Embryonic development of the pars intercerebralis/central complex of the grasshopper

Abstract

We have studied the embryonic development of the pars intercerebralis/central complex in the brain of the grasshopper using immunocytochemical and histochemical techniques. Expression of the cell-surface antigen lachesin reveals that the neuroblasts of the pars intercerebralis first differentiate from the neuroectoderm at around 26% of embryogenesis. Differentiation of medial and lateral neuroblasts occurs first. By the 28% stage a more or less uniform sheet of 20 neuroblasts has formed. As a result of both cell proliferation and cell translocation, the pars intercerebralis proliferative cluster in each hemisphere expands so that at 30% the most medial neuroblasts lie apposed at the midline. We followed the further development of the pars intercerebralis of each brain hemisphere using bromo-deoxy-uridine incorporation and osmium-ethyl-gallate staining. Within the pars intercerebralis itself, the neuroblasts redistribute into discrete subsets. The neuroblasts of each subset generate clusters of progeny which extend in a stereotypic, subset-specific direction in the brain. We have used this feature to identify one subset of four neuroblasts as being the likely progenitor cells for four clusters of embryonic neurons (W, X, Y, Z) which develop at around 55% of embryogenesis. We show that these progeny project axons via four discrete fascicles (w, x, y, z) into the embryonic central complex. At the single cell level, Golgi impregnation reveals that the axons from these neighbouring cell clusters remain discrete, and those from the same cluster tightly fasciculated, as they project into the central complex, consistent with a modular organization for this brain region.

Segment polarity and DV patterning gene expression reveals segmental organization of theDrosophilabrain

“…In Drosophila, little is known about the embryonic origin of the central complex. In the grasshopper, it was recently documented that NBs in the pars intercerebralis contribute neurones to the central complex (Boyan and Williams, 1997). Taking into consideration that the identified labral NBs presumably represent the progenitors of cells of the pars intercerebralis and that the fundamental 'bauplan' of the brain is believed to be conserved among insects (Boyan et al, 1993;Nassif et al, 1998), we suggest that, in Drosophila progeny cells of labral NBs participate in the formation of the central complex.…”

Compartmentalization of the precheliceral neuroectoderm in the spider Cupiennius salei: Development of the arcuate body, optic ganglia, and mushroom body

“…In this insect group, the progeny of neuroblasts that are located in each half of the developing pars intercerebralis, an area that contributes to the neuroendocrine system, give rise to the central complex (Boyan and Williams, 1997;Malzacher, 1968;Williams and Boyan, 2008;Williams et al, 2005). Thus, similarly to the case in the spider, the unpaired midline neuropile in orthopteran insects derives from bilateral groups of neural precursors.…”

Lazarillo expression reveals a subset of neurons contributing to the primary axon scaffold of the embryonic brain of the grasshopperSchistocerca gregaria

“…Two key events in the early embryonic development of the grasshopper brain involve the delamination of neuroblasts from the neuroectoderm Boyan and Williams, 1997) followed by directed axogenesis by pioneering progeny to establish a primary axon scaffold (Boyan et al, 1995). In the current study of axogenesis in the early embryonic brain of the grasshopper Schistocerca gregaria, we show that, despite the enormous complexity of the adult brain, a set of simple developmental processes involving individually identifiable cells and axons underlies early axogenesis.…”

“…Whereas considerable knowledge is now available on neurogenesis Younossi-Hartenstein et al, 1996;Boyan and Williams, 1997;Dumstrei et al, 1998) and the molecular genetics of insect brain development (Finkelstein and Perrimon, 1991;Schmidt-Ott and Technau, 1992;Finkelstein and Boncinelli, 1994;Schmidt-Ott et al, 1994;Hirth et al, 1995;Younossi-Hartenstein et al, 1997;Leuzinger et al, 1998;Hartmann and Reichert, 1998;Hirth et al, 1998), far less is known about the mechanisms by which the progeny of brain neuroblasts produce the complex axonal projections of the adult brain (Boyan et al, 1993(Boyan et al, , 1995Zacharias et al, 1993;Therianos et al, 1995;Boyan and Williams, 1997;Nassif et al, 1998).…”