Early Life Brain Network Connectivity Antecedents of Executive Function in Children Born Preterm

Overview

Journal Commun Biol

Specialty Biology

Date 2025 Mar 2

PMID 40025105

Authors

Abiot Y Derbie

Mekibib Altaye

Junqi Wang

Armin Allahverdy

Lili He

Leanne Tamm

Nehal A Parikh

Affiliations

Soon will be listed here.

Abstract

Preterm birth is associated with an increased risk of executive function (EF) deficits, yet the underlying neural mechanisms remain unclear. We combine diffusion MRI, resting-state functional MRI, and graph theory analyses to examine how structural (SC) and functional connectivity (FC) at term-equivalent age (TEA) influence EF outcomes at 3 years corrected age in children born at or below 32 weeks' gestation. Here we show shorter average path length (a measure of efficient structural communication) in the insula is linked to better EF performance, implying that more direct structural pathways in this region facilitate critical cognitive processes. Additionally, higher betweenness centrality (a node-level metric of information flow) in parietal and superior temporal regions is associated with improved EF, reflecting these areas' prominent integrative roles in the whole-brain functional network. Importantly, our multimodal analyses reveal that regional structural efficiency helps shape functional organization, indicating a specific interplay between white-matter architecture and emergent functional hubs at TEA. These findings extend current knowledge by demonstrating how earlier disruptions in SC can alter subsequent FC patterns that support EF. By focusing on precise node-level metrics rather than broad within-network effects, our results clarify the contribution that SC has in guiding functional relationships essential for EF.

References

Kline J, Priyanka Illapani V, Li H, He L, Yuan W, Parikh N . Diffuse white matter abnormality in very preterm infants at term reflects reduced brain network efficiency. Neuroimage Clin. 2021; 31:102739. PMC: 8378797. DOI: 10.1016/j.nicl.2021.102739. View

DOria V, Beckmann C, Arichi T, Merchant N, Groppo M, Turkheimer F . Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci U S A. 2010; 107(46):20015-20. PMC: 2993415. DOI: 10.1073/pnas.1007921107. View

Whitfield-Gabrieli S, Nieto-Castanon A . Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012; 2(3):125-41. DOI: 10.1089/brain.2012.0073. View

Jenkinson M, Bannister P, Brady M, Smith S . Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002; 17(2):825-41. DOI: 10.1016/s1053-8119(02)91132-8. View

Bullmore E, Sporns O . The economy of brain network organization. Nat Rev Neurosci. 2012; 13(5):336-49. DOI: 10.1038/nrn3214. View

Fitzgibbon S, Harrison S, Jenkinson M, Baxter L, Robinson E, Bastiani M . The developing Human Connectome Project (dHCP) automated resting-state functional processing framework for newborn infants. Neuroimage. 2020; 223:117303. PMC: 7762845. DOI: 10.1016/j.neuroimage.2020.117303. View

Honey C, Sporns O, Cammoun L, Gigandet X, Thiran J, Meuli R . Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci U S A. 2009; 106(6):2035-40. PMC: 2634800. DOI: 10.1073/pnas.0811168106. View

Schmitz-Koep B, Haller B, Coupe P, Menegaux A, Gaser C, Zimmer C . Grey and White Matter Volume Changes after Preterm Birth: A Meta-Analytic Approach. J Pers Med. 2021; 11(9). PMC: 8468941. DOI: 10.3390/jpm11090868. View

Kelly C, Thompson D, Chen J, Josev E, Pascoe L, Spencer-Smith M . Working memory training and brain structure and function in extremely preterm or extremely low birth weight children. Hum Brain Mapp. 2019; 41(3):684-696. PMC: 6977425. DOI: 10.1002/hbm.24832. View

10.

Volpe J . Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2008; 8(1):110-24. PMC: 2707149. DOI: 10.1016/S1474-4422(08)70294-1. View

11.

Parikh N, Sharma P, He L, Li H, Altaye M, Priyanka Illapani V . Perinatal Risk and Protective Factors in the Development of Diffuse White Matter Abnormality on Term-Equivalent Age Magnetic Resonance Imaging in Infants Born Very Preterm. J Pediatr. 2020; 233:58-65.e3. PMC: 8290900. DOI: 10.1016/j.jpeds.2020.11.058. View

12.

Shine J, Hearne L, Breakspear M, Hwang K, Muller E, Sporns O . The Low-Dimensional Neural Architecture of Cognitive Complexity Is Related to Activity in Medial Thalamic Nuclei. Neuron. 2019; 104(5):849-855.e3. DOI: 10.1016/j.neuron.2019.09.002. View

13.

Bjuland K, Lohaugen G, Martinussen M, Skranes J . Cortical thickness and cognition in very-low-birth-weight late teenagers. Early Hum Dev. 2013; 89(6):371-80. DOI: 10.1016/j.earlhumdev.2012.12.003. View

14.

Brunet J, Tamayo P, Golub T, Mesirov J . Metagenes and molecular pattern discovery using matrix factorization. Proc Natl Acad Sci U S A. 2004; 101(12):4164-9. PMC: 384712. DOI: 10.1073/pnas.0308531101. View

15.

Barnes-Davis M, Williamson B, Merhar S, Holland S, Kadis D . Rewiring the extremely preterm brain: Altered structural connectivity relates to language function. Neuroimage Clin. 2020; 25:102194. PMC: 7005506. DOI: 10.1016/j.nicl.2020.102194. View

16.

Corbetta M, Shulman G . Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002; 3(3):201-15. DOI: 10.1038/nrn755. View

17.

Burzynska A, Garrett D, Preuschhof C, Nagel I, Li S, Backman L . A scaffold for efficiency in the human brain. J Neurosci. 2013; 33(43):17150-9. PMC: 6618437. DOI: 10.1523/JNEUROSCI.1426-13.2013. View

18.

Kline J, Priyanka Illapani V, He L, Altaye M, Logan J, Parikh N . Early cortical maturation predicts neurodevelopment in very preterm infants. Arch Dis Child Fetal Neonatal Ed. 2019; 105(5):460-465. PMC: 7205568. DOI: 10.1136/archdischild-2019-317466. View

19.

Medaglia J, Lynall M, Bassett D . Cognitive network neuroscience. J Cogn Neurosci. 2015; 27(8):1471-91. PMC: 4854276. DOI: 10.1162/jocn_a_00810. View

20.

Beck D, Schaefer C, Pang K, Carlson S . Executive Function in Preschool Children: Test-Retest Reliability. J Cogn Dev. 2011; 12(2):169-193. PMC: 3105625. DOI: 10.1080/15248372.2011.563485. View