Multifocal pattern of postnatal development of the macroglial framework of the rat fimbria

Abstract

The development of the rat fimbria over the first postnatal month is associated with an approximate doubling of the tract diameter, a large increase in the number of glial cells, and the transformation of the prenatal radial glial skeleton into the adult interfascicular glial rows of solitary astrocytes and contiguous myelinating oligodendrocytes. The ventricular zone is reduced from a heterogeneous germinal layer of three or more cells thick at birth to the mature adult unicellular ependyma of homogeneous pale, mitotically inactive cells by the end of the second postnatal week. Mitoses are present throughout the body of the tract at all times, and persist, at reduced levels, in the adult. At birth the interior of the fimbria has only few scattered glial cell nuclei, largely solitary, or at most in longitudinal pairs. Over the first two postnatal weeks, the numbers and density of the interfascicular glia increase continuously. The scattered cells and cell clusters become progressively transformed into longer unicellular rows, which are aligned along the longitudinal axis of the tract, and which finally coalesce to form the continuous regular astrocyte/oligodendrocyte units that make up the interfascicular glial rows of the adult fimbrial glial skeleton. The increased cell packing density of the developing fimbrial glia is associated with a substantial decrease in nuclear and cytoplasmic size. From the end of the second postnatal week, the characteristic, large pale solitary astrocytes, and the smaller, more numerous, densely stained, closely packed oligodendrocytes are recognisable. Immunostaining for glial fibrillary acidic protein shows that immediately after birth the characteristic embryonic pattern of regular parallel radial glial processes starts to be modified by the progressive accumulation of longitudinal astrocytic processes, so the prenatal radial glial framework is rapidly transformed into the adult type of rectilinear array of radial and longitudinal processes. The development of the oligodendrocytes is shown clearly by immunostaining for myelin basic protein in enlarged, cytoplasm-rich, symmetrically placed cell pairs first seen at around P7. At P8-P10, there is a characteristic pattern of simultaneous multifocal maturation in which a single oligodendrocyte in each cluster develops a full complement of parallel, rather varicose myelinating processes. By P14 myelination is becoming confluent, oligodendrocytes are smaller, darker, with little cytoplasm, and individual myelinating processes cannot be discerned. Even at the end of the first postnatal month there are still many immature glia of indeterminate morphology. Myelination tends at first to be concentrated in the region adjacent to the hippocampus, and only reaches completion by the end of the second month.(ABSTRACT TRUNCATED AT 400 WORDS)

Brevican in the developing hippocampal fimbria: Differential expression in myelinating oligodendrocytes and adult astrocytes suggests a dual role for brevican in central nervous system fiber tract development

“…4Ak). Such an increase in brevican-expressing cells correlates with the increase in oligodendrocytes during this period (Suzuki and Raisman, 1994). Then, at P21 (Fig.…”

“…As the fimbria develops, GFAPpositive astrocytes begin to appear in the interior of the fimbria. In the adult fimbria, large GFAP-positive astrocytes were observed as solitary cells interspersed within linear clusters of oligodendrocytes (Suzuki and Raisman, 1994). In P4 fimbria, where most of the GFAP immunoreactivities represent radial glial fibers, GFAP immunoreactivities did not coincide with brevican-expressing cells (Fig.…”

“…An IGR is composed of linear clusters of oligodendrocytes and occasional, solitary astrocytes interspersed singly between stretches of contiguous oligodendrocytes. This characteristic glial structure develops during the first 4 or 5 weeks after birth in rat fimbria, starting from small numbers of scattered glial cells and progressing to mature, densely packed glial rows (Suzuki and Raisman, 1994). The number of oligodendrocytes in an IGR increases from a few cells at P4 to more than 50 in the adult (Suzuki and Raisman, 1992).…”

“…To determine whether they are indeed astrocytes, we performed triple labeling of developing fimbria by in situ hybridization, GFAP-immunohistochemistry, and Hoechst 33342 staining of cell nuclei. Suzuki and Raisman (1994) reported that, in early postnatal fimbria (P0 -P4), GFAP-immunoreactive glial elements are predominantly glial fibers originating from radial glia residing in the ependymal layer, not from white matter astrocytes. As the fimbria develops, GFAPpositive astrocytes begin to appear in the interior of the fimbria.…”

Transient Inactivation of the Neonatal Ventral Hippocampus Permanently Disrupts the Mesolimbic Regulation of Prefrontal Cholinergic Transmission: Implications for Schizophrenia

“…The well-known manifestation of a SZ-like phenotype at the time of late puberty in these various hippocampal-based models (Alexander et al, 2009;Tseng et al, 2007) of the disorder may relate, in part, to the timing of this inappropriate pruning. Finally, TTX-induced changes in impulse flow may diminish myelination of hippocampal and other projection neurons, during the sensitive period around PD7, but not PD32 (Suzuki and Raisman, 1994;Zalc and Fields, 2000). It is possible that changes in the myelination of hippocampal projection neurons during periods of innervations in PFC may dysregulate cortical ACh release, uncouple the synchrony of neuronal oscillations, and, as a result, produce the cognitive deficits in seen SZ (Ford et al, 2007;Jones, 2010).…”