Differential distribution of AMPA receptors and glutamate during pre- and postnatal development in the visual cortex of ferrets

Abstract

Immunohistochemical methods were used to study the distribution and time-course of appearance of cells expressing glutamate and alpha-amino-3-hydroxy-5-methyl-4-isoaxazole propionic acid (AMPA)-type glutamate receptors (GluR1 and GluR2/3) during development of the ferret visual cortex. Glutamate is present in many neurons in the ventricular zone, intermediate zone, developing cortical plate, and marginal zone as early as embryonic day (E) 34 (birth is at E41 in ferrets). Glutamate attains its adult distribution coincident with the completion of cellular migration. By contrast, GluR1 immunoreactivity emerges more slowly. By birth, GluR1 immunoreactivity is present only in a few neurons in the marginal zone and ventricular zone but is abundant in the marginal zone and subplate, where synaptogenesis commences. The number and staining intensity of GluR1-positive cells increases dramatically during the first two postnatal weeks and is maximal between the second and third week, before slowly declining to adult levels. Cortical cells immunopositive for GluR2/3 follow a similar pattern, although their distribution differs: GluR2/3-positive cells are mainly pyramidal cells. During the first postnatal week, GluR2/3 is also transiently present in fibers in the intermediate zone, which at this stage contains many thalamocortical and callosal and corticofugal axons. The abundance of glutamate at fetal stages, especially in the ventricular zone, is consistent with the previously proposed role of glutamate in mediating trophic effects in vivo, as previously demonstrated in vitro. The expression of AMPA receptors, as well as their transient overexpression, confirms the results of in situ hybridization studies and may imply a developmental role in neuronal differentiation for these receptors, in addition to their mature role in mediating cortical transmission.

Glutamate Transporter Protein Subtypes Are Expressed Differentially during Rat CNS Development

“…Thus, during corticogenesis at late embryonic and early postnatal periods, glutamate transport by neurons, specifically via EAAC1, may predominate over astroglial transport of glutamate. Expression of EAAC1 at high levels in the external plexiform layer appears to coincide with the maturation of the apical dendritic bouquets of pyramidal neurons (Marín-Padilla, 1992) at a time when non-NMDA glutamate receptors are also highly enriched in the marginal zone (Furuta et al, 1995;Herrmann, 1996;Martin et al, 1997b). Glutamatergic mechanisms are operative in undifferentiated proliferative zones during embryogenesis.…”

“…Glutamatergic mechanisms are operative in undifferentiated proliferative zones during embryogenesis. Glutamate activates non-NMDA glutamate receptors in the ventricular zone (LoTurco et al, 1995), and AM PA receptor protein is expressed in proliferative zones in developing ferret (Herrmann, 1996), rat (Martin et al, 1997b), and ovine brain (Furuta et al, 1995). GL AST and GLT-1 mRNAs are expressed in the ventricular zone of embryonic mouse brain Sutherland et al, 1996); although, at low levels, we found GL AST immunoreactivity in the ventricular and subventricular zones of the telencephalon and GLT-l and EAAC1 immunoreactivities in the ganglionic eminence.…”

Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex

“…N -Methyl- d -aspartate (NMDA), α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) and kainate receptors and the essential subunits for their receptor function have been demonstrated in the subplate of various species, suggesting the presence of functional glutamatergic synapses in subplate neurons (Herrmann, 1996; Aoki, 1997; Catalano et al, 1997; Furuta and Martin, 1999). The expression of benzodiazepine binding sites (Schlumpf et al, 1983), GABA A receptors (Huntley et al, 1990) and GABA A receptor subunits (Meinecke and Rakic, 1992) in the subplate indicate that functional GABAergic synaptic inputs should also be present in subplate neurons.…”

Distribution of Glutamate Transporter Subtypes During Human Brain Development

“…In adult brain there is generally a correlation between glutamate uptake and glutamatergic ac- tivity in different brain regions (Kugler, 1993). Indeed, a-amino-3-hydroxy-5-methyli soxazole-4-propionate (AMPA) receptor protein is expressed in proliferative zones in developing ferret (Herrmann, 1996) and in rat (A. Furuta, personal observation).…”