Differential Change in Hippocampal Radial Astrocytes and Neurogenesis in Shorebirds With Contrasting Migratory Routes

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.

Contrasting migratory journeys and changes in hippocampal astrocyte morphology in shorebirds

“…In the present study, our samples included stellate and vascular but not radial astrocytes. Radial astrocytes, involved in adult neurogenesis and astrogenesis, have been previously investigated in the same species, and the influence of contrasting migratory flights on their morphology has been described and published elsewhere (Lima, 2019).…”

Shorebirds’ Longer Migratory Distances Are Associated With Larger ADCYAP1 Microsatellites and Greater Morphological Complexity of Hippocampal Astrocytes

“…We previously explored how the contrasting navigation strategies of the semipalmated sandpiper (Calidris pusilla) and the semipalmated plover (Charadrius semipalmatus) during autumn migration were related to hippocampal astroglia morphology (Carvalho-Paulo et al, 2018;Mendes de Lima et al, 2019;Henrique et al, 2020). This comparative analysis of morphological features to classify astrocytes revealed there were two types of morphological astrocytes influenced in different ways by contrasting long-distance migratory flights suggesting distinct physiological roles for these cells (Carvalho-Paulo et al, 2018;Henrique et al, 2020).…”

Shorebird’s Longer Migratory Distances are Associated with Larger ADCYAP1 Microsatellites and Greater Morphological Complexity of Hippocampal Astrocytes

“…The matrices were constructed with the combination of all cells of a given group taken pairwise, followed by the weighted calculation of a scalar Euclidean distance between cells using all morphometric variables. [23,24].…”

“…This system was coupled to a microprocessor that controlled the movements of the microscopic stage with the aid of a specialized program (Neurolucida, MBF Bioscience, Williston, VT USA) to store the spatial information (X, Y, Z coordinates) of each digitized point of interest. Three types of cells were identi ed: protoplasmic, brous and radial astrocytes similar to previous descriptions [22][23][24]. In this study, we used only protoplasmic astrocytes.…”

“…Because the hippocampal formation of migratory birds seems to be the center for integration of all navigation systems [14,17], we explored how the contrasting navigation strategies of the semipalmated sandpiper (Calidris pusilla) and the semipalmated plover (Charadrius semipalmatus) during autumn migration are related to hippocampal astroglia morphology [22][23][24] and size of the ADCYAP1 allele. A combination of genetic, developmental, and epigenetic factors de ne life-long adaptive plasticity of astroglia [25] and morphometric studies of its arbors and molecular pro le have revealed that they may change with environmental enrichment [26][27][28] learning and memory [29][30][31].…”