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Neurogenesis, gliogenesis and the developing chicken optic tectum: an immunohistochemical and ultrastructural analysis

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Abstract

We present the first comprehensive analysis of avian optic tectum development, including proliferation, migration and maturation of both neuronal and glial cells. The distribution of doublecortin, Tuj-1, vimentin and GFAP was characterized by immunohistochemistry between E3 and E20, and correlated with the electron microscopic structure in the chicken optic tectum. The immunohistological markers used in our study are known to be critical for distinct steps of neurogenesis and gliogenesis. We demonstrate that neurogenesis within the optic tectum starts at E3 with prominent doublecortin and moderate Tuj-1 expression. With the aid of electron microscopy, we also show that most of the cells are still undifferentiated at E4. Starting from E6, all postmitotic Tuj-1-positive neurons have left the ventricular zone and concurrently, with the end of proliferation around E12, doublecortin disappears from this region. Before hatching, doublecortin expression totally ceases, indicating that now all neurons have matured, this was also confirmed by ultrastructural investigations. Furthermore, vimentin expression starts around E4, prior to the appearance of the first radial glial cells at E6. Astrocytes can be detected by GFAP expression at E12. As radial glial cells (RGC) transform into astrocytes between E12 and E20, the vimentin signal is progressively replaced by the GFAP signal. We could also show that vimentin-positive RGCs do express doublecortin between E4 and E6, the time-point of prominent neurogenesis, reflecting their bipotent character.

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Abbreviations

CLSM:

Confocal laser scanning microscopy

DCX:

Doublecortin

E :

Embryonic day

EZ:

Ependymal zone

GFAP:

Glial fibrillary acidic protein

HH:

Developmental stage according to classification of Hamburger and Hamilton

INP:

Intermediate neuronal precursors

IZ:

Intermediate zone

L:

Layer

MZ:

Marginal zone

NSC:

Neural stem cells

OT:

Optic tectum

PBS:

Phosphate-buffered saline

PFA:

Paraformaldehyde

RGC:

Radial glial cells

SAC:

Stratum album centrale

SFP:

Stratum fibrosum periventriculare

SGC:

Stratum griseum centrale

SGFS:

Stratum griseum et fibrosum superficiale

SO:

Stratum opticum

TP:

Tectal plate

Tuj-1:

βIII-tubulin, clone Tuj-1

VZ:

Ventricular zone

References

  • Anthony TE, Klein C, Fishell G, Heintz N (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41(6):881–890

    Article  CAS  PubMed  Google Scholar 

  • Benowitz LI, Karten HJ (1976) Organization of the tectofugal visual pathway in the pigeon: a retrograde transport study. J Comp Neurol 167(4):503–520

    Article  CAS  PubMed  Google Scholar 

  • Bloch J, Kaeser M, Sadeghi Y, Rouiller EM, Redmond DE Jr, Brunet JF (2011) Doublecortin-positive cells in the adult primate cerebral cortex and possible role in brain plasticity and development. J Comp Neurol 519(4):775–789

    Article  CAS  PubMed  Google Scholar 

  • Bohn W, Wiegers W, Beuttenmüller M, Traub P (1992) Species-specific recognition of monoclonal antibodies directed against vimentin. Exp Cell Res 201(1):1–7

    Article  CAS  PubMed  Google Scholar 

  • Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Capes-Davis A, Tolhurst O, Dunn JM, Jeffrey PL (2005) Expression of doublecortin (DCX) and doublecortin-like kinase (DCLK) within the developing chick brain. Dev Dyn 232(2):457–467

    Article  CAS  PubMed  Google Scholar 

  • Charalambous P, Hurst LA, Thanos S (2008) Engrafted chicken neural tube-derived stem cells support the innate propensity for axonal regeneration within the rat optic nerve. Invest Ophthalmol Vis Sci 49(8):3513–3524

    Article  PubMed  Google Scholar 

  • Corbin JG, Gaiano N, Juliano SL, Poluch S, Stancik E, Haydar TF (2008) Regulation of neural progenitor cell development in the nervous system. J Neurochem 106(6):2272–2287

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21(1):1–14

    Article  PubMed  Google Scholar 

  • Cowan WM, Adamson L, Powell TP (1961) An experimental study of the avian visual system. J Anat 95:545–563

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fedtsova N, Quina LA, Wang S, Turner EE (2008) Regulation of the development of tectal neurons and their projections by transcription factors Brn3a and Pax7. Dev Biol 316(1):6–20

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23(2):247–256

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara A, Ohozone Y, Naito J (2000) The developmental study on lamination of the optic tectum in relation to the retinotectal projection in chicks and chick embryos. J Vet Med Sci 62(5):511–516

    Article  CAS  PubMed  Google Scholar 

  • Galileo DS, Gray GE, Owens GC, Majors J, Sanes JR (1990) Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-specific antibodies. Proc Natl Acad Sci USA 87(1):458–462

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257–271

    Article  CAS  PubMed  Google Scholar 

  • Gray GE (1990) Migratory patterns of clonally related cells in the developing central nervous system. Experientia 46(9):929–940

    Article  CAS  PubMed  Google Scholar 

  • Gray GE, Sanes JR (1991) Migratory paths and phenotypic choices of clonally related cells in the avian optic tectum. Neuron 6(2):211–225

    Article  CAS  PubMed  Google Scholar 

  • Gray GE, Glover JC, Majors J, Sanes JR (1988) Radial arrangement of clonally related cells in the chicken optic tectum: lineage analysis with a recombinant retrovirus. Proc Natl Acad Sci USA 85(19):7356–7360

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Güntürkün O, Melsbach G, Hörster W, Daniel S (1993) Different sets of afferents are demonstrated by the fluorescent tracers fast blue and rhodamine. J Neurosci Methods 49(1–2):103–111

    Article  PubMed  Google Scholar 

  • Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195(4):231–272

    Article  CAS  PubMed  Google Scholar 

  • Hayes BP, Webster KE (1985) Cytoarchitectural fields and retinal termination: an axonal transport study of laminar organization in the avian optic tectum. Neuroscience 16(3):641–657

    Article  CAS  PubMed  Google Scholar 

  • Kálmán M, Székely AD, Csillag A (1998) Distribution of glial fibrillary acidic protein and vimentin-immunopositive elements in the developing chicken brain from hatch to adulthood. Anat Embryol (Berl) 198(3):213–235

    Article  Google Scholar 

  • Karten HJ, Revzin AM (1966) The afferent connections of the nucleus rotundus in the pigeon. Brain Res 2(4):368–377

    Article  CAS  PubMed  Google Scholar 

  • Karten HJ, Shimizu T (1989) The origins of neocortex: connections and laminations as distinct events in evolution. J Cog Neurosci 1:291–301

    Article  CAS  Google Scholar 

  • Karten HJ, Cox K, Mpodozis J (1997) Two distinct populations of tectal neurons have unique connections within the retinal tectoro tundal pathway of the pigeon (Columba livia). J Comp Neurol 387(3):449–465

    Article  CAS  PubMed  Google Scholar 

  • Kim DW, Park SW, Jeon GS, Seo JH, Golden JA, Cho SS (2006) The multiple dorsoventral origins and migratory pathway of tectal oligodendrocytes in the developing chick. Brain Res 1:16–24

    Google Scholar 

  • Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, Horvat V, Volk B, Kempermann G (2010) Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS ONE 5(1):e8809

    Article  PubMed Central  PubMed  Google Scholar 

  • Korzhevskii DE, Petrova ES, Kirik OV, Otellin VA (2009) Assessment of neuron differentiation during embryogenesis in rats using immunocytochemical detection of doublecortin. Neurosci Behav Physiol 39(6):513–516

    Article  CAS  PubMed  Google Scholar 

  • Kriegstein AR, Götz M (2003) Radial glia diversity: a matter of cell fate. Glia 43(1):37–43

    Article  PubMed  Google Scholar 

  • Kriegstein A, Noctor S, Martínez-Cerdeño V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7(11):883–890

    Article  CAS  PubMed  Google Scholar 

  • LaVail JH, Cowan WM (1971a) The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Res 28(3):391–419

    Article  CAS  PubMed  Google Scholar 

  • LaVail JH, Cowan WM (1971b) The development of the chick optic tectum. II. Autoradiographic studies. Brain Res 28(3):421–441

    Article  CAS  PubMed  Google Scholar 

  • Luksch H, Cox K, Karten HJ (1998) Bottlebrush dendritic endings and large dendritic fields: motion-detecting neurons in the tectofugal pathway. J Comp Neurol 396(3):399–414

    Article  CAS  PubMed  Google Scholar 

  • Malatesta P, Hartfuss E, Götz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127(24):5253–5263

    CAS  PubMed  Google Scholar 

  • McGraw CF, McLaughlin BJ (1980) Fine structural studies of synaptogenesis in the superficial layers of the chick optic tectum. J Neurocytol 9(1):79–93

    Article  CAS  PubMed  Google Scholar 

  • Menezes JR, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14(9):5399–5416

    CAS  PubMed  Google Scholar 

  • Mey J, Thanos S (2000) Development of the visual system of the chick. I. Cell differentiation and histogenesis. Brain Res Rev 32(2–3):343–379

    Article  CAS  PubMed  Google Scholar 

  • Mission JP, Takahashi T, Caviness VS Jr (1991) Ontogeny of radial and other astroglial cells in murine cerebral cortex. Glia 4(2):138–148

    Article  CAS  PubMed  Google Scholar 

  • Mizuguchi M, Yamanouchi H, Becker LE, Itoh M, Takashima S (2002) Doublecortin immunoreactivity in giant cells of tuberous sclerosis and focal cortical dysplasia. Acta Neuropathol 104(4):418–424

    CAS  PubMed  Google Scholar 

  • Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7(2):136–144

    Article  CAS  PubMed  Google Scholar 

  • Rager G (1976) Morphogenesis and physiogenesis of the retino-tectal connection in the chicken. II. The retino-tectal synapses. Proc R Soc Lond B Biol Sci 192(1108):353–370

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145(1):61–83

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (1988) Defects of neuronal migration and the pathogenesis of cortical malformations. Prog Brain Res 73:15–37

    Article  CAS  PubMed  Google Scholar 

  • Rapacioli M, Rodriguez CA, Duarte S, Ortallli AL, Di Napoli J, Teruel L, Sánchez V, Scicolone G, Flores V (2011) The chick optic tectum developmental stages. A dynamic table based on temporal- and spatial- dependent histogenetic changes: a structural, morphometric and immunocytochemical analysis. J Morphol 272(6):675–697

    Article  PubMed  Google Scholar 

  • Reiner A, Karten HJ (1982) Laminar distribution of the cells of origin of the descending tectofugal pathways in the pigeon (Columba livia). J Comp Neurol 204(2):165–187

    Article  CAS  PubMed  Google Scholar 

  • Rogers LJ (1995) The Development of brain and behaviour in the chicken, 1st edn. CABI Publishing, Wallingford pp 217

    Google Scholar 

  • Scicolone G, Pereyra-Alfonso S, Brusco A, Pecci Saavedra J, Flores V (1995) Development of the laminated pattern of the chick tectum opticum. Int J Dev Neurosci 13(8):845–858

    Article  CAS  PubMed  Google Scholar 

  • Seo JH, Chang JH, Song SH, Lee HN, Jeon GS, Kim DW, Chung CK, Cho SS (2008) Spatiotemporal gradient of astrocyte development in the chick optic tectum: evidence for multiple origins and migratory paths of astrocytes. Neurochem Res 33(7):1346–1355

    Article  CAS  PubMed  Google Scholar 

  • Snow RL, Robson JA (1995) Migration and differentiation of neurons in the retina and optic tectum of the chick. Exp Neurol 134(1):13–24

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama S, Nakamura H (2003) The role of Grg4 in tectal laminar formation. Development 130(3):451–462

    Article  CAS  PubMed  Google Scholar 

  • Thanos S, Mey J (2001) Development of the visual system of the chick. II. Mechanisms of axonal guidance. Brain Res Rev 35(3):205–245

    Article  CAS  PubMed  Google Scholar 

  • von Bohlen und Halbach O (2011) Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res 345(1):1–19

  • Walker TL, Yasuda T, Adams DJ, Bartlett PF (2007) The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27(14):3734–3742

    Article  CAS  PubMed  Google Scholar 

  • Wirsching HG, Kretz O, Morosan-Puopolo G, Chernogorova P, Theiss C, Brand-Saberi B (2012) Thymosin β4 induces folding of the developing optic tectum in the chicken (Gallus domesticus). J Comp Neurol 520(8):1650–1662

    Article  CAS  PubMed  Google Scholar 

  • Yang HK, Sundholm-Peters NL, Goings GE, Walker AS, Hyland K, Szele FG (2004) Distribution of doublecortin expressing cells near the lateral ventricles in the adult mouse brain. Neurosci Res 76(3):282–295

    Article  CAS  Google Scholar 

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Acknowledgments

We wish to thank Daniel Terheyden-Keighley and Alison Jacob for critically reading the manuscript, C. Grzelak, H.-T. Nguyen and A. Lodwig for excellent technical assistance, as well as A. Lenz for secretarial work.

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The authors declare that they have no competing interests.

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  1. Faculty of Medicine, Institute of Anatomy and Molecular Embryology, Ruhr-University Bochum, Universitätsstraße 150, 44780, Bochum, Germany

    Mael Lever, Beate Brand-Saberi & Carsten Theiss

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  1. Mael Lever
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  2. Beate Brand-Saberi
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Correspondence to Beate Brand-Saberi.

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Lever, M., Brand-Saberi, B. & Theiss, C. Neurogenesis, gliogenesis and the developing chicken optic tectum: an immunohistochemical and ultrastructural analysis. Brain Struct Funct 219, 1009–1024 (2014). https://doi.org/10.1007/s00429-013-0550-6

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