Glial cells develop a laminar pattern before neuronal cells in the lateral geniculate nucleus.

Abstract

The lateral geniculate nucleus, which lies between the retina and the striate cortex in the visual pathway of mammals, is often made up of several distinctive cell layers, or laminae. We have used immunohistochemical methods to localize two glial cell intermediate filament proteins, glial fibrillary acidic protein and vimentin, and have found that layering of glial cells is evident before neuronal cell layers develop in the lateral geniculate nucleus. The correlation between glial cell lamination and neuronal lamination is consistent with the suggestion that glia are guiding neurons not only during the early postmitotic migratory phase of development but also during the later formation of functional divisions such as layers and nuclei.For some time now, we have been interested in the mechanisms that result in the presence of distinctive cell layers in the lateral geniculate nucleus (LGN), the major thalamic target of retinal fibers in mammals (1-4). One aspect of these studies has been to examine correlations between the various events involved in lamination in the LGN of the tree shrew (Tupaia belangeri), one of the few species in which LGN cell layers develop postnatally (1-4).Lamination is generally defined as areas packed with neuronal somata that alternate with relatively cell-free interlaminar zones. However, this describes only one of at least three types of lamination in the LGN. Each type has a distinct time course and may involve a distinct mechanism (1-4). Retinal terminals innervating the LGN are found in layers at birth in tree shrews (1-4) and probably begin and end their segregation process during the last 2 weeks of embryonic development (V.A.C. and G. J. Condo, unpublished data).[Gestation in the tree shrew is 43 days. We have designated the day of birth as postnatal day zero (P0); therefore, embryonic day 43 is equivalent to P0.] This afferent lamination is contrasted with cytoarchitectonic lamination, the differential packing density of cells (i.e., into cellular and cell-free zones). The latter process occurs during postnatal week 1 in tree shrews (1-4). Finally, the LGN exhibits cytological lamination-differences in the size and shape of cell bodies. In the tree shrew LGN, this process occurs during postnatal weeks 2 and 3 (1-4).At present, it is unclear what mechanisms are involved in the development of cell layers. A role for glial cell involvement in the development of more elaborate cytoarchitectonic arrangements of neurons is suggested by recent studies (5, 6) that show arrangements of glia during early development of the barrel fields of rodent somatosensory cortex and of the neostriatum that are strikingly similar to neuronal patterns present in the adult. A specific interaction ofglia and neurons in vitro, involving ultrastructural specializations, has been demonstrated (7,8). Similar specific neuronal-glial interactions may operate in vivo as well.The present paper reports evidence that glial cells are distributed in layers just before neurons show a cytoarchitectonically de...

Synthesis and release of neuroactive substances by glial cells

“…During migration the glia appear to serve merely as guides for neuronal movement, but the already established scaffold of radial glia determines the subsequent destination of the neurons. In the lateral geniculate nucleus, this initial neuronal migration is followed by the development of astrocytic laminae and then by the organization of the neurons into their characteristic laminar pattern (Hutchins and Casagrande, 1988 glia undoubtedly must engage in complex molecular interactions during these processes. In cell culture, serine proteases appear to be involved in neuronal migration (Krysotek and Seeds, 1981a,b;Moonen et al, 1982), and glial-derived protease inhibitors, such as the nexins, suppress migration and induce neurite outgrowth (Gloor et al, 1986;Gurwitz and Cunningham, 1988;Wagner et al, 1991).…”

Cellular localization of PDGF mRNAs in developing human forebrain

“…The developing vertebrate CNS is thought to use a glial cell scaffold upon which to form the neuronal networks characteristic of the adult nervous system [ 20]. Examples include the cell layers of the lateral geniculate nucleus [ 11, 12] and the barrel fields of somatosensory cortex [ 5]. Protooncogene expression, including that of sis/PDGF‐B, has been shown to reveal a transient columnar organization of the mouse forebrain within the late embryonic ventricular zone, which is immunoreactive for the glial cell intermediate filament protein vimentin [ 16].…”

“…The precise formation of this glial scaffold is achieved by accurate innervation of the target cells. In the barrel fields of somatosensory cortex and the cell layers of the lateral geniculate nucleus, the appearance of glial markers coincides with the afferent pattern of innervation suggesting a chemotactic function [ 5, 11, 12]. Similarly, glial cells of the floor and roof plates of developing spinal cord and tectum have been proposed to guide the growth of these neuronal afferents [ 3, 24, 25, 27].…”

argos is required for projection of photoreceptor axons during optic lobe development in Drosophila

“…Candidates for the cells acting as a guidance cue are glial cells, because they are generated before the retinal innervation to be located in the route of the subsequent R-axonal projection (Winberg et al, 1992). In several systems of both vertebrate and invertebrate, glial cells are present before neuronal differentiation and act as a substrate required for axonal guidance and neuronal migration (Hutchins and Casagrande, 1988;Jacobs and Goodman, 1989). This view is supported by the present result that expression of Rep0 in the lamina is impaired wild-type R-a argos rep0 Fig.…”