Hierarchical complexity of the macro-scale neonatal brain

Blesa, Manuel and Galdi, Paola and Cox, Simon R. and Sullivan, Gemma and Stoye, David Q. and Lamb, Gillian J. and Quigley, Alan J. and Thrippleton, Michael J. and Escudero, Javier and Bastin, Mark E. and Smith, Keith M. and Boardman, James P. (2021) Hierarchical complexity of the macro-scale neonatal brain. Cerebral Cortex, 31 (4). pp. 2071-2084. ISSN 1047-3211 (https://doi.org/10.1093/cercor/bhaa345)

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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.