Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species

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Abstract

In insects, morphological, molecular and genetic studies have provided a detailed insight into the ontogenetic processes that shape the ventral nerve cord. On the other hand, owing to its complexity and less obvious segmental composition, the knowledge about the development of the brain is still fragmentary. A promising approach towards gaining insight into fundamental processes underlying brain development is the comparison of embryonic brain development among different insect species. However, so far such comparative analyses are scarce. In this review, we summarize and compare data on the early steps in brain formation in different hemi- and holometabolous insects. We show that basic aspects of the spatial and temporal development of the embryonic brain neuroblast pattern are conserved among insects. Furthermore, we compare the number and proliferation patterns of neuroblasts related to major neuropil structures such as mushroom bodies, central complex, and antennal lobe. Finally, comparing the expression patterns of engrailed in different species, and considering new data from Drosophila melanogaster, we discuss the segmental organization of the insect brain.

Introduction

An initial step in the development of the central nervous system (CNS) is the determination of a specialized ectodermal region, the neurogenic region. In insects, the CNS of the trunk (ventral nerve cord) derives from the ventral neurogenic region, and the brain from the procephalic neurogenic region. In a second step, a population of neural stem cells, called neuroblasts (Wheeler, 1891, Wheeler, 1893) becomes defined, and these cells subsequently delaminate from the neuroectoderm (cells remaining in the periphery develop as epidermoblasts). Finally, each neuroblast produces a certain number of progeny cells which differentiate into specific neuronal and/or glial cell types. Accordingly, each neuroblast generates a characteristic cell lineage. Various aspects of these processes during early neurogenesis have been morphologically described in several insect species. The genetic mechanisms controlling neuroblast formation and specification have been elucidated using the fruit fly Drosophila melanogaster Meigen, 1830 (Diptera) as a model system. Work on this system has also provided a large collection of technical tools, such as molecular markers, which are now extensively applied in the developmental analysis and comparison with other species.

In the following, we summarize and compare data on early neurogenesis in different hemi- and holometabolous insect species (including long germ band and short germ band insects). We will mainly focus on the pattern of neuroblast formation and segmentation in the developing embryonic brain.

Section snippets

Spatial and temporal aspects of the developing brain neuroblast pattern

Due to morphogenetic movements of the procephalic ectoderm and growth during early neurogenesis the spatial orientation of the brain neuraxis changes relative to the embryonic body axis (e.g. in the desert locust Schistocerca gregaria Forskål, 1775 (Caelifera): Zacharias et al., 1993, Boyan et al., 1995a; the yellow meal beetle Tenebrio molitor Linné, 1758 (Coleoptera): Urbach et al., 2003a, and D. melanogaster: Schmidt-Ott and Technau, 1994). We therefore refer in the following to the neuraxis

Numbers of brain neuroblasts

An overview of the numbers of NBs found in the different parts of the brain of several insect species is summarized in Table 1. The total number of brain NBs does not differ significantly among the orthopterans C. morosus and S. gregaria (Malzacher, 1968, Zacharias et al., 1993), the blattodean P. americana (Malzacher, 1968), and the coleopteran T. molitor (Urbach et al., 2003a). In each of these species about 120–130 NBs, and in D. melanogaster about 106 NBs (Urbach et al., 2003b) have been

Modes of brain neuroblast formation

In general, the process of brain NB formation appears to be similar in different insects. In S. gregaria and D. melanogaster it has been shown that brain NBs delaminate from the neuroectoderm, very similar to NBs in the trunk. Thereby, single cells enlarge and subsequentially move into the embryo (Poulson, 1950, Doe and Goodman, 1985, Zacharias et al., 1993, Younossi-Hartenstein et al., 1996, Urbach et al., 2003b; Hartenstein and Campos-Ortega, 1984). However, in D. melanogaster additional

Aspects of brain neuroblast proliferation

In most insect species brain NBs divide asymmetrically in a stem cell mode, budding off a chain of smaller ganglion mother cells, which then divide symmetrically to give rise to two neural progeny cells (Bauer, 1904, Schrader, 1938, Poulson, 1950, Panov, 1963, Malzacher, 1968, Younossi-Hartenstein et al., 1996, Urbach et al., 2003a, Urbach et al., 2003b). However, glial precursors might divide symmetrically. For example, in D. melanogaster, a tritocerebral glioblast has been characterized (Td7

Brain midline structures

In the trunk of the early embryo of D. melanogaster mesectodermal cells on either side separate the anlage of the mesoderm from the lateral neurogenic ectoderm and become aligned along the ventral midline upon gastrulation. In D. melanogaster and S. gregaria these mesectodermal progenitors give rise to glia and neurons forming the midline region of the ventral nerve cord (Jacobs and Goodman, 1989, Klämbt et al., 1991, Bossing and Technau, 1994, Condron et al., 1994, Sonnenfeld and Jacobs, 1994

Mushroom body neuroblasts

The mushroom bodies represent a paired protocerebral brain structure which is found in all insects (as well as in other arthropod groups except crustaceans; reviewed in Strausfeld et al. (1998)), and are involved in higher brain function, like olfactory learning and memory (for review see Heisenberg, 1998, Menzel, 2001). They consist of a large number of neurons (Kenyon cells) the fibres of which forming typical substructures, the calyx, peduncle and lobes (Fig. 3A). Despite the highly

Identification of individual neuroblasts and serial homology in D. melanogaster

As shown above, the comparative analysis of early embryonic brain development in insects has so far been largely limited to descriptions of the general pattern or subgroups of progenitor cells. To gain deeper insight into the evolution of early brain development the analysis has to be brought to the level of individually identifiable cells. In D. melanogaster, about 100 embryonic brain NBs have been shown to develop on either side from the procephalic neuroectoderm according to a well defined

Comparison of engrailed expression in the early brain of different insects and its implication for head segmentation

The segment-polarity gene engrailed (en) is expressed in the posterior compartment of each segment (Kornberg et al., 1985, DiNardo et al., 1985) and has been used by several authors to describe the metameric organization of the insect head and brain (Diederich et al., 1991, Fleig, 1994, Schmidt-Ott and Technau, 1992, Schmidt-Ott et al., 1994a, Schmidt-Ott et al., 1994b, Zacharias et al., 1993, Younossi-Hartenstein et al., 1996, Rogers and Kaufman, 1996, Boyan and Williams, 2000, Boyan and

A neuromeric model of the brain in D. melanogaster

As discussed above, En has been employed so far as a segmental marker, which is informative with regard to the number and perhaps position of neuromeres. Due to the fact that in the procephalon, in contrast to the trunk, En marks only part of the border between two segments, substantial parts of the segmental boundary remained unclear. In addition, brain NBs are not arranged in a repetitive segmental pattern, and morphological landmarks which may indicate neuromeric boundaries are normally

Prospects

Although the arthropod body plan exhibits great diversity, the organization of the head shows striking similarities in members of some of the major taxa of euarthropods (including myriapods, crustaceans, insects, and presumably chelicerates; e.g. Damen et al., 1998, Popadic et al., 1998a, Abzhanov and Kaufman, 1999, Hughes and Kaufman, 2002). Among insects and crustaceans, a subdivision of the brain into three main regions, the trito-, deuto- and protocerebrum, appears to be conserved (Bullock

Acknowledgements

We are grateful to Ana Rogulja-Ortmann for comments on the manuscript and to the Deutsche Forschungsgemeinschaft for support.

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