.1038/s41562-017-0189-z CrossRef

Berman S, West KL, Does MD, Yeatman JD, Mezer AA (2017) Evaluating g-ratio weighted changes in the corpus callosum as a function of age and sex. Neuroimage. https://doi.org/10.1016/j.neuroimage.2017.06.076 CrossRefPubMed

Bjornholm L, Nikkinen J, Kiviniemi V, Nordstrom T, Niemela S, Drakesmith M, Evans JC, Pike GB, Veijola J, Paus T (2017) Structural properties of the human corpus callosum: multimodal assessment and sex differences. Neuroimage 152:108–118. https://doi.org/10.1016/j.neuroimage.2017.02.056 CrossRefPubMed

Byrne ML, Whittle S, Vijayakumar N, Dennison M, Simmons JG, Allen NB (2017) A systematic review of adrenarche as a sensitive period in neurobiological development and mental health. Dev Cogn Neurosci 25:12–28. https://doi.org/10.1016/j.dcn.2016.12.004 CrossRefPubMed

Caminiti R, Carducci F, Piervincenzi C, Battaglia-Mayer A, Confalone G, Visco-Comandini F, Pantano P, Innocenti GM (2013) Diameter, length, speed, and conduction delay of callosal axons in macaque monkeys and humans: comparing data from histology and magnetic resonance imaging diffusion tractography. J Neurosci 33(36):14501-+. https://doi.org/10.1523/jneurosci.0761-13.2013 CrossRefPubMed

Chang YS, Owen JP, Pojman NJ, Thieu T, Bukshpun P, Wakahiro MLJ, Berman JI, Roberts TPL, Nagarajan SS, Sherr EH, Mukherjee P (2015) White matter changes of neurite density and fiber orientation dispersion during human brain maturation. PLoS One 10(6):e0123656. https://doi.org/10.1371/journal.pone.0123656 CrossRefPubMedPubMedCentral

Chang EH, Argyelan M, Aggarwal M, Chandon T-SS, Karlsgodt KH, Mori S, Malhotra AK (2017) The role of myelination in measures of white matter integrity: combination of diffusion tensor imaging and two-photon microscopy of CLARITY intact brains. Neuroimage 147:253–261. https://doi.org/10.1016/j.neuroimage.2016.11.068 CrossRefPubMed

Chavarria MC, Sanchez FJ, Chou YY, Thompson PM, Luders E (2014) Puberty in the corpus callosum. Neuroscience 265:1–8. https://doi.org/10.1016/j.neuroscience.2014.01.030 CrossRefPubMedPubMedCentral

Genc S, Malpas CB, Holland SK, Beare R, Silk TJ (2017a) Neurite density index is sensitive to age related differences in the developing brain. Neuroimage 148:373–380. https://doi.org/10.1016/j.neuroimage.2017.01.023 CrossRefPubMed

Genc S, Seal ML, Dhollander T, Malpas CB, Hazell P, Silk TJ (2017b) White matter alterations at pubertal onset. Neuroimage 156:286–292. https://doi.org/10.1016/j.neuroimage.2017.05.017 CrossRefPubMed

Grumbach MM, Styne DM (1998) Puberty: ontogeny, neuroendocrinology, physiology, and disorders. Williams Textb Endocrinol 9:1509–1625

Herting MM, Kim R, Uban KA, Kan E, Binley A, Sowell ER (2017) Longitudinal changes in pubertal maturation and white matter microstructure. Psychoneuroendocrinology 81:70–79. https://doi.org/10.1016/j.psyneuen.2017.03.017 CrossRefPubMedPubMedCentral

Highley JR, Esiri MM, McDonald B, Cortina-Borja M, Herron BM, Crow TJ (1999) The size and fibre composition of the corpus callosum with respect to gender and schizophrenia: a post-mortem study. Brain 122(Pt 1):99–110CrossRefPubMed

Holland SKVJ., Schmithorst VJ, Wagner M, Lee GR, Rajagopal A, Sroka MC, Felicelli N, Rupert A, Clark K, Toga AW, Freund LS, C-MIND Consortium (2015) The C-MIND project: normative MRI and behavioral data from children from birth to 18 years. In: 21st annual meeting of the organization for human brain mapping (OHBM), Honolulu, HA, 8–12 June 2015

Horowitz A, Barazany D, Tavor I, Bernstein M, Yovel G, Assaf Y (2015) In vivo correlation between axon diameter and conduction velocity in the human brain. Brain Struct Funct 220(3):1777–1788. https://doi.org/10.1007/s00429-014-0871-0 CrossRefPubMed

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 73:239–254. https://doi.org/10.1016/j.neuroimage.2012.06.081 CrossRefPubMed

Juraska JM, Willing J (2017) Pubertal onset as a critical transition for neural development and cognition. Brain Res 1654 Part B:87–94. https://doi.org/10.1016/j.brainres.2016.04.012 CrossRef

LaMantia A, Rakic P (1990) Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. J Neurosci 10(7):2156–2175CrossRefPubMed

Lebel C, Beaulieu C (2011) Longitudinal development of human brain wiring continues from childhood into adulthood. J Neurosci 31(30):10937–10947. https://doi.org/10.1523/jneurosci.5302-10.2011 CrossRefPubMed

Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40(3):1044–1055. https://doi.org/10.1016/j.neuroimage.2007.12.053 CrossRefPubMed

Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60(1):340–352. https://doi.org/10.1016/j.neuroimage.2011.11.094 CrossRefPubMed

Lenroot RK, Giedd JN (2006) Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev 30(6):718–729. https://doi.org/10.1016/j.neubiorev.2006.06.001 CrossRefPubMed

Liu F, Vidarsson L, Winter JD, Tran H, Kassner A (2010) Sex differences in the human corpus callosum microstructure: a combined T2 myelin-water and diffusion tensor magnetic resonance imaging study. Brain Res 1343:37–45. https://doi.org/10.1016/j.brainres.2010.04.064 CrossRefPubMed

Mah A, Geeraert B, Lebel C (2017) Detailing neuroanatomical development in late childhood and early adolescence using NODDI. PLoS One 12(8):e0182340. https://doi.org/10.1371/journal.pone.0182340 CrossRefPubMedPubMedCentral

Maninger N, Wolkowitz OM, Reus VI, Epel ES, Mellon SH (2009) Neurobiological and neuropsychiatric effects of dehydroepiandrosterone (DHEA) and DHEA sulfate (DHEAS). Front Neuroendocrinol 30(1):65–91. https://doi.org/10.1016/j.yfrne.2008.11.002 CrossRefPubMed

McNab JA, Edlow BL, Witzel T, Huang SY, Bhat H, Heberlein K, Feiweier T, Liu K, Keil B, Cohen-Adad J, Tisdall MD, Folkerth RD, Kinney HC, Wald LL (2013) The human connectome project and beyond: initial applications of 300 mT/m gradients. Neuroimage 80:234–245. https://doi.org/10.1016/j.neuroimage.2013.05.074 CrossRefPubMed

Mills KL, Goddings A-L, Herting MM, Meuwese R, Blakemore S-J, Crone EA, Dahl RE, Güroğlu B, Raznahan A, Sowell ER, Tamnes CK (2016) Structural brain development between childhood and adulthood: convergence across four longitudinal samples. Neuroimage 141:273–281. https://doi.org/10.1016/j.neuroimage.2016.07.044 CrossRefPubMedPubMedCentral

Mollink J, Kleinnijenhuis M, Cappellen van Walsum A-Mv, Sotiropoulos SN, Cottaar M, Mirfin C, Heinrich MP, Jenkinson M, Pallebage-Gamarallage M, Ansorge O, Jbabdi S, Miller KL (2017) Evaluating fibre orientation dispersion in white matter: comparison of diffusion MRI, histology and polarized light imaging. Neuroimage 157:561–574. https://doi.org/10.1016/j.neuroimage.2017.06.001 CrossRefPubMedPubMedCentral

Nave K-A (2010) Myelination and support of axonal integrity by glia. Nature 468(7321):244–252CrossRefPubMed

Nilsson M, Latt J, Stahlberg F, van Westen D, Hagslatt H (2012) The importance of axonal undulation in diffusion MR measurements: a Monte Carlo simulation study. NMR Biomed 25(5):795–805. https://doi.org/10.1002/nbm.1795 CrossRefPubMed

Nilsson M, Lasic S, Drobnjak I, Topgaard D, Westin CF (2017) Resolution limit of cylinder diameter estimation by diffusion MRI: the impact of gradient waveform and orientation dispersion. NMR Biomed 30(7):e3711. https://doi.org/10.1002/nbm.3711 CrossRefPubMedCentral

Pangelinan MM, Leonard G, Perron M, Pike GB, Richer L, Veillette S, Pausova Z, Paus T (2016) Puberty and testosterone shape the corticospinal tract during male adolescence. Brain Struct Funct 221(2):1083–1094. https://doi.org/10.1007/s00429-014-0956-9 CrossRefPubMed

Paus T (2010) Growth of white matter in the adolescent brain: myelin or axon? Brain Cogn 72(1):26–35. https://doi.org/10.1016/j.bandc.2009.06.002 CrossRefPubMed

Paus T, Toro R (2009) Could sex differences in white matter be explained by g ratio?. Front Neuroanat 3 (14). https://doi.org/10.3389/neuro.05.014.2009

Perrin JS, Herve PY, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T (2008) Growth of white matter in the adolescent brain: role of testosterone and androgen receptor. J Neurosci 28(38):9519–9524. https://doi.org/10.1523/jneurosci.1212-08.2008 CrossRefPubMed

Perrin JS, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T (2009) Sex differences in the growth of white matter during adolescence. Neuroimage 45(4):1055–1066. https://doi.org/10.1016/j.neuroimage.2009.01.023 CrossRefPubMed

Pesaresi M, Soon-Shiong R, French L, Kaplan DR, Miller FD, Paus T (2015) Axon diameter and axonal transport: in vivo and in vitro effects of androgens. Neuroimage 115:191–201. https://doi.org/10.1016/j.neuroimage.2015.04.048 CrossRefPubMedPubMedCentral

Raffelt D, Tournier JD, Rose S, Ridgway GR, Henderson R, Crozier S, Salvado O, Connelly A (2012) Apparent fibre density: a novel measure for the analysis of diffusion-weighted magnetic resonance images. Neuroimage 59(4):3976–3994. https://doi.org/10.1016/j.neuroimage.2011.10.045 CrossRefPubMed

Raffelt DA, Smith RE, Ridgway GR, Tournier JD, Vaughan DN, Rose S, Henderson R, Connelly A (2015) Connectivity-based fixel enhancement: whole-brain statistical analysis of diffusion MRI measures in the presence of crossing fibres. Neuroimage 117:40–55. https://doi.org/10.1016/j.neuroimage.2015.05.039 CrossRefPubMedPubMedCentral

Raffelt DA, Tournier JD, Smith RE, Vaughan DN, Jackson G, Ridgway GR, Connelly A (2017) Investigating white matter fibre density and morphology using fixel-based analysis. Neuroimage 144 (Pt A):58–73. https://doi.org/10.1016/j.neuroimage.2016.09.029 CrossRefPubMedPubMedCentral

Ronen I, Budde M, Ercan E, Annese J, Techawiboonwong A, Webb A (2014) Microstructural organization of axons in the human corpus callosum quantified by diffusion-weighted magnetic resonance spectroscopy of N-acetylaspartate and post-mortem histology. Brain Struct Funct 219(5):1773–1785. https://doi.org/10.1007/s00429-013-0600-0 CrossRefPubMed

Schulz KM, Molenda-Figueira HA, Sisk CL (2009) Back to the future: the organizational–activational hypothesis adapted to puberty and adolescence. Horm Behav 55(5):597–604. https://doi.org/10.1016/j.yhbeh.2009.03.010 CrossRefPubMedPubMedCentral

Sciberras E, Efron D, Schilpzand EJ, Anderson V, Jongeling B, Hazell P, Ukoumunne OC, Nicholson JM (2013) The Children’s Attention Project: a community-based longitudinal study of children with ADHD and non-ADHD controls. BMC Psychiatry 13:18–18. https://doi.org/10.1186/1471-244X-13-18 CrossRefPubMedPubMedCentral

Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6(9):683–690. https://doi.org/10.1038/nrn1743 CrossRefPubMed

Shirtcliff EA, Dahl RE, Pollak SD (2009) Pubertal development: correspondence between hormonal and physical development. Child Dev 80(2):327–337CrossRefPubMedPubMedCentral

Silk TJ, Genc S, Anderson V, Efron D, Hazell P, Nicholson JM, Kean M, Malpas CB, Sciberras E (2016) Developmental brain trajectories in children with ADHD and controls: a longitudinal neuroimaging study. BMC Psychiatry 16:59. https://doi.org/10.1186/s12888-016-0770-4 CrossRefPubMedPubMedCentral

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang YY, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208-S219. https://doi.org/10.1016/j.neuroimage.2004.07.051 CrossRef

Stikov N, Campbell JSW, Stroh T, Lavelee M, Frey S, Novek J, Nuara S, Ho MK, Bedell BJ, Dougherty RF, Leppert IR, Boudreau M, Narayanan S, Duval T, Cohen-Adad J, Picard PA, Gasecka A, Cote D, Pike GB (2015) In vivo histology of the myelin g-ratio with magnetic resonance imaging. Neuroimage 118:397–405. https://doi.org/10.1016/j.neuroimage.2015.05.023 CrossRefPubMed

Vos SB, Jones DK, Viergever MA, Leemans A (2011) Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 55(4):1566–1576. https://doi.org/10.1016/j.neuroimage.2011.01.048 CrossRefPubMed

Yakovlev PI, Lecours AR (1967) The myelogenetic cycles of regional maturation of the brain. In: Minkowski A (ed) Regional development of the brain in early life. Blackwell, Oxford, pp 3–70

Zhang H, Yushkevich PA, Alexander DC, Gee JC (2006) Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med Image Anal 10(5):764–785. https://doi.org/10.1016/j.media.2006.06.004 CrossRefPubMed

Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61(4):1000–1016. https://doi.org/10.1016/j.neuroimage.2012.03.072 CrossRefPubMed

Title: Age, sex, and puberty related development of the corpus callosum: a multi-technique diffusion MRI study
Authors: Sila Genc
Charles B. Malpas
Gareth Ball
Timothy J. Silk
Marc L. Seal
Publication date: 01-07-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1658-5

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Age, sex, and puberty related development of the corpus callosum: a multi-technique diffusion MRI study

Abstract

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