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Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications

Brain Structure and Function volume 220, pages 2905–2926 (2015)Cite this article

Abstract

Tangential neuronal migration occurs along different axes from the axis demarcated by radial glia and it is thought to have evolved as a mechanism to increase the diversity of cell types in brain areas, which in turn resulted in increased complexity of functional networks. In the telencephalon of amniotes, different embryonic tangential pathways have been characterized. However, little is known about the exact routes of migrations in basal vertebrates. Cartilaginous fishes occupy a key phylogenetic position to assess the ancestral condition of vertebrate brain organization. In order to identify putative subpallial-derived tangential migratory pathways in the telencephalon of sharks, we performed a detailed analysis of the distribution pattern of GAD and Dlx2, two reliable markers of tangentially migrating interneurons of subpallial origin in the developing forebrain. We propose the existence of five tangential routes directed toward different telencephalic regions. We conclude that four of the five routes might have emerged in the common ancestor of jawed vertebrates. We have paid special attention to the characterization of the proposed migratory pathway directed towards the olfactory bulbs. Our results suggest that it may be equivalent to the “rostral migratory stream” of mammals and led us to propose a hypothesis about its evolution. The analysis of the final destinations of two other streams allowed us to identify the putative dorsal and medial pallium of sharks, the regions from which the neocortex and hippocampus might have, respectively, evolved. Derived features were also reported and served to explain some distinctive traits in the morphology of the telencephalon of cartilaginous fishes.

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Abbreviations

Cb:

Cerebellum

Di:

Diencephalon

Glom:

Glomerulus

LGE-h:

Lateral ganglionic eminence homolog

LS:

Lateral stream

Mes:

Mesencephalon

MGE-h:

Medial ganglionic eminence homolog

MS:

Medial stream

MP:

Medial pallium

OB:

Olfactory bulb

OT:

Optic tectum

P:

Pallium

Rh:

Rhombencephalon

RS:

Rostral stream

Sp:

Subpallium

Tel:

Telencephalon

V:

Ventricle

References

  • Abellán A, Legaz I, Vernier B, Rétaux S, Medina L (2009) Olfactory and amygdalar structures of the chicken ventral pallium based on the combinatorial expression patterns of LIM and other developmental regulatory genes. J Comp Neurol 516:166–186

    Article  PubMed  CAS  Google Scholar 

  • Adolf B, Chapouton P, Lam CS, Topp S, Tannhäuser B, Strähle U, Götz M, Bally-Cuif L (2006) Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295:278–293

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A (1997) Mechanism of migration of olfactory bulb interneurons. Semin Cell Dev Biol 8:207–213

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629–634

    CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683–686

    Article  CAS  PubMed  Google Scholar 

  • Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474–476

    Article  CAS  PubMed  Google Scholar 

  • Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353–363

    CAS  PubMed  Google Scholar 

  • Antypa M, Faux C, Eichele G, Parnavelas John G, Andrews WD (2011) Differential gene expression in migratory streams of cortical interneurons. Eur J Neurosci 34:1584–1594

    Article  PubMed Central  PubMed  Google Scholar 

  • Ballard WW, Mellinguer J, Lechenault H (1993) A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318–336

    Article  Google Scholar 

  • Balthazart J, Boseret G, Konkle ATM, Hurley LL, Ball GF (2008) Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC. Eur J Neurosci 27:801–817

    Article  PubMed  Google Scholar 

  • Barker JM, Boonstra R, Wojtowicz JM (2011) From pattern to purpose: how comparative studies contribute to understanding the function of adult neurogenesis. Eur J Neurosci 34:963–977

    Article  PubMed  Google Scholar 

  • Berninger B, Guillemot F, Götz M (2007) Directing neurotransmitter identity of neurones derived from expanded adult neural stem cells. Eur J Neurosci 25:2581–2590

    Article  PubMed  Google Scholar 

  • Brill MS (2008) Regionalization of adult neurogenesis: The role of the transcription factors Dlx2 and Pax6 in the murine subependymal zone. Doctoral thesis. Ludwig-Maximilians-Universität München, Germany

  • Brill MS, Snapyan M, Wohlfrom H, Ninkovic J, Jawerka M, Mastick GS, Ashery-Padan R, Saghatelyan A, Berninger B, Götz M (2008) A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J Neurosci 28:6439–6452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Broglio C, Gómez A, Durán E, Ocaña FM, Jiménez-Moya F, Rodríguez F, Salas C (2005) Hallmarks of a common forebrain vertebrate plan: specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish. Brain Res Bull 66:277–281

    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 467:1–10

    Article  CAS  PubMed  Google Scholar 

  • Bulchand S, Subramanian L, Tole S (2003) Dynamic spatiotemporal expression of LIM genes and cofactors in the embryonic and postnatal cerebral cortex. Dev Dyn 226:460–469

    Article  CAS  PubMed  Google Scholar 

  • Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy. In: evolution and adaptation. 2nd ed. Wiley-Liss, Hoboken, NJ

  • Byrd CA, Brunjes PC (2001) Neurogenesis in the olfactory bulb of adult zebrafish. Neuroscience 105:793–801

    Article  CAS  PubMed  Google Scholar 

  • Candal EM, Caruncho HJ, Sueiro C, Anadón R, Rodríguez-Moldes I (2005) Reelin expression in the retina and optic tectum of developing common brown trout. Dev Brain Res 154:187–197

    Article  CAS  Google Scholar 

  • Carney RSE, Bystron I, López-Bendito G, Molnár Z (2007) Comparative analysis of extra-ventricular mitoses at early stages of cortical development in rat and human. Brain Struct Funct 212:37–54

    Article  PubMed  Google Scholar 

  • Carrera I, Ferreiro-Galve S, Sueiro C, Anadón R, Rodríguez-Moldes I (2008) Tangentially migrating GABAergic cells of subpallial origin invade massively the pallium in developing sharks. Brain Res Bull 75:405–409

    Article  CAS  PubMed  Google Scholar 

  • Carrera I, Anadón R, Rodríguez-Moldes I (2012) Development of tyrosine hydroxylase-immunoreactive cell populations and fiber pathways in the brain of the dogfish Scyliorhinus canicula: new perspectives on the evolution of the vertebrate catecholaminergic system. J Comp Neurol 520:3574–3603

    Article  CAS  PubMed  Google Scholar 

  • Cobos I, Puelles L, Martínez S (2001) The avian telencephalic subpallium originates inhibitory neurons that invade tangentially the pallium (dorsal ventricular ridge and cortical areas). Dev Biol 239:30–45

    Article  CAS  PubMed  Google Scholar 

  • Compagnucci C, Debiais M, Coolen M, Fish J, Griffin JN, Bertocchini F, Minoux M, Rijli FM, Borday-Birraux V, Casane D, Mazan S, Depew MJ (2013) Pattern and polarity in the development and evolution of the Gnathostome jaw: both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Dev Biol 377:428–448

    Article  CAS  PubMed  Google Scholar 

  • Coolen M, Sauka-Spengler T, Nicolle D, Le-Mentec C, Lallemand Y, Da Silva C, Plouhinec JL, Robert B, Wincker P, Shi DL, Mazan S (2007) Evolution of axis specification mechanisms in jawed vertebrates: insights from a chondrichthyan. PLoS One 2(2):e374

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Coolen M, Menuet A, Chassoux D, Compagnucci C, Henry S, Lévèque L, Da Silva C, Gavory F, Samain S, Wincker P, Thermes C, D’Aubenton-Carafa Y, Rodríguez-Moldes I, Naylor G, Depew M, Sourdaine P, Mazan S (2009) The dogfish Scyliorhinus canicula, a reference in jawed vertebrates. In: Behringer RR, Johnson AD, Krumlauf RE, editors. Emerging model organisms. A laboratory manual. Vol. 1. Cold Spring Harbor, NY: CSHL Press pp 431-446

  • Corbin JG, Nery S, Fishell G (2001) Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat Neurosci 4:1177–1182

    Article  CAS  PubMed  Google Scholar 

  • Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtås S, Van Roon-Mom WMC, Björk-Eriksson T, Nordborg C, Frisén J, Dragunow M, Faull RLM, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249

    Article  CAS  PubMed  Google Scholar 

  • De Carlos JA, López-Mascaraque L, Valverde F (1996) Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16:6146–6156

    PubMed  Google Scholar 

  • De Chevigny A, Core N, Follert P, Wild S, Bosio A, Yoshikawa K, Cremer H, Beclin C (2012) Dynamic expression of the pro-dopaminergic transcription factors Pax6 and Dlx2 during postnatal olfactory bulb neurogenesis. Front Cell Neurosci 6:6

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dhaliwal J, Lagace DC (2011) Visualization and genetic manipulation of adult neurogenesis using transgenic mice. Eur J Neurosci 33:1025–1036

    Article  PubMed  Google Scholar 

  • Doetsch F (2002) Challenges for brain repair : insights from adult neurogenesis in birds and mammals. Brain Behav Evol 58:306–322

    Article  Google Scholar 

  • Englund C, Fink A, Lau C, Pham D, Daza RA, Bulfone A, Kowalczyk T, Hevner RF (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247–251

    Article  CAS  PubMed  Google Scholar 

  • Ferrando S, Gallus L, Gambardella C, Ghigliotti L, Ravera S, Vallarino M, Vacchi M, Tagliafierro G (2010) Cell proliferation and apoptosis in the olfactory epithelium of the shark Scyliorhinus canicula. J Chem Neuroanat 40:293–300

    Article  CAS  PubMed  Google Scholar 

  • Ferreiro-Galve S, Rodríguez-Moldes I, Anadón R, Candal E (2010) Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas. J Chem Neuroanat 39:1–14

    Article  PubMed  Google Scholar 

  • Ferreiro-Galve S, Candal E, Rodríguez-Moldes I (2012a) Dynamic expression of pax6 in the shark olfactory system: evidence for the presence of pax6 cells along the olfactory nerve pathway. J Exp Zool 318:79–90

    Article  CAS  Google Scholar 

  • Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2012b) Pax6 expression during retinogenesis in sharks: comparison with markers of cell proliferation and neuronal differentiation. J Exp Zool 318:91–108

    Article  CAS  Google Scholar 

  • Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218:52–61

    Article  CAS  PubMed  Google Scholar 

  • Font E, Desfilis E, Pérez-Cañellas MM, García-Verdugo JM (2002) Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav Evol 58:276–295

    Article  Google Scholar 

  • Gadisseux JF, Goffinet AM, Lyon G, Evrard P (1992) The human transient subpial granular layer: an optical, immunohistochemical, and ultrastructural analysis. J Comp Neurol 324:94–114

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Verdugo JM, Llahi S, Ferrer I, Lopez-Garcia C (1989) Postnatal neurogenesis in the olfactory bulbs of a lizard: a tritiated thymidine autoradiographic study. Neurosci Lett 98:247–252

    Article  CAS  PubMed  Google Scholar 

  • Grandel H, Kaslin J, Ganz J, Wenzel I, Brand M (2006) Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295:263–277

    Article  CAS  PubMed  Google Scholar 

  • Guerrero-Cázares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, García-Verdugo JM, Quinoñes-Hinojosa A (2011) Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol 519:1165–1180

    Article  PubMed  Google Scholar 

  • Hack MA, Saghatelyan A, De Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Götz M (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8:865–872

    Article  CAS  PubMed  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360

    Article  CAS  PubMed  Google Scholar 

  • Hodge RD, Kahoud RJ, Hevner RF (2012) Transcriptional control of glutamatergic differentiation during adult neurogenesis. Cell Mol Life Sci 69:2125–2134

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hofmann MH, Northcutt RG (2012) Forebrain organization in elasmobranchs. Brain Behav Evol 80:142–151

    Article  PubMed  Google Scholar 

  • Humphrey T (1940) The development of the olfactory and the accessory olfactory formations in human embryos and fetuses. J Comp Neurol 73:431–468

    Article  Google Scholar 

  • Jiménez D, López-Mascaraque LM, Valverde F, De Carlos JA (2002) Tangential migration in neocortical development. Dev Biol 244:155–169

    Article  PubMed  CAS  Google Scholar 

  • Kam M, Curtis MA, McGlashan SR, Connor B, Nannmark U, Faull RL (2009) The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat 37:196–205

    Article  CAS  PubMed  Google Scholar 

  • Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363:101–122

    Article  PubMed Central  PubMed  Google Scholar 

  • Kempermann G (2012) New neurons for “survival of the fittest”. Nat Rev Neurosc 13:727–736

    CAS  Google Scholar 

  • Kishimoto N, Alfaro-Cervello C, Shimizu K, Asakawa K, Urasaki A, Nonaka S, Kawakami K, Garcia-Verdugo JM, Sawamoto K (2011) Migration of neuronal precursors from the telencephalic ventricular zone into the olfactory bulb in adult zebrafish. J Comp Neurol 519:3549–3565

    Article  CAS  PubMed  Google Scholar 

  • Kohwi M, Osumi N, Rubenstein JLR, Alvarez-Buylla A (2005) Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25:6997–7003

    Article  CAS  PubMed  Google Scholar 

  • LaDage LD, Roth TC, Pravosudov VV (2011) Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.). Proc Biol Sci 278:138–143

    Article  PubMed Central  PubMed  Google Scholar 

  • Lanuza E, Novejarque A, Moncho-Bogani J, Hernández A, Martínez-García F (2002) Understanding the basic circuitry of the cerebral hemispheres: the case of lizards and its implications in the evolution of the telencephalon. Brain Res Bull 57:471–473

    Article  PubMed  Google Scholar 

  • Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881–7888

    CAS  PubMed  Google Scholar 

  • Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148

    Article  CAS  PubMed  Google Scholar 

  • Lois C, García-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981

    Article  CAS  PubMed  Google Scholar 

  • Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL (2007) Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27:3230–3243

    Article  CAS  PubMed  Google Scholar 

  • Marín O, Rubenstein JL (2003) Cell migration in the forebrain. Annu Rev Neurosci 26:441–483

    Article  PubMed  CAS  Google Scholar 

  • Marín O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063–6076

    PubMed  Google Scholar 

  • Martínez-de-la-Torre M, Pombal MA, Puelles L (2011) Distal-less-like protein distribution in the larval lamprey forebrain. Neuroscience 178:270–284

    Article  PubMed  CAS  Google Scholar 

  • McManus KJ, Hendzel MJ (2006) The relationship between histone H3 phosphorylation and acetylation throughout the mammalian cell cycle. Biochem Cell Biol 84:640–657

    Article  CAS  PubMed  Google Scholar 

  • Medina L, Abellán A (2009) Development and evolution of the pallium. Semin Cell Dev Biol 20:698–711

    Article  PubMed  Google Scholar 

  • Meléndez-Ferro M, Pérez-Costas E, Villar-Cheda B, Abalo XM, Rodríguez-Muñoz R, Rodicio MC, Anadón R (2002) Ontogeny of gamma-aminobutyric populations in the forebrain and midbrain of the sea lamprey. J Comp Neurol 376:360–376

    Article  Google Scholar 

  • Mendoza-Torreblanca JG, Martínez-Martínez E, Tapia-Rodríguez M, Ramírez-Hernández R, Gutiérrez-Ospina G (2008) The rostral migratory stream is a neurogenic niche that predominantly engenders periglomerular cells: in vivo evidence in the adult rat brain. Neurosci Res 60:289–299

    Article  PubMed  Google Scholar 

  • Métin C, Alvarez C, Moudoux D, Vitalis T, Pieau C, Molnár Z (2007) Conserved pattern of tangential neuronal migration during forebrain development. Development 134:2815–2827

    Article  PubMed  CAS  Google Scholar 

  • Meyer G, Soria JM, Martínez-Galán JR, Martín-Clemente B, Fairén A (1998) Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol 397:493–518

    Article  CAS  PubMed  Google Scholar 

  • Ming G-L, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morante-Oria J, Carleton A, Ortino B, Kremer EJ, Fairén A, Lledo PM (2003) Subpallial origin of a population of projecting pioneer neurons during corticogenesis. Proc Natl Acad Sci USA 100:12468–12473

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moreno N, González A, Rétaux S (2008) Evidences for tangential migrations in Xenopus telencephalon: developmental patterns and cell tracking experiments. Dev Neurobiol 68:504–520

    Article  PubMed  Google Scholar 

  • Moreno N, González A, Rétaux S (2009) Development and evolution of the subpallium. Semin Cell Dev Biol 20:735–743

    Article  PubMed  Google Scholar 

  • Mueller T, Wullimann MF, Guo SU (2008) Early teleostean basal ganglia development visualized by zebrafish GAD67 gene expression. J Comp Neurol 507:1245–1257

    Article  CAS  PubMed  Google Scholar 

  • Nityanandam A, Parthasarathy S, Tarabykin V (2012) Postnatal subventricular zone of the neocortex contributes GFAP + cells to the rostral migratory stream under the control of Sip1. Dev Biol 366:341–356

    Article  CAS  PubMed  Google Scholar 

  • Pencea V, Luskin MB (2003) Prenatal development of the rodent rostral migratory stream. J Comp Neurol 463:402–418

    Article  PubMed  Google Scholar 

  • Pérez-Costas E (2002). Expresión y distribución de reelina en el sistema nervioso central de la lamprea de mar. Doctoral thesis, University of Santiago de Compostela, Spain

  • Pérez-Costas E, Meléndez-Ferro M, Santos Y, Anadón R, Rodicio MC, Caruncho HJ (2002) Reelin immunoreactivity in the larval sea lamprey brain. J Chem Neuroanat 23:211–221

    Article  PubMed  Google Scholar 

  • Pérez-García CG, González-Delgado FJ, Suárez-Solá ML, Castro-Fuentes R, Martín-Trujillo JM, Ferres-Torres R, Meyer G (2001) Reelin-immunoreactive neurons in the adult vertebrate pallium. J Chem Neuroanat 21:41–51

    Article  PubMed  Google Scholar 

  • Plachez C, Puche AC (2012) Early specification of GAD67 subventricular derived olfactory interneurons. J Mol Histol 43:215–221

    Article  CAS  PubMed  Google Scholar 

  • Pleasure SJ, Anderson S, Hevner R, Bagri A, Marín O, Lowenstein DH, Rubenstein JL (2000) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727–740

    Article  CAS  PubMed  Google Scholar 

  • Porteus MH, Bulfone A, Liu JK, Puelles L, Lo LC, Rubenstein JL (1994) Dlx-2, Mash-l, and Map-2 expression and bromodeoxyuridine incorpkation define molecularl and distinct cell population and in the embryonic mouse forebrain. J Neurosci 14:6370–6383

    CAS  PubMed  Google Scholar 

  • Puelles L, Rubenstein JL (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469–476

    Article  CAS  PubMed  Google Scholar 

  • Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438

    Article  CAS  PubMed  Google Scholar 

  • Quintana-Urzainqui I, Sueiro C, Carrera I, Ferreiro-Galve S, Santos-Durán G, Pose-Méndez S, Mazan S, Candal E, Rodríguez-Moldes I (2012a) Contributions of developmental studies in the dogfish Scyliorhinus canicula to the brain anatomy of elasmobranchs: insights on the basal ganglia. Brain Behav Evol 80:127–141

    Article  PubMed  Google Scholar 

  • Quintana-Urzainqui I, Rodríguez-Moldes I, Candal E (2012b) Developmental, tract-tracing and immunohistochemical study of the peripheral olfactory system in a basal vertebrate: insights on Pax6 neurons migrating along the olfactory nerve. Brain Struct Funct. doi:10.1007/s00429-012-0486-2

    PubMed Central  PubMed  Google Scholar 

  • Ramirez-Castillejo C, Nacher J, Molowny A, Ponsoda X, Lopez-Garcia C (2002) PSA-NCAM immunocytochemistry in the cerebral cortex and other telencephalic areas of the lizard Podarcis hispanica: differential expression during medial cortex neuronal regeneration. J Comp Neurol 453:145–156

    Article  PubMed  Google Scholar 

  • Rétaux S, Rogard M, Bach I, Failli V, Besson MJ (1999) Lhx9: a novel LIM homeodomain gene expressed in the developing forebrain. J Neurosci 19:783–793

    PubMed  Google Scholar 

  • Rodríguez F, López JC, Vargas JP, Broglio C, Gómez Y, Salas C (2002) Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish. Brain Res Bull 57:499–503

    Article  PubMed  Google Scholar 

  • Rodríguez-Moldes I (2009) A developmental approach to forebrain organization in elasmobranchs: new perspectives on the regionalization of the telencephalon. Brain Behav Evol 74:20–29

    Article  PubMed  Google Scholar 

  • Rodríguez-Moldes I, Ferreiro-Galve S, Carrera I, Sueiro C, Candal E, Mazan S, Anadón R (2008) Development of the cerebellar body in sharks: spatiotemporal relations of Pax6 expression, cell proliferation and differentiation. Neurosci Lett 432:105–110

    Article  PubMed  CAS  Google Scholar 

  • Sanai N, Tramontin AD, Quiñones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-García Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744

    Article  CAS  PubMed  Google Scholar 

  • Sanai N, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2007) Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science 318:393

    Article  CAS  PubMed  Google Scholar 

  • Smeets WJ (1983) The secondary olfactory connections in two chondrichthians, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 218:334–344

    Article  CAS  PubMed  Google Scholar 

  • Smeets WJ (1998) Cartilaginous fish. In: Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrates, vol 1. Springer-Verlag, Berlin, pp 551–654

    Chapter  Google Scholar 

  • Smeets WJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes: Structure and functional correlations. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Srivastava UC, Maurya RC, Chand P (2009) Cyto-architecture and neuronal types of the dorsomedial cerebral cortex of the common Indian wall lizard, Hemidactylus flaviviridis. Arch Ital Biol 147:21–35

    CAS  PubMed  Google Scholar 

  • Stenman J, Toresson H, Campbell K (2003) Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167–174

    CAS  PubMed  Google Scholar 

  • Stühmer T, Puelles L, Ekker M, Rubenstein JLR (2002) Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12:75–85

    Article  PubMed  Google Scholar 

  • Sueiro C (2003) Estudio inmunohistoquímico de los sistemas gabaérgicos del sistema nervioso central de peces elasmobranquios y su relación con sistemas catecolaminérgicos y peptidérgicos. Doctoral Thesis. Universidade de Santiago de Compostela, Spain

  • Sueiro C, Carrera I, Molist P, Rodríguez-Moldes I, Anadón R (2004) Distribution and development of glutamic acid decarboxylase immunoreactivity in the spinal cord of the dogfish Scyliorhinus canicula (elasmobranchs). J Comp Neurol 478:189–206

    Article  PubMed  Google Scholar 

  • Sueiro C, Carrera I, Ferreiro S, Molist P, Adrio F, Anadón R, Rodríguez-Moldes I (2007) New insights on Saccus vasculosus evolution: a developmental and immunohistochemical study in elasmobranchs. Brain Behav Evol 70:187–204

    Article  PubMed  Google Scholar 

  • Tucker ES, Polleux F, LaMantia A-S (2006) Position and time specify the migration of a pioneering population of olfactory bulb interneurons. Dev Biol 297:387–401

    Article  CAS  PubMed  Google Scholar 

  • Tuorto F, Alifragis P, Failla V, Parnavelas JG, Gulisano M (2003) Tangential migration of cells from the basal to the dorsal telencephalic regions in the chick. Eur J Neurosci 18:3388–3393

    Article  CAS  PubMed  Google Scholar 

  • Wasowicz M, Ward R, Repérant J (1999) An investigation of astroglial morphology in Torpedo and Scyliorhinus. J Neurocytol 28:639–653

    Article  CAS  PubMed  Google Scholar 

  • Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759–3771

    CAS  PubMed  Google Scholar 

  • Wu S, Esumi S, Watanabe K, Chen J, Nakamura KC, Nakamura K, Kometani K, Minato N, Yanagawa Y, Akashi K, Sakimura K, Kaneko T, Tamamaki N (2011) Tangential migration and proliferation of intermediate progenitors of GABAergic neurons in the mouse telencephalon. Development 138:2499–2509

    Article  CAS  PubMed  Google Scholar 

  • Wullimann MF (2009) Secondary neurogenesis and telencephalic organization in zebrafish and mice: a brief review. Integr Zool 4:123–133

    Article  PubMed  Google Scholar 

  • Yáñez J, Folgueira M, Köhler E, Martínez C, Anadón R (2011) Connections of the terminal nerve and the olfactory system in two galeomorph sharks: an experimental study using a carbocyanine dye. J Comp Neurol 519:3202–3217

    Article  PubMed  Google Scholar 

  • Zupanc GKH, Hinsch K, Gage FH (2005) Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488:290–319

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Prof. Dr. R. Anadón for the valuable comments made during the preparation of this paper and his critical reading of the manuscript. This work was supported by grants from the Spanish Dirección General de Investigación-FEDER (BFU2010- 15816), the Xunta de Galicia (10PXIB200051PR, CN 2012/237), and European Community-Research Infrastructure Action under the FP7 ‘‘Capacities’’ Specific Programme (ASSEMBLE 227799).

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Authors and Affiliations

  1. Departamento de Biología Celular y Ecología, Edificio CIBUS, Campus Vida, University of Santiago de Compostela, 15782, Santiago de Compostela, Spain

    Idoia Quintana-Urzainqui, Isabel Rodríguez-Moldes & Eva Candal

  2. UMR7150, UPMC Université Paris 6, CNRS, Université Européenne de Bretagne, UMR 7150, SBR, Roscoff, France

    Sylvie Mazan

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  1. Idoia Quintana-Urzainqui
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  2. Isabel Rodríguez-Moldes
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  3. Sylvie Mazan
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  4. Eva Candal
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Corresponding author

Correspondence to Eva Candal.

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Online Resource 1 Video showing a three-dimensional reconstruction of the telencephalon and the distribution of the different streams at stage 31 of development. The rostral-most sections were not included in the reconstruction process and, as a result, the rostral-end of the lateral ventricles appears opened in the final reconstruction.

Online Resource 2 Video showing a three-dimensional reconstruction of the telencephalon and the distribution of the different streams at stage 32 of development.

Supplementary material 1 (MP4 3308 kb)

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Quintana-Urzainqui, I., Rodríguez-Moldes, I., Mazan, S. et al. Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications. Brain Struct Funct 220, 2905–2926 (2015). https://doi.org/10.1007/s00429-014-0834-5

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  • DOI: https://doi.org/10.1007/s00429-014-0834-5

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