Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species
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.
References (170)
- et al.
The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm
Developmental Biology
(1996) - et al.
Building the antennal lobe: engrailed expression reveals a contribution from protocerebral neuroblasts in the grasshopper Schistocerca gregaria
Arthropod Structure and Development
(2000) - et al.
A single cell analysis of engrailed in the early embryonic brain of the grasshopper Schistocerca gregaria: ontogeny and identity of the secondary head spot cells
Arthropod Structure and Development
(2002) - et al.
Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust
Arthropod Structure and Development
(2002) - et al.
New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system
Mechanisms of Development
(1995) - et al.
Engrailed controls glial/neuronal cell fate decisions at the midline of the central nervous system
Neuron
(1994) - et al.
Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein
Cell
(1985) - et al.
Early events in insect neurogenesis I. Development and segmental differences in the pattern of neuronal precursor cells
Developmental Biology
(1985) - et al.
How far does cell lineage influence cell fate specification in crustacean embryos?
Seminars in Cell Development and Biology
(1997) - et al.
Embryogenesis of the honey bee Apis mellifera L. (Hymenoptera: Apidae): and SEM study
International Journal of Insect Morphology and Embryology
(1986)
An immunhistochemical study on structure and development of the nervous system in the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda, Anostraca) with remarks on the evolution of the arthropod brain
Arthropod Structure and Development
Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster
Developmental Biology
The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance
Cell
The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression
Cell
Secretion and localized transcription suggests a role in positional signaling for products of the segmentation gene hedgehog
Cell
Common design in a unique midline neuropil in the brains of arthropods
Arthropod Structure and Development
Expression of engrailed proteins in arthropods, annelids, and chordates
Cell
Homeotic genes and the arthropod head: expression patterns of the labial, proboscipedia, and deformed genes in crustaceans and insects
Proceedings of the National Academy of Science in U S A
Embryology and Phylogeny in Annelids and Arthropods
Embryology of the butterbur stem sawfly Aglaeostigma occipitosa (Malaise) are studied by external observations (Tenthredinidae, Hymenoptera)
Acta Hymenoptera
Zur inneren Metamorphose des Zentralnervensystems der Insekten
Zoologisches Jahrbuch der Abteilung Anatomie und Ontogenie der Tiere
The short antennae of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein
Development
Patterns of neurogenesis in the midbrain of embryonic lobsters differ from proliferation in the insect and the crustacean ventral nerve cord
Journal of Neurobiology
Modulation of life-long neurogenesis in the decapod crustacean brain
Arthropod Structure and Development
The fate of the CNS midline progenitors in Drosophila as revealed by a new method for single cell labelling
Development
Embryonic development of the pars intercerebralis/central complex of the grasshopper
Development Genes Evolution
Morphogenetic reorganization of the brain during embryogenesis in the grasshopper
Journal of Comparative Neurology
Organization of a midline proliferative cluster in the embryonic brain of the grasshopper
Roux's Archives of Developmental Biology
Structural homology of identified motoneurones in larval and adult stages of hemi- and holometabolous insects
Journal of Comparative Neurology
Embryonic and postembryonic development of serial homologous neurons in the subesophageal ganglion of Tenebrio molitor (Insecta: Coleoptera)
Microscopy Research and Technique
Neuroanatomy of the central nervous system of the harvestman, Rilaena triangularis (HERBST 1799) (Arachnida, Opiliones)—Principal organization, GABA-like and serotonin-immunohistochemistry
Zoologischer Anzeiger
Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca
Development
Embryonic expression of the single Tribolium engrailed homolog
Developmental Genetics
Structure and Function in the Nervous System of Invertebrates
The Neurobiology of an Insect Brain
Genetic mechanisms of early neurogenesis in Drosophila melanogaster
Molecular Neurobiology
Neurogenesis in adult insect mushroom bodies
Journal of Comparative Neurology
A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider
Proceedings of the National Academy of Science U S A
The organization of the subesophageal nervous system in Tardigrades: insights into the evolution of the arthropod hypostome and tritocerebrum
Zoologischer Anzeiger
Developmental and evolutionary implications of labial, deformed and engrailed expression in the Drosophila head
Development
Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system
Development
Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more simiarities to chelicerates than to insects
Development
EGFR signaling is required for the differentiation and maintenance of neural progenitors along the dorsal midline of the Drosophila embryonic head
Development
The embryology of Pieris rapae. Organogeny
Philosophical Transactions of the Royal Society London B
Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system
Journal of Morphology
Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation
Journal of Comparative Neurology
Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera
Journal of Comparative Neurology
Engrailed expression and body segmentation in the honeybee Apis mellifera
Roux's Archives of Developmental Biology
Head segmentation in the embryo of the Colorado beetle Leptinotarsa decemlineata as seen with anti-en immunostaining
Roux's Archives of Developmental Biology
Über den einheitlichen Bau des Gehirns in den verschiedenen Insektenordnungen
Zeitschrift für Wissenschaftliche Zoologie
Cited by (86)
Brain size scaling through development in the whitelined sphinx moth (Hyles lineata) shows mass and cell number comparable to flies, bees, and wasps
2024, Arthropod Structure and DevelopmentMetamorphosis and denucleation of the brain in the miniature wasp Megaphragma viggianii (Hymenoptera: Trichogrammatidae)
2022, Arthropod Structure and DevelopmentCitation Excerpt :Over the last century, development of the brain and its neuropilar centers during metamorphosis was described in detail for a wide range of insect orders, covering such structures as the mushroom bodies (Panov, 1957; Edwards, 1970; Nordlander and Edwards, 1970; Ito and Hotta, 1992; Farris et al., 1999; Farris and Sinakevitch 2003; Panov, 2022), antennal lobes (Panov, 1959a, 1961a; Edwards, 1970; Nordlander and Edwards, 1970; Groh and Rössler, 2008; Roat and da Cruz-Landim, 2011), optic lobes (Hanström, 1926; Pflugfelder 1936, 1937; Panov, 1960; Nordlander and Edwards, 1969), and central complex (Panov, 1959b; Nordlander and Edwards, 1970; Wegerhoff and Breidbach, 1992). Most of the studies published in the 21st century are devoted to neurogenesis and the regulation of insect brain development (Urbach and Technau, 2003; Urbach et al., 2003; Lichtneckert and Reichert, 2005; Technau, 2008; Spindler and Hartenstein, 2010; Bridi et al., 2020). Dynamics and quantitative data of brain/body changes (volumes, cell number, etc.) during postembryonic development have been obtained for some insect species (Power, 1952; Panov, 1961b, c; Hinke, 1961; Lucht-Bertram, 1962; Witthöft, 1967; Staub, 1979).
Genetic mechanisms controlling anterior expansion of the central nervous system
2020, Current Topics in Developmental BiologyCitation Excerpt :Two factors contribute to the phenomenon of “super generation” of NBs in B1. First, group delamination of NBs from the proneural clusters of the procephalic neurogenic regions (Urbach & Technau, 2003), as opposed to the single NB delamination from the proneural clusters of the ventral neurogenic regions (Campos-Ortega, 1993). This is, in part, caused by reduced Notch signaling in the procephalic neuroectoderm (Stuttem & Campos-Ortega, 1991; Urbach & Technau, 2003).
A general theory of genital homologies for the Hexapoda (Pancrustacea) derived from skeletomuscular correspondences, with emphasis on the Endopterygota
2018, Arthropod Structure and DevelopmentOrigin and evolution of the panarthropod head – A palaeobiological and developmental perspective
2017, Arthropod Structure and DevelopmentFrom the Eye to the Brain. Development of the Drosophila Visual System
2016, Current Topics in Developmental Biology