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A cellular network of dye-coupled glia associated with the embryonic central complex in the grasshopper Schistocerca gregaria

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Abstract

The central complex of the grasshopper (Schistocerca gregaria) brain comprises a modular set of neuropils, which develops after mid-embryogenesis and is functional on hatching. Early in embryogenesis, Repo-positive glia cells are found intermingled among the commissures of the midbrain, but then redistribute as central complex modules become established and, by the end of embryogenesis, envelop all midbrain neuropils. The predominant glia associated with the central body during embryogenesis are glutamine synthetase-/Repo-positive astrocyte-like glia, which direct extensive processes (gliopodia) into and around midbrain neuropils. We used intracellular dye injection in brain slices to ascertain whether such glia are dye-coupled into a communicating cellular network during embryogenesis. Intracellular staining of individual cells located at any one of four sites around the central body revealed a population of dye-coupled cells whose number and spatial distribution were stereotypic for each site and comparable at both 70 and 100 % of embryogenesis. Subsequent immunolabeling confirmed these dye-coupled cells to be astrocyte-like glia. The addition of n-heptanol to the bathing saline prevented all dye coupling, consistent with gap junctions linking the glia surrounding the central body. Since dye coupling also occurred in the absence of direct intersomal contacts, it might additionally involve the extensive array of gliopodia, which develop after glia are arrayed around the central body. Collating the data from all injection sites suggests that the developing central body is surrounded by a network of dye-coupled glia, which we speculate may function as a positioning system for the developing neuropils of the central complex.

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Acknowledgments

We thank Dr. Les Williams for assistance with the silver intensification procedures, Karin Fischer for establishing protocols for producing the brain slices, and Ms. Stefanie Götz for criticisms of the manuscript. Grant sponsor: Deutsche Forschungsgemeinschaft (BO 1434/3-5).

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  1. Developmental Neurobiology Group, Biocenter, Ludwig-Maximilians-Universität, Grosshadernerstrasse 2, 82152, Martinsried, Germany

    George S. Boyan, Yu Liu & Michael Loser

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  1. George S. Boyan
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Correspondence to George S. Boyan.

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Fig. 10

Dye injection into extracellular space is not taken up by neighboring somata or processes. a Photomicrograph (DIC) of a brain slice (100 % of embryogenesis) shows tip of glass microelectrode filled with dye (Alexa® Fluor 568) situated in extracellular space (outlined dashed white) associated with a small cluster of glia cells (white stars) of the protocerebrum (PC). Several gliopodia are visible (white arrowheads). b. Fluorescence micrograph of the same preparation as a but following 5 min of dye injection into the extracellular space and with simultaneous background illumination (for details, see Fig. 4). Focal depth is slightly different to that in a in order to visualize neighboring cells (open white dots). Most of the dye has dissipated into extracellular space; some residual dye (open/white arrowhead) is still visible at the electrode tip. No dye has been taken up either by the cluster of glia cells (white stars) or their neighbors. Scale bar in b represents 22 μm throughout (JPEG 36 kb)

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Boyan, G.S., Liu, Y. & Loser, M. A cellular network of dye-coupled glia associated with the embryonic central complex in the grasshopper Schistocerca gregaria . Dev Genes Evol 222, 125–138 (2012). https://doi.org/10.1007/s00427-012-0394-8

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