Hierarchical complexity of the macro-scale neonatal brain

Manuel Blesa; Paola Galdi; Simon R. Cox; Gemma Sullivan; David Q. Stoye; Gillian J. Lamb; Alan J. Quigley; Michael J. Thrippleton; Javier Escudero; Mark E. Bastin; Keith M. Smith; James P. Boardman

doi:10.1093/cercor/bhaa345

Hierarchical complexity of the macro-scale neonatal brain

Manuel Blesa^*, Paola Galdi, Simon R. Cox, Gemma Sullivan, David Q. Stoye, Gillian J. Lamb, Alan J. Quigley, Michael J. Thrippleton, Javier Escudero, Mark E. Bastin, Keith M. Smith, James P. Boardman

^*Corresponding author for this work

Computer And Information Sciences

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Abstract

The human adult structural connectome has a rich nodal hierarchy, with highly diverse connectivity patterns aligned to the diverse range of functional specializations in the brain. The emergence of this hierarchical complexity in human development is unknown. Here, we substantiate the hierarchical tiers and hierarchical complexity of brain networks in the newborn period, assess correspondences with hierarchical complexity in adulthood, and investigate the effect of preterm birth, a leading cause of atypical brain development and later neurocognitive impairment, on hierarchical complexity. We report that neonatal and adult structural connectomes are both composed of distinct hierarchical tiers and that hierarchical complexity is greater in term born neonates than in preterms. This is due to diversity of connectivity patterns of regions within the intermediate tiers, which consist of regions that underlie sensorimotor processing and its integration with cognitive information. For neonates and adults, the highest tier (hub regions) is ordered, rather than complex, with more homogeneous connectivity patterns in structural hubs. This suggests that the brain develops first a more rigid structure in hub regions allowing for the development of greater and more diverse functional specialization in lower level regions, while connectivity underpinning this diversity is dysmature in infants born preterm.

Original language	English
Pages (from-to)	2071-2084
Number of pages	14
Journal	Cerebral Cortex
Volume	31
Issue number	4
Early online date	7 Dec 2020
DOIs	https://doi.org/10.1093/cercor/bhaa345
Publication status	Published - 1 Apr 2021

Funding

Theirworld (www.theirworld.org); Health Data Research UK (Medical Research Council (MRC) ref Mr/S004122/1), which is funded by the UK Medical Research Council, Engineering and Physical Sciences Research Council, Economic and Social Research Council, National Institute for Health Research (England), Chief Scientist Office of the Scottish Government Health and Social Care Directorates, Health and Social Care Research and Development Division (Welsh Government), Public Health Agency (Northern Ireland), British Heart Foundation, and Wellcome; National Health Service (NHS) Lothian Research and Development Office (to M.J.T.); Part of the work was undertaken in the Medical Research Council (MRC) Centre for Reproductive Health, which is funded by MRC Centre Grant (MRC G1002033); MRC (MR/R024065/1 to S.R.C.); and National Institutes of Health (R01AG054628 to S.R.C.).

Keywords

developing brain
dMRI
hierarchical complexity
network analysis
newborn
structural connectome

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10.1093/cercor/bhaa345Licence: CC BY 4.0

Blesa-etal-CC-2020-Hierarchical-complexity-of-the-macro-scale-neonatal-brainFinal published version, 1.82 MBLicence: CC BY 4.0

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title = "Hierarchical complexity of the macro-scale neonatal brain",

abstract = "The human adult structural connectome has a rich nodal hierarchy, with highly diverse connectivity patterns aligned to the diverse range of functional specializations in the brain. The emergence of this hierarchical complexity in human development is unknown. Here, we substantiate the hierarchical tiers and hierarchical complexity of brain networks in the newborn period, assess correspondences with hierarchical complexity in adulthood, and investigate the effect of preterm birth, a leading cause of atypical brain development and later neurocognitive impairment, on hierarchical complexity. We report that neonatal and adult structural connectomes are both composed of distinct hierarchical tiers and that hierarchical complexity is greater in term born neonates than in preterms. This is due to diversity of connectivity patterns of regions within the intermediate tiers, which consist of regions that underlie sensorimotor processing and its integration with cognitive information. For neonates and adults, the highest tier (hub regions) is ordered, rather than complex, with more homogeneous connectivity patterns in structural hubs. This suggests that the brain develops first a more rigid structure in hub regions allowing for the development of greater and more diverse functional specialization in lower level regions, while connectivity underpinning this diversity is dysmature in infants born preterm.",

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AU - Lamb, Gillian J.

AU - Quigley, Alan J.

AU - Thrippleton, Michael J.

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AB - The human adult structural connectome has a rich nodal hierarchy, with highly diverse connectivity patterns aligned to the diverse range of functional specializations in the brain. The emergence of this hierarchical complexity in human development is unknown. Here, we substantiate the hierarchical tiers and hierarchical complexity of brain networks in the newborn period, assess correspondences with hierarchical complexity in adulthood, and investigate the effect of preterm birth, a leading cause of atypical brain development and later neurocognitive impairment, on hierarchical complexity. We report that neonatal and adult structural connectomes are both composed of distinct hierarchical tiers and that hierarchical complexity is greater in term born neonates than in preterms. This is due to diversity of connectivity patterns of regions within the intermediate tiers, which consist of regions that underlie sensorimotor processing and its integration with cognitive information. For neonates and adults, the highest tier (hub regions) is ordered, rather than complex, with more homogeneous connectivity patterns in structural hubs. This suggests that the brain develops first a more rigid structure in hub regions allowing for the development of greater and more diverse functional specialization in lower level regions, while connectivity underpinning this diversity is dysmature in infants born preterm.

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KW - structural connectome

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Hierarchical complexity of the macro-scale neonatal brain

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