Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells.

The earliest events in the development of the central nervous system in insect embryos involve the differentiation of a stereotyped pattern of individually identified neuronal precursor cells, called neuroblasts (NBs), each of which generates a stereotyped family of neuronal progeny. After gastrulation, the midventral region of the ectoderm becomes a neuroepithelium; it is from this sheet of seemingly uniform ectodermal cells that certain cells enlarge to become NBs while the rest of the cells either die or acquire other nonneuronal phenotypes. Here we focus on three aspects of neurogenesis. First, we examine the morphological changes associated with the differentiation of neuronal precursor cells and nonneuronal support cells. The differentiation of each cell type is reflected by its morphology; moreover, the identity of individual cells of certain cell types (e.g., a particular NB) is reflected by their position within the neuroepithelium. Second, we show that there is a characteristic temporal sequence of differentiation in the stereotyped pattern of NBs. Third, we show that this stereotyped pattern of NBs varies in a segment-specific way by the addition or deletion of particular neuronal precursor cells. These studies on the events of early neurogenesis set the stage for the experimental manipulations described in the following paper (C. Q. Doe and C.S. Goodman, 1985, Dev. Biol. 110, 206-219).

[1]  C. Bate.  Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. , 1976, Journal of embryology and experimental morphology.

[2]  J. White,et al.  On the control of germ cell development in Caenorhabditis elegans. , 1981, Developmental biology.

[3]  K. White.  Defective neural development in Drosophila melanogaster embryos deficient for the tip of the X chromosome. , 1980, Developmental biology.

[4]  E. Hafen,et al.  Spatial distribution of Antennapedia transcripts during Drosophila development. , 1983, The EMBO journal.

[5]  C. Bate,et al.  Embryogenesis of an insect nervous system II: a second class of neuron precursor cells and the origin of the intersegmental connectives. , 1981, Journal of embryology and experimental morphology.

[6]  G. Mitchison,et al.  Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms. , 1973, Journal of cell science.

[7]  C Q Doe,et al.  Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. , 1985, Developmental biology.

[8]  C. Goodman,et al.  Cell determination and differentiation of identified serotonin- immunoreactive neurons in the grasshopper embryo , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  C. Goodman.  Embryonic Development of Identified Neurons in the Grasshopper , 1982 .

[10]  J Kimble,et al.  Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegans. , 1981, Developmental biology.

[11]  W. M. Wheeler.  A contribution to insect embryology , 1893 .

[12]  J. G. Carlson,et al.  Studies on cytokinesis in neuroblasts of the grasshopper, Chortophaga viridifasciata (De Geer). III. Factors determining the location of the cleavage furrow. , 1962, Experimental cell research.

[13]  C. Goodman,et al.  Neuronal determination during embryonic development of the grasshopper nervous system. , 1985, Developmental biology.

[14]  H. Keshishian,et al.  Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. , 1979, Journal of embryology and experimental morphology.

[15]  M J Bastiani,et al.  Cell recognition during neuronal development. , 1984, Science.

[16]  C. Goodman,et al.  Embryonic development of identified neurones: differentiation from neuroblast to neurone , 1979, Nature.

[17]  R. Ho,et al.  Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. , 1982, Developmental biology.

[18]  P. Lawrence.  The cellular basis of segmentation in insects , 1981, Cell.

[19]  J. Campos-Ortega,et al.  A region of the Drosophila genome necessary for CNS development , 1979, Nature.

[20]  C. Goodman,et al.  Cell determination and regulation during development of neuroblasts and neurones in grasshopper embryo , 1984, Nature.

[21]  J. Sulston,et al.  The embryonic cell lineage of the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[22]  V. Wigglesworth,et al.  Local and General Factors in the Development of "Pattern" in Rhodnius Prolixus (Hemiptera) , 1940 .

[23]  M. Bastiani,et al.  Pathfinding by neuronal growth cones in grasshopper embryos. III. Selective affinity of the G growth cone for the P cells within the A/P fascicle , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  G. Mitchison,et al.  Phyllotaxis and the Fibonacci Series , 1977, Science.

[25]  A. Garcı́a-Bellido,et al.  Developmental Analysis of the Achaete-Scute System of DROSOPHILA MELANOGASTER. , 1978, Genetics.

[26]  F. Turner,et al.  Scanning electron microscopy of Drosophila melanogaster embryogenesis. II. Gastrulation and segmentation. , 1977, Developmental Biology.

[27]  H. Horvitz,et al.  Mutations that affect neural cell lineages and cell fates during the development of the nematode Caenorhabditis elegans. , 1983, Cold Spring Harbor symposia on quantitative biology.

[28]  Michael Bate,et al.  Neuronal development in the grasshopper , 1981, Trends in Neurosciences.

[29]  J. Sulston,et al.  Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. , 1980, Developmental biology.

[30]  J. Sulston,et al.  Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. , 1977, Developmental biology.

[31]  J. Richelle,et al.  Determination of sensory bristles and pattern formation in Drosophila. I. A model. , 1979, Developmental biology.

[32]  M. Bastiani,et al.  From grasshopper to Drosophila: a common plan for neuronal development , 1984, Nature.

[33]  C STERN,et al.  Two or three bristles. , 1955, Science in progress.