Abstract

Little is known about environmental influences on radial glia-like (RGL) α cells (radial astrocytes) and their relation to neurogenesis. Because radial glia is involved in adult neurogenesis and astrogenesis, we investigated this association in two migratory shorebird species that complete their autumnal migration using contrasting strategies. Before their flights to South America, the birds stop over at the Bay of Fundy in Canada. From there, the semipalmated sandpiper (Calidris pusilla) crosses the Atlantic Ocean in a non-stop 5-day flight, whereas the semipalmated plover (Charadrius semipalmatus) flies primarily overland with stopovers for rest and feeding. From the hierarchical cluster analysis of multimodal morphometric features, followed by the discriminant analysis, the radial astrocytes were classified into two main morphotypes, Type I and Type II. After migration, we detected differential changes in the morphology of these cells that were more intense in Type I than in Type II in both species. We also compared the number of doublecortin (DCX)-immunolabeled neurons with morphometric features of radial glial–like α cells in the hippocampal V region between C. pusilla and C. semipalmatus before and after autumn migration. Compared to migrating birds, the convex hull surface area of radial astrocytes increased significantly in wintering individuals in both C. semipalmatus and C. pusilla. Although to a different extent we found a strong correlation between the increase in the convex hull surface area and the increase in the total number of DCX immunostained neurons in both species. Despite phylogenetic differences, it is of interest to note that the increased morphological complexity of radial astrocytes in C. semipalmatus coincides with the fact that during the migratory process over the continent, the visuospatial environment changes more intensely than that associated with migration over Atlantic. The migratory flight of the semipalmated plover, with stopovers for feeding and rest, vs. the non-stop flight of the semipalmated sandpiper may differentially affect radial astrocyte morphology and neurogenesis.

Highlights

  • Radial glia are non-neuronal cells of the astroglial lineage, characterized by an ovoid cell body located near the ventricular wall with typically asymmetric bipolar branches

  • Independent of the origin of the sample, the results showed two families of astrocytes that we designated as Type I and Type II, respectively, in both C. pusilla (Figures 3, 4 and Tables 1, 2) and C. semipalmatus (Figures 5, 6 and Tables 3, 4)

  • We found that compared with migrating birds, the morphological complexity of radial glia-like (RGL) α cells in wintering birds significantly increased in C. semipalmatus and decreased in C. pusilla, to different magnitudes

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Summary

Introduction

Radial glia are non-neuronal cells of the astroglial lineage, characterized by an ovoid cell body located near the ventricular wall with typically asymmetric bipolar branches. Rakic coined the name when describing the mode of neuronal migration to the superficial layers of the fetal monkey neocortex (Rakic, 1972), suggesting that glial radial fibers provided guides for cell migration. The true (primary) radial glia seem to be limited to the developing brain, which has led to a change in the original designation of adult radial astrocytes to ‘‘radial glia-like (RGL)’’ in the adult brain. Adult radial glia, RGL cells, or radial astrocytes were coined to limit radial glia designation to the developmental period (Verkhratsky and Nedergaard, 2018). RGL cells expressing glial acid fibrillary protein (GFAP) found in the subgranular layer of the dentate gyrus and subventricular zone of adult animals show increased proliferative activity in association with vascular interaction, voluntary exercise on running wheels, or enriched environment (Bednarczyk et al, 2011; Kempermann, 2012)

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