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Published on: April 3, 2013
Axonal development in the cerebral white matter of the human fetus and infant
Robin L Haynes1, Natalia S Borenstein, Tara M Desilva
1Department of Pathology, Children's Hospital Boston and Harvard Medical School, Boston, Massachusetts 02115, USA. robin.haynes@childrens.harvard.edu
Insights
This study details human parietal white matter axonal development from 20-183 postconceptional weeks. Immature axons are vulnerable to damage during this critical growth period, impacting conditions like cerebral palsy.
Area of Science:
- Neuroscience
- Developmental Biology
- Pathology
Background:
- Axonal elongation is crucial for forming neural circuits after neuronal migration.
- The human parietal white matter undergoes significant axonal development from midgestation through infancy.
- Understanding this period is vital for comprehending neurodevelopmental disorders.
Purpose of the Study:
- To characterize axonal development in the human parietal white matter during a critical growth period (20-183 postconceptional weeks).
- To investigate the expression patterns of key axonal markers and myelination.
- To provide insights into the vulnerability of developing axons to injury, particularly in relation to periventricular leukomalacia.
Main Methods:
- Immunocytochemistry and Western blot analysis were used.
- Normative cases spanning 20-183 postconceptional weeks were examined.
- Specific markers for neurofilaments (SMI 312, SMI 32, SMI 31), axonal growth (GAP-43), and myelination (myelin basic protein) were assessed.
Main Results:
- Neurofilament staining (SMI 312) was observed as early as 23 weeks.
- Axonal maturity markers (phosphorylated NFH, SMI 31) showed low levels until 34 weeks.
- High expression of axonal growth marker (GAP-43) persisted until 64 weeks, with myelination onset around 54 weeks.
- Adult-like myelination was achieved by 72-92 weeks.
Conclusions:
- This study provides a detailed timeline of axonal maturation in the human parietal white matter during a previously understudied critical period.
- Immature axons during this period are susceptible to damage, as seen in periventricular leukomalacia, a major cause of cerebral palsy.
- The timing of axonal maturation is a key factor in understanding the pathology of white matter injury and its long-term consequences.
Abstract:
After completion of neuronal migration to form the cerebral cortex, axons undergo rapid elongation to their intra- and subcortical targets, from midgestation through infancy. We define axonal development in the human parietal white matter in this critical period. Immunocytochemistry and Western blot analysis were performed on 46 normative cases from 20-183 postconceptional (PC) weeks. Anti-SMI 312, a pan-marker of neurofilaments, stained axons as early as 23 weeks. Anti-SMI 32, a marker for nonphosphorylated neurofilament high molecular weight (NFH), primarily stained neuronal cell bodies (cortical, subcortical, and Cajal-Retzius). Anti-SMI 31, which stains phosphorylated NFH, was used as a marker of axonal maturity, and showed relatively low levels of staining (approximately one-fourth of adult levels) from 24-34 PC weeks. GAP-43, a marker of axonal growth and elongation, showed high levels of expression in the white matter from 21-64 PC weeks and lower, adult-like levels beyond 17 postnatal months. The onset of myelination, as seen by myelin basic protein expression, was approximately 54 weeks, with progression to "adult-like" staining by 72-92 PC weeks. This study provides major insight into axonal maturation during a critical period of growth, over an age range not previously examined and one coinciding with the peak period of periventricular leukomalacia (PVL), the major disorder underlying cerebral palsy in premature infants. These data suggest that immature axons are susceptible to damage in PVL and that the timing of axonal maturation must be considered toward establishing its pathology relative to the oligodendrocyte/myelin/axonal unit.
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