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Published in: Brain Structure and Function 3/2019

Open Access 01-04-2019 | Magnetic Resonance Imaging | Original Article

Local-to-distant development of the cerebrocerebellar sensorimotor network in the typically developing human brain: a functional and diffusion MRI study

Authors: Kaoru Amemiya, Tomoyo Morita, Daisuke N. Saito, Midori Ban, Koji Shimada, Yuko Okamoto, Hirotaka Kosaka, Hidehiko Okazawa, Minoru Asada, Eiichi Naito

Published in: Brain Structure and Function | Issue 3/2019

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Abstract

Sensorimotor function is a fundamental brain function in humans, and the cerebrocerebellar circuit is essential to this function. In this study, we demonstrate how the cerebrocerebellar circuit develops both functionally and anatomically from childhood to adulthood in the typically developing human brain. We measured brain activity using functional magnetic resonance imaging while a total of 57 right-handed, blindfolded, healthy children (aged 8–11 years), adolescents (aged 12–15 years), and young adults (aged 18–23 years) (n = 19 per group) performed alternating extension–flexion movements of their right wrists in precise synchronization with 1-Hz audio tones. We also collected their diffusion MR images to examine the extent of fiber maturity in cerebrocerebellar afferent and efferent tracts by evaluating the anisotropy-sensitive index of hindrance modulated orientational anisotropy (HMOA). During the motor task, although the ipsilateral cerebellum and the contralateral primary sensorimotor cortices were consistently activated across all age groups, the functional connectivity between these two distant regions was stronger in adults than in children and adolescents, whereas connectivity within the local cerebellum was stronger in children and adolescents than in adults. The HMOA values in cerebrocerebellar afferent and efferent tracts were higher in adults than in children (some were also higher than in adolescents). The results indicate that adult-like cerebrocerebellar functional coupling is not completely achieved during childhood and adolescence, even for fundamental sensorimotor brain function, probably due to anatomical immaturity of cerebrocerebellar tracts. This study clearly demonstrated the principle of “local-to-distant” development of functional brain networks in the human cerebrocerebellar sensorimotor network.
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Literature
go back to reference Catani M, Thiebaut de Schotten M (2012) Atlas of human brain connections. Oxford University Press, New YorkCrossRef Catani M, Thiebaut de Schotten M (2012) Atlas of human brain connections. Oxford University Press, New YorkCrossRef
go back to reference Dell’Acqua F, Simmons A, Williams SC, Catani M (2013) Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Hum Brain Mapp 34:2464–2483. https://doi.org/10.1002/hbm.22080 CrossRefPubMed Dell’Acqua F, Simmons A, Williams SC, Catani M (2013) Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Hum Brain Mapp 34:2464–2483. https://​doi.​org/​10.​1002/​hbm.​22080 CrossRefPubMed
go back to reference Grant G (1982) Spinocerebellar connections in the cat with particular emphasis on their cellular origin. Exp Brain Res Suppl 6:466–476CrossRef Grant G (1982) Spinocerebellar connections in the cat with particular emphasis on their cellular origin. Exp Brain Res Suppl 6:466–476CrossRef
go back to reference Guell X, Schmahmann J, Gabrieli J, Ghosh S (2018b) Cerebellar organization is sensorimotor-fugal, and lobules VIII–IX/X share hierarchical principles. In: 24th Annual Meeting of the Organization for Huma Brain Mapping (Singapore) poster no 2722 Guell X, Schmahmann J, Gabrieli J, Ghosh S (2018b) Cerebellar organization is sensorimotor-fugal, and lobules VIII–IX/X share hierarchical principles. In: 24th Annual Meeting of the Organization for Huma Brain Mapping (Singapore) poster no 2722
go back to reference Holmes A, Friston K (1998) Generalisability, random effects and population inference. Neuroimage 7:S754CrossRef Holmes A, Friston K (1998) Generalisability, random effects and population inference. Neuroimage 7:S754CrossRef
go back to reference Leemans A, Jeurissen B, Sijbers J, Jones D ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. In: 17th Annual Meeting of the International Society of Magnetic Resonance in Medicine (2009) p 3537 Leemans A, Jeurissen B, Sijbers J, Jones D ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. In: 17th Annual Meeting of the International Society of Magnetic Resonance in Medicine (2009) p 3537
go back to reference Naito E, Morita T, Asada M (2016) Immature cerebro-cerebellar interaction for timing motor control in children. In: 22nd Annual Meeting of the Organization for Huma Brain Mapping (Geneva) poster no 2000 Naito E, Morita T, Asada M (2016) Immature cerebro-cerebellar interaction for timing motor control in children. In: 22nd Annual Meeting of the Organization for Huma Brain Mapping (Geneva) poster no 2000
go back to reference Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI Atlas of the Human Cerebellum. Academic Press, San Diego Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI Atlas of the Human Cerebellum. Academic Press, San Diego
go back to reference Wang R, Benner T, Sorensen AG, Wedeen VJ (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. In: Proceedings of the international society for magnetic resonance medicine (Berlin), vol 3720 Wang R, Benner T, Sorensen AG, Wedeen VJ (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. In: Proceedings of the international society for magnetic resonance medicine (Berlin), vol 3720
Metadata
Title
Local-to-distant development of the cerebrocerebellar sensorimotor network in the typically developing human brain: a functional and diffusion MRI study
Authors
Kaoru Amemiya
Tomoyo Morita
Daisuke N. Saito
Midori Ban
Koji Shimada
Yuko Okamoto
Hirotaka Kosaka
Hidehiko Okazawa
Minoru Asada
Eiichi Naito
Publication date
01-04-2019
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-01821-5

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