Development of axonal pathways in the human fetal fronto-limbic brain: Histochemical characterization and diffusion tensor imaging

Lana Vasung, Hao Huang, Nataša Jovanov-Milošević, Mihovil Pletikos, Susumu Mori, Ivica Kostović

Research output: Contribution to journalArticle

90 Citations (Scopus)

Abstract

The development of cortical axonal pathways in the human brain begins during the transition between the embryonic and fetal period, happens in a series of sequential events, and leads to the establishment of major long trajectories by the neonatal period. We have correlated histochemical markers (acetylcholinesterase (AChE) histochemistry, antibody against synaptic protein SNAP-25 (SNAP-25-immunoreactivity) and neurofilament 200) with the diffusion tensor imaging (DTI) database in order to make a reconstruction of the origin, growth pattern and termination of the pathways in the period between 8 and 34 postconceptual weeks (PCW). Histological sections revealed that the initial outgrowth and formation of joined trajectories of subcortico-frontal pathways (external capsule, cerebral stalk-internal capsule) and limbic bundles (fornix, stria terminalis, amygdaloid radiation) occur by 10 PCW. As early as 11 PCW, major afferent fibers invade the corticostriatal junction. At 13-14 PCW, axonal pathways from the thalamus and basal forebrain approach the deep moiety of the cortical plate, causing the first lamination. The period between 15 and 18 PCW is dominated by elaboration of the periventricular crossroads, sagittal strata and spread of fibers in the subplate and marginal zone. Tracing of fibers in the subplate with DTI is unsuccessful due to the isotropy of this zone. Penetration of the cortical plate occurs after 24-26 PCW. In conclusion, frontal axonal pathways form the periventricular crossroads, sagittal strata and 'waiting' compartments during the path-finding and penetration of the cortical plate. Histochemistry is advantageous in the demonstration of a growth pattern, whereas DTI is unique for demonstrating axonal trajectories. The complexity of fibers is the biological substrate of selective vulnerability of the fetal white matter.

Original languageEnglish (US)
Pages (from-to)400-417
Number of pages18
JournalJournal of Anatomy
Volume217
Issue number4
DOIs
StatePublished - Oct 2010

Fingerprint

Diffusion Tensor Imaging
Cerebral Cortex
trajectories
brain
image analysis
histochemistry
trajectory
Brain
Synaptosomal-Associated Protein 25
Internal Capsule
thalamus
penetration
Acetylcholinesterase
acetylcholinesterase
Growth
Thalamus
isotropy
lamination
Databases
Radiation

Keywords

  • Axonal pathways
  • Development
  • fronto-limbic connectivity
  • Human fetal brain
  • Subplate

ASJC Scopus subject areas

  • Anatomy
  • Histology
  • Developmental Biology
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Cell Biology

Cite this

Development of axonal pathways in the human fetal fronto-limbic brain : Histochemical characterization and diffusion tensor imaging. / Vasung, Lana; Huang, Hao; Jovanov-Milošević, Nataša; Pletikos, Mihovil; Mori, Susumu; Kostović, Ivica.

In: Journal of Anatomy, Vol. 217, No. 4, 10.2010, p. 400-417.

Research output: Contribution to journalArticle

Vasung, Lana ; Huang, Hao ; Jovanov-Milošević, Nataša ; Pletikos, Mihovil ; Mori, Susumu ; Kostović, Ivica. / Development of axonal pathways in the human fetal fronto-limbic brain : Histochemical characterization and diffusion tensor imaging. In: Journal of Anatomy. 2010 ; Vol. 217, No. 4. pp. 400-417.
@article{afe18281d0674424ad78c816955a159a,
title = "Development of axonal pathways in the human fetal fronto-limbic brain: Histochemical characterization and diffusion tensor imaging",
abstract = "The development of cortical axonal pathways in the human brain begins during the transition between the embryonic and fetal period, happens in a series of sequential events, and leads to the establishment of major long trajectories by the neonatal period. We have correlated histochemical markers (acetylcholinesterase (AChE) histochemistry, antibody against synaptic protein SNAP-25 (SNAP-25-immunoreactivity) and neurofilament 200) with the diffusion tensor imaging (DTI) database in order to make a reconstruction of the origin, growth pattern and termination of the pathways in the period between 8 and 34 postconceptual weeks (PCW). Histological sections revealed that the initial outgrowth and formation of joined trajectories of subcortico-frontal pathways (external capsule, cerebral stalk-internal capsule) and limbic bundles (fornix, stria terminalis, amygdaloid radiation) occur by 10 PCW. As early as 11 PCW, major afferent fibers invade the corticostriatal junction. At 13-14 PCW, axonal pathways from the thalamus and basal forebrain approach the deep moiety of the cortical plate, causing the first lamination. The period between 15 and 18 PCW is dominated by elaboration of the periventricular crossroads, sagittal strata and spread of fibers in the subplate and marginal zone. Tracing of fibers in the subplate with DTI is unsuccessful due to the isotropy of this zone. Penetration of the cortical plate occurs after 24-26 PCW. In conclusion, frontal axonal pathways form the periventricular crossroads, sagittal strata and 'waiting' compartments during the path-finding and penetration of the cortical plate. Histochemistry is advantageous in the demonstration of a growth pattern, whereas DTI is unique for demonstrating axonal trajectories. The complexity of fibers is the biological substrate of selective vulnerability of the fetal white matter.",
keywords = "Axonal pathways, Development, fronto-limbic connectivity, Human fetal brain, Subplate",
author = "Lana Vasung and Hao Huang and Nataša Jovanov-Milošević and Mihovil Pletikos and Susumu Mori and Ivica Kostović",
year = "2010",
month = "10",
doi = "10.1111/j.1469-7580.2010.01260.x",
language = "English (US)",
volume = "217",
pages = "400--417",
journal = "Journal of Anatomy",
issn = "0021-8782",
publisher = "Wiley-Blackwell",
number = "4",

}

TY - JOUR

T1 - Development of axonal pathways in the human fetal fronto-limbic brain

T2 - Histochemical characterization and diffusion tensor imaging

AU - Vasung, Lana

AU - Huang, Hao

AU - Jovanov-Milošević, Nataša

AU - Pletikos, Mihovil

AU - Mori, Susumu

AU - Kostović, Ivica

PY - 2010/10

Y1 - 2010/10

N2 - The development of cortical axonal pathways in the human brain begins during the transition between the embryonic and fetal period, happens in a series of sequential events, and leads to the establishment of major long trajectories by the neonatal period. We have correlated histochemical markers (acetylcholinesterase (AChE) histochemistry, antibody against synaptic protein SNAP-25 (SNAP-25-immunoreactivity) and neurofilament 200) with the diffusion tensor imaging (DTI) database in order to make a reconstruction of the origin, growth pattern and termination of the pathways in the period between 8 and 34 postconceptual weeks (PCW). Histological sections revealed that the initial outgrowth and formation of joined trajectories of subcortico-frontal pathways (external capsule, cerebral stalk-internal capsule) and limbic bundles (fornix, stria terminalis, amygdaloid radiation) occur by 10 PCW. As early as 11 PCW, major afferent fibers invade the corticostriatal junction. At 13-14 PCW, axonal pathways from the thalamus and basal forebrain approach the deep moiety of the cortical plate, causing the first lamination. The period between 15 and 18 PCW is dominated by elaboration of the periventricular crossroads, sagittal strata and spread of fibers in the subplate and marginal zone. Tracing of fibers in the subplate with DTI is unsuccessful due to the isotropy of this zone. Penetration of the cortical plate occurs after 24-26 PCW. In conclusion, frontal axonal pathways form the periventricular crossroads, sagittal strata and 'waiting' compartments during the path-finding and penetration of the cortical plate. Histochemistry is advantageous in the demonstration of a growth pattern, whereas DTI is unique for demonstrating axonal trajectories. The complexity of fibers is the biological substrate of selective vulnerability of the fetal white matter.

AB - The development of cortical axonal pathways in the human brain begins during the transition between the embryonic and fetal period, happens in a series of sequential events, and leads to the establishment of major long trajectories by the neonatal period. We have correlated histochemical markers (acetylcholinesterase (AChE) histochemistry, antibody against synaptic protein SNAP-25 (SNAP-25-immunoreactivity) and neurofilament 200) with the diffusion tensor imaging (DTI) database in order to make a reconstruction of the origin, growth pattern and termination of the pathways in the period between 8 and 34 postconceptual weeks (PCW). Histological sections revealed that the initial outgrowth and formation of joined trajectories of subcortico-frontal pathways (external capsule, cerebral stalk-internal capsule) and limbic bundles (fornix, stria terminalis, amygdaloid radiation) occur by 10 PCW. As early as 11 PCW, major afferent fibers invade the corticostriatal junction. At 13-14 PCW, axonal pathways from the thalamus and basal forebrain approach the deep moiety of the cortical plate, causing the first lamination. The period between 15 and 18 PCW is dominated by elaboration of the periventricular crossroads, sagittal strata and spread of fibers in the subplate and marginal zone. Tracing of fibers in the subplate with DTI is unsuccessful due to the isotropy of this zone. Penetration of the cortical plate occurs after 24-26 PCW. In conclusion, frontal axonal pathways form the periventricular crossroads, sagittal strata and 'waiting' compartments during the path-finding and penetration of the cortical plate. Histochemistry is advantageous in the demonstration of a growth pattern, whereas DTI is unique for demonstrating axonal trajectories. The complexity of fibers is the biological substrate of selective vulnerability of the fetal white matter.

KW - Axonal pathways

KW - Development

KW - fronto-limbic connectivity

KW - Human fetal brain

KW - Subplate

UR - http://www.scopus.com/inward/record.url?scp=77956466596&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77956466596&partnerID=8YFLogxK

U2 - 10.1111/j.1469-7580.2010.01260.x

DO - 10.1111/j.1469-7580.2010.01260.x

M3 - Article

C2 - 20609031

AN - SCOPUS:77956466596

VL - 217

SP - 400

EP - 417

JO - Journal of Anatomy

JF - Journal of Anatomy

SN - 0021-8782

IS - 4

ER -