Spatiotemporal tissue maturation of thalamocortical pathways in the human fetal brain
Abstract
The development of connectivity between the thalamus and maturing cortex is a fundamental process in the second half of human gestation, establishing the neural circuits that are the basis for several important brain functions. In this study, we acquired high-resolution in utero diffusion MRI from 140 fetuses as part of the Developing Human Connectome Project, to examine the emergence of thalamocortical white matter over the second to third trimester. We delineate developing thalamocortical pathways and parcellate the fetal thalamus according to its cortical connectivity using diffusion tractography. We then quantify microstructural tissue components along the tracts in fetal compartments that are critical substrates for white matter maturation, such as the subplate and intermediate zone. We identify patterns of change in the diffusion metrics that reflect critical neurobiological transitions occurring in the second to third trimester, such as the disassembly of radial glial scaffolding and the lamination of the cortical plate. These maturational trajectories of MR signal in transient fetal compartments provide a normative reference to complement histological knowledge, facilitating future studies to establish how developmental disruptions in these regions contribute to pathophysiology.
Data availability
Developing Human Connectome project data is open-access and available for download following completion of a data-usage agreement via: http://www.developingconnectome.org/. Data will also be available at: https://nda.nih.gov/edit_collection.html?id=3955
Article and author information
Author details
Funding
European Research Council (Seventh Framework Programme: FP/2007/2013)
- Maximilian Pietsch
- Lucilio Cordero-Grande
- Daan Christiaens
- Vyacheslav R Karolis
- Vanessa Kyriakopoulou
- Anthony N Price
- Jana Hutter
- Emer J Hughes
- Jacques-Donald Tournier
- Joseph V Hajnal
- A David Edwards
Wellcome Trust (Sir Henry Dale Fellowship: 206675/Z/17/Z)
- Jonathan O'Muicheartaigh
Medical Research Council Centre for Neurodevelopmental Disorders (MR/N0266063/1)
- Sian Wilson
- Mary A Rutherford
- A David Edwards
- Jonathan O'Muicheartaigh
- Tomoki Arichi
Medical Research Council (Translation support fellowship: MR/V036874/1)
- Vyacheslav R Karolis
- Tomoki Arichi
Wellcome / EPSRC Centre for Biomedical Engineering, Kings College London (WT 203148/Z/16/Z)
- Anthony N Price
- Jana Hutter
- Jacques-Donald Tournier
- Joseph V Hajnal
Medical Research Council (Clinician Scientist Fellowship MR/P008712/1)
- Tomoki Arichi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Finnegan J Calabro, University of Pittsburgh, United States
Ethics
Human subjects: The study was approved by the UK Health Research Authority (Research Ethics Committee reference number: 14/LO/1169) and written parental consent was obtained in every case for imaging and open data release of the anonymized data.
Version history
- Received: September 26, 2022
- Preprint posted: October 25, 2022 (view preprint)
- Accepted: March 31, 2023
- Accepted Manuscript published: April 3, 2023 (version 1)
- Version of Record published: April 24, 2023 (version 2)
- Version of Record updated: May 26, 2023 (version 3)
Copyright
© 2023, Wilson et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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