Elsevier

Brain Research Bulletin

Volume 54, Issue 3, February 2001, Pages 255-266
Brain Research Bulletin

Maturation of white matter in the human brain: a review of magnetic resonance studies

https://doi.org/10.1016/S0361-9230(00)00434-2Get rights and content

Abstract

This review focuses on the maturation of brain white-matter, as revealed by magnetic resonance (MR) imaging carried out in healthy subjects. The review begins with a brief description of the nature of the MR signal and its possible biological underpinnings, and proceeds with a description of MR findings obtained in newborns, infants, children and adolescents. On MR images, a significant decrease in water content leads to a decrease of longitudinal relaxation times (T1) and transverse relaxation times (T2) and consequent “adult-like” appearance of T1-weighted and T2-weighted images becomes evident towards the end of the first year of life. Owing to the onset of myelination and the related increase of lipid content, MR images gradually acquire an exquisite grey-white matter contrast in a temporal sequence reflecting the time course of myelination. Albeit less pronounced, age-related changes in white matter continue during childhood and adolescence; white matter increases its overall volume and becomes more myelinated in a region-specific fashion. Detection of more subtle changes during this “late” phase of brain development is greatly aided by computational analyses of MR images. The review also briefly outlines future directions, including the use of novel MR techniques such as diffusion tensor imaging and magnetization transfer, as well as the suggestion for the concurrent use of experimental behavioral test-batteries, with structural MR imaging, to study developmental changes in structure-function relationships.

Introduction

The non-invasive nature of magnetic resonance imaging (MRI) has opened unique opportunities for in vivo investigation of the developing human brain. In the past decade, significant progress has been made in delineating changes in brain morphology, including those in grey and white matter, from birth to adolescence. In this review, we focus on MRI findings, obtained in healthy subjects, pertinent to the maturation of brain white matter. This emphasis is motivated by the interest in studies of functional inter-regional interactions, or functional connectivity, in the adult and developing human brain. In the adult, functional interactions are studied with a variety of tools, including positron emission tomography 27, 53, 65, functional MRI 9, 28, electroencephalography (EEG) [31], and with the combination of transcranial magnetic stimulation (TMS) and brain imaging (reviewed in [63]).

In the child, studies of functional interactions are in their infancy. With the exception of age-related changes in EEG coherence (e.g., [81]) and in TMS-derived cortico-spinal 25, 56, 61 and transcallosal 37, 74 conduction times, very little is known about inter-regional communication in the developing human brain. Because the smooth flow of information depends, to a great extent, on the structural properties of connecting pathways, MRI investigations of anatomic maturation in major fiber tracts provide information essential for the understanding of functional interactions in the developing human brain.

Age-related changes in MR signals reflect the effects of a variety of biological factors. To facilitate the interpretation of the MR findings, we begin this review with a description of the nature of the MR signal and its possible biological underpinnings. We proceed with reviewing MR findings obtained in newborns and infants, followed by a review of MR findings obtained in children and adolescents. Finally future directions are outlined, including the use of diffusion tensor imaging to reveal major fiber tracts and the concurrent use of experimental behavioral test-batteries and structural MRI to study developmental changes in structure-function relationships.

Section snippets

Principles of MRI

Nuclei that have an odd number of nucleons (protons and neutrons) possess both a magnetic moment and angular momentum (or spin). In the presence of an external magnetic field such nuclei precess (or wobble) around their axis at a rate proportional to the strength of the magnetic field, emitting electromagnetic energy in the process. The hydrogen atom contains only a single proton, and therefore precesses when exposed to a magnetic field. In the majority of MR imaging studies, precessing nuclei

MRI in newborns and infants (0–4 years)

The majority of early MR studies provide qualitative descriptions of T1- and/or T2-weighted images, focusing on the grey-white matter contrast and degree of myelination 3, 4, 7, 14, 23, 36, 47, 51, 52, 84. In most studies, the scans were acquired for clinical reasons and later screened to include only subjects without neurological (or MR) abnormalities; the number of subjects varied from 34 to 120. In several studies, MRIs of premature (29 to 37 post-conception weeks) newborns were also

MRI in children and adolescents (5–18 years)

Brain weight reaches adult values (about 1.45 kg) between 10 and 12 years of age. The fastest growth occurs during the first 3 years of life so that by the age of 5 years the infant’s brain weighs about 90% of the adult value [19]. Clearly, changes in brain morphology in childhood and adolescence are more subtle that those in the first 4 years of life. Qualitative evaluation of MR images is of little value at this point and the ability to obtain quantitative measurements is of the essence if we

Future directions

Computational analysis of MR images clearly enhances our ability to detect subtle age-related changes in white matter, as measured with conventional T1- and T2-weighted imaging. The use of such techniques to analyse large and, preferably, longitudinal datasets will undoubtedly reveal new details about maturation of the human brain. It is also likely that, in the near future, our knowledge will be further expanded by measuring more directly distinct properties of white matter, such as those

Acknowledgements

This work was supported in part by the International Consortium for Brain Mapping and Canadian Institutes of Health Research. We thank Drs. Dauphne Maurer and Kate Watkins for their help with the selection of experimental tests included in Tables1 and 2, and Drs. Jay Giedd and Judith Rapoport for the fruitful collaboration on MR studies of brain development.

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