Prominent periventricular fiber system related to ganglionic eminence and striatum in the human fetal cerebrum

Abstract

Periventricular pathway (PVP) system of the developing human cerebrum is situated medial to the intermediate zone in the close proximity to proliferative cell compartments. In order to elucidate chemical properties and developing trajectories of the PVP we used DTI in combination with acetylcholinesterase histochemistry, SNAP-25 immunocytochemistry and axonal cytoskeletal markers (SMI312, MAP1b) immunocytochemistry on postmortem paraformaldehyde-fixed brains of 30 human fetuses ranging in age from 10 to 38 postconceptional weeks (PCW), 2 infants (age 1-3 months) and 1 adult brain. The PVP appears in the early fetal period (10-13 PCW) as two defined fibre bundles: the corpus callosum (CC) and the fetal fronto-occipital fascicle (FOF). In the midfetal period (15-18 PCW), all four components of the PVP can be identified: (1) the CC, which at rostral levels forms a voluminous callosal plate; (2) the FOF, with SNAP-25-positive fibers; (3) the fronto-pontine pathway (FPP) which for a short distance runs within the PVP; and (4) the subcallosal fascicle of Muratoff (SFM) which contains cortico-caudate projections. The PVPs are situated medial to the internal capsule at the level of the cortico-striatal junction; they remain prominent during the late fetal and early preterm period (19-28 PCW) and represent a portion of the wider periventricular crossroad of growing associative, callosal and projection pathways. In the perinatal period, the PVPs change their topographical relationships, decrease in size and the FOF looses its SNAP-25-reactivity. In conclusion, the hitherto undescribed PVP of the human fetal cerebrum contains forerunners of adult associative and projection pathways. Its transient chemical properties and relative exuberance suggest that the PVP may exert influence on the development of cortical connectivity (intermediate targeting) and other neurogenetic events such as neuronal proliferation. The PVP's topographical position also indicates that it is a major site of vulnerability in hypoxic-ischaemic perinatal brain injury.

Spatiotemporal Relationship of Brain Pathways during Human Fetal Development Using High-Angular Resolution Diffusion MR Imaging and Histology

“…We have found that corticofugal projection pathways show deeper (closer to the ventricles) positioning (e.g., subcallosal fasciculus and corticopontine pathways were situated in the periventricular fiber rich zone, at the level of corticostriatal junction) compared to corticopetal thalamocortical fibers, which run more superficially (toward pia; Figure 1F). This finding is in agreement with previous studies (Vasung et al, 2011). …”

“…Our results are in agreement with our previous findings (Vasung et al, 2011), showing that the periventricular frontooccipital fasciculus (FOF) develops early in life (Figure 1B). In contrast, other, more laterally situated, long association pathways form a part of the centrum semiovale during the mid fetal period, and develop pronanunced trajectory much later (Huang et al, 2006; Kasprian et al, 2008; Song et al, 2015).…”

Spatiotemporal Relationship of Brain Pathways during Human Fetal Development Using High-Angular Resolution Diffusion MR Imaging and Histology

“…We have found that corticofugal projection pathways show deeper (closer to the ventricles) positioning (e.g., subcallosal fasciculus and corticopontine pathways were situated in the periventricular fiber rich zone, at the level of corticostriatal junction) compared to corticopetal thalamocortical fibers, which run more superficially (toward pia; Figure 1F). This finding is in agreement with previous studies (Vasung et al, 2011). …”

“…Our results are in agreement with our previous findings (Vasung et al, 2011), showing that the periventricular frontooccipital fasciculus (FOF) develops early in life (Figure 1B). In contrast, other, more laterally situated, long association pathways form a part of the centrum semiovale during the mid fetal period, and develop pronanunced trajectory much later (Huang et al, 2006; Kasprian et al, 2008; Song et al, 2015).…”

In Vivo Tractography of Fetal Association Fibers

“…The general appearance of the fornix as visualized by in utero tractography corresponds to the results of postmortem fetal tractography studies [ 29 – 33 ]. Both in utero and postmortem tractography are able to visualize crus, corpus and columns of the fornix as a compact c-shaped fiber bundle.…”

Developmental Dynamics of Radial Vulnerability in the Cerebral Compartments in Preterm Infants and Neonates

“…We found that both focal and diffused lesions, depending on their radial extent, affect well identified and spatially segregated classes of axons: periventricular pathways of mixed modalities within ventricular/subventricular zone (65), major projection pathways within the crossroads (11, 54) and sagittal strata (18, 54, 75, 81), associative pathways within the centrum semiovale and deep cortical subplate and thalamocorticals in the subplate of early preterms. Moreover, characteristic spatial arrangement of these axonal pathways shows time-related sequential growth, with some overlap during 22–36 PCW.…”

Spatiotemporal Relationship of Brain Pathways during Human Fetal Development Using High-Angular Resolution Diffusion MR Imaging and Histology

“…We have found that corticofugal projection pathways show deeper (closer to the ventricles) positioning (e.g., subcallosal fasciculus and corticopontine pathways were situated in the periventricular fiber rich zone, at the level of corticostriatal junction) compared to corticopetal thalamocortical fibers, which run more superficially (toward pia; Figure 1F). This finding is in agreement with previous studies (Vasung et al, 2011). …”

“…Our results are in agreement with our previous findings (Vasung et al, 2011), showing that the periventricular frontooccipital fasciculus (FOF) develops early in life (Figure 1B). In contrast, other, more laterally situated, long association pathways form a part of the centrum semiovale during the mid fetal period, and develop pronanunced trajectory much later (Huang et al, 2006; Kasprian et al, 2008; Song et al, 2015).…”

In Vivo Tractography of Fetal Association Fibers

“…The general appearance of the fornix as visualized by in utero tractography corresponds to the results of postmortem fetal tractography studies [ 29 – 33 ]. Both in utero and postmortem tractography are able to visualize crus, corpus and columns of the fornix as a compact c-shaped fiber bundle.…”

Developmental Dynamics of Radial Vulnerability in the Cerebral Compartments in Preterm Infants and Neonates

“…We found that both focal and diffused lesions, depending on their radial extent, affect well identified and spatially segregated classes of axons: periventricular pathways of mixed modalities within ventricular/subventricular zone (65), major projection pathways within the crossroads (11, 54) and sagittal strata (18, 54, 75, 81), associative pathways within the centrum semiovale and deep cortical subplate and thalamocorticals in the subplate of early preterms. Moreover, characteristic spatial arrangement of these axonal pathways shows time-related sequential growth, with some overlap during 22–36 PCW.…”

Spatiotemporal Relationship of Brain Pathways during Human Fetal Development Using High-Angular Resolution Diffusion MR Imaging and Histology

“…We have found that corticofugal projection pathways show deeper (closer to the ventricles) positioning (e.g., subcallosal fasciculus and corticopontine pathways were situated in the periventricular fiber rich zone, at the level of corticostriatal junction) compared to corticopetal thalamocortical fibers, which run more superficially (toward pia; Figure 1F). This finding is in agreement with previous studies (Vasung et al, 2011). …”

“…Our results are in agreement with our previous findings (Vasung et al, 2011), showing that the periventricular frontooccipital fasciculus (FOF) develops early in life (Figure 1B). In contrast, other, more laterally situated, long association pathways form a part of the centrum semiovale during the mid fetal period, and develop pronanunced trajectory much later (Huang et al, 2006; Kasprian et al, 2008; Song et al, 2015).…”

In Vivo Tractography of Fetal Association Fibers

“…The general appearance of the fornix as visualized by in utero tractography corresponds to the results of postmortem fetal tractography studies [ 29 – 33 ]. Both in utero and postmortem tractography are able to visualize crus, corpus and columns of the fornix as a compact c-shaped fiber bundle.…”

Developmental Dynamics of Radial Vulnerability in the Cerebral Compartments in Preterm Infants and Neonates

“…We found that both focal and diffused lesions, depending on their radial extent, affect well identified and spatially segregated classes of axons: periventricular pathways of mixed modalities within ventricular/subventricular zone (65), major projection pathways within the crossroads (11, 54) and sagittal strata (18, 54, 75, 81), associative pathways within the centrum semiovale and deep cortical subplate and thalamocorticals in the subplate of early preterms. Moreover, characteristic spatial arrangement of these axonal pathways shows time-related sequential growth, with some overlap during 22–36 PCW.…”