Temporal and spatial regulation of chondroitin sulfate, radial glial cells, growing commissural axons, and other hippocampal efferents in developing hamsters

Abstract

We investigated the time and space relationship between growth of hippocampal efferents, particularly those forming the hippocampal commissure, and expression of extracellular matrix components related to radial glial cells. Developing hamster brains from embryonic day (E) 13 to postnatal day (P) 7 had 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) crystals implanted into the hippocampus or were processed for fluorescent immunohistochemistry against chondroitin sulfate (CS) glycosaminoglycans and glial fibrillary acidic protein (GFAP). The first, pioneer fibers from the hippocampus were seen crossing the midline at E15 and arriving at the contralateral hippocampus 24-48 hours later (P1), followed closely by a thick front of growing fibers. Before E15, CS expression was preceded by septal fusion and was concomitant with formation of the commissural tract. On E15, CS expression formed a U-shaped border below the fimbria. From E15 to P3, CS became expressed between the hippocampal commissure and the third ventricle and at the caudal borders of the fornix columns. As the hippocampal commissure expanded, CS expression became gradually lighter to virtually disappear by P7. On E15 and P1, GFAP-positive radial glial cells were present caudal (but not rostral) to the commissure at the midline, partially overlapping CS expression. Similar cells were present dorsal to the fimbria, extending their processes perpendicularly over the growing axons. The data reveal that CS and radial glial cells form a tunnel surrounding the developing fimbria and a border at the midline caudal to the hippocampal commissure. It is suggested that these cellular and molecular borders play a role in guidance of hippocampal efferents.

Cellular and molecular tunnels surrounding the forebrain commissures of human fetuses

“…Insofar as these cellular and molecular structures have also been observed in other mammals (Silver et al, 1982(Silver et al, , 1993Pires-Neto et al, 1998;Shu and Richards, 2001;Richards, 2002;Braga-de-Souza and Lent, 2004), and because they participate in the guidance of developing commissural and callosal axons across the midline (Silver et al, 1982;Shu and Richards, 2001), it is likely that they have the same role in human embryonic development as well. The ECM labeling for midline fiber tracts described here and in other studies (Hoffman-Kim et al, 1998;Shu and Richards, 2001;Braga-de-Souza and Lent, 2004) is not evident for fiber tracts that do not cross the midline, such as the internal capsule; therefore, it is likely that this pattern is specifically involved in the guidance of fiber bundles across the midline and that such guidance reflects a general strategy that is developed for commissural axons.…”

“…Axonal boundaries formed by extracellular glycoconjugates are transiently expressed in various developing areas of the CNS and are often associated with glial cells (Steindler, 1993;Garcia-Abreu et al, 1996a,b, 2000Wu et al, 1998;Pires-Neto et al, 1998;Braga-de-Souza and Lent, 2004), a phenomenon first observed in the roof plate of the spinal cord and of the optic tectum (Snow et al, 1990a). We report here that the expression of ECM molecules associated with glial cells is spatially and temporally related to the emergence of the major forebrain commissures in the developing human brain.…”

Postnatal Development of Entorhinodentate Projection of the <i>Reeler</i> Mutant Mouse

“…Such an accumulation of astroglial cells along the hippocampal fissure of reeler mice serves as a barrier which interferes with the penetration of the entorhinodentate axons crossing through the fissure. In addition, it is known that astroglial cells inhibit ingrowth of hippocampal afferents by production of chondroitin sulfate [Braga-de-Souza and Lent, 2004;Katoh-Semba et al, 1995;Pires-Neto et al, 1998]. Chondroitin sulfate overproduced by accumulated astroglial cells along the reeler hippocampal fissure may inhibit stabilization of perforant pathways in the mutant.…”

Wiring the Brain: The Biology of Neuronal Guidance

“…3). Molecules expressed by these glial populations include Slits (Erskine et al 2000;Plump et al 2002;Shu et al 2003c), Wnts (Keeble and Cooper 2006), Ephrins (Mendes et al 2006;Williams et al, 2003), Draxin ), and chondroitin sulphate proteoglycans (Braga-de-Souza and Lent 2004). The development of these glial populations is regulated by transcription factors such as Nfi genes (Shu et al 2003a;Steele-Perkins et al 2005;Barry et al 2008) and fibroblast growth factor signaling (Smith et al 2006).…”

“…Midline glial populations are associated with every commissural and decussating projection in the brain (Silver et al 1993). These glial populations are known as the "palisade" (optic chiasm) , "tunnels" (anterior commissure and fornix) (Pires-Neto et al 1998;Braga-de-Souza and Lent 2004;Lent et al 2005), "wedge" and "indusium griseum glia" (corpus callosum) (Shu and Richards 2001;Shu et al 2003b) (Fig. 3).…”