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e-Neuroforum

, Volume 7, Issue 4, pp 82–88 | Cite as

Cajal-Retzius cells: organizers of cortical development

  • Werner Kilb
  • Michael Frotscher
Review article

Abstract

Cajal-Retzius cells (CRc) are a major neuronal population in the marginal zones of the developing neocortex and hippocampus. CRc belong to the earliest born neurons in the cortex and originate from several regions at the pallial-subpallial border. A substantial fraction of CRc disappears during postnatal development. CRc express a variety of neurotransmitter receptors, receive mainly GABAergic synaptic inputs and give rise to glutamatergic synapses. Recent studies identified some modes of how CRc are integrated into immature neuronal circuits, although their exact role for immature information processing remains unknown. As a major source for the extracellular matrix protein reelin, which is critically involved in lamination of the cerebral cortex, CRc are an important factor for the structural development of the neocortex and hippocampus. In addition, CRc contribute to the patterning of cortical areas and shape the development of perforant path connections in the hippocampus. In summary, CRc are a major cellular element in the structural development of the cerebral cortex and may serve as a link between early electrical activity and morphological organization during prenatal und early postnatal development.

Keywords

Cortical development Neuronal migration Marginal zone Reelin Hippocampus Neocortex 

Notes

Acknowledgements

The authors thank all colleagues who dedicated their research to Cajal-Retzius cells. We apologize that we were not able to include all relevant publications on this topic due to space limitations. We thank our coworkers and the funding agencies, especially the Deutsche Forschungsgemeinschaft, for continuous support.

References

  1. 1.
    Aboitiz F, Montiel J (2007) Origin and evolution of the vertebrate telencephalon, with special reference to the mammalian neocortex. Adv Anat Embryol Cell Biol 193:1–112CrossRefPubMedGoogle Scholar
  2. 2.
    Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J, Fukuda A, Luhmann HJ, Kilb W (2007) Kinetic properties of Cl− uptake mediated by Na+-dependent K+-2Cl(−) cotransport in immature rat neocortical neurons. J Neurosci 27:8616–8627CrossRefPubMedGoogle Scholar
  3. 3.
    Alcantara S, Ruiz M, D’Arcangelo G, Ezan F, De Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779–7799PubMedGoogle Scholar
  4. 4.
    Anstoetz M, Cosgrove KE, Hack I, Mugnaini E, Maccaferri G, Luebke JH (2013) Morphology, input-output relations and synaptic connectivity of Cajal-Retzius cells in layer 1 of the developing neocortex of CXCR4-EGFP mice. Brain Struct Funct 2:1–21Google Scholar
  5. 5.
    Anstoetz M, Huang H, Marchionni I, Haumann I, Maccaferri G, Luebke JHR (2016) Developmental profile, morphology, and synaptic connectivity of Cajal-Retzius cells in the postnatal mouse hippocampus. Cereb Cortex 26:855–872Google Scholar
  6. 6.
    Barber M, Arai Y, Morishita Y, Vigier L, Causeret F, Borello U, Ledonne F, Coppola E, Contremoulins V, Pfrieger FW, Tissir F, Govindan S, Jabaudon D, Proux-Gillardeaux V, Galli T, Pierani A (2015) Migration speed of Cajal-Retzius cells modulated by vesicular trafficking controls the size of higher-order cortical areas. Curr Biol 25:2466–2478CrossRefPubMedGoogle Scholar
  7. 7.
    Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A (2005) Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8:1002–1012CrossRefPubMedGoogle Scholar
  8. 8.
    Blanquie O, Liebmann L, Hubner CA, Luhmann HJ, Sinning A (2016) NKCC1-mediated GABAergic signaling promotes postnatal cell death in neocortical Cajal-Retzius cells. Cereb Cortex. doi: 10.1093/cercor/bhw004 PubMedGoogle Scholar
  9. 9.
    Borrell V, Ruiz M, Del Río JA, Soriano E (1999) Development of commissural connections in the hippocampus of reeler mice: evidence of an inhibitory influence of Cajal-Retzius cells. Exp Neurol 156:268–282CrossRefPubMedGoogle Scholar
  10. 10.
    Cajal SR (1891) Sur la structure de lecorce cerebrale de quelques mammiferes. Cellule 7:123–176Google Scholar
  11. 11.
    Ceranik K, Deng JB, Heimrich B, Lübke J, Zhao ST, Förster E, Frotscher M (1999) Hippocampal Cajal-Retzius cells project to the entorhinal cortex: retrograde tracing and intracellular labelling studies. Eur J Neurosci 11:4278–4290CrossRefPubMedGoogle Scholar
  12. 12.
    Chai X, Förster E, Zhao S, Bock HH, Frotscher M (2009) Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n‑cofilin phosphorylation at serine3. J Neurosci 29:288–299CrossRefPubMedGoogle Scholar
  13. 13.
    Chai X, Fan L, Shao H, Lu X, Zhang W, Li J, Wang J, Chen S, Frotscher M, Zhao S (2015) Reelin induces branching of neurons and radial glial cells during corticogenesis. Cereb Cortex 25:3640–3653CrossRefPubMedGoogle Scholar
  14. 14.
    Chowdhury TG, Jimenez JC, Bomar JM, Cruz-Martin A, Cantle JP, Portera-Cailliau C (2010) Fate of Cajal-Retzius neurons in the postnatal mouse neocortex. Front Neuroanat 4:10PubMedPubMedCentralGoogle Scholar
  15. 15.
    Cosgrove KE, Maccaferri G (2012) mGlu1 alpha-dependent recruitment of excitatory GABAergic input to neocortical Cajal-Retzius cells. Neuropharmacology 63:486–493CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    D’Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719–723CrossRefPubMedGoogle Scholar
  17. 17.
    Del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E (1995) Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 5:13–21CrossRefPubMedGoogle Scholar
  18. 18.
    Del Rio JA, Heimrich B, Borrell V, Förster E, Drakew A, Alcántara S, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Derer P, Frotscher M, Soriano E (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70–74CrossRefPubMedGoogle Scholar
  19. 19.
    Derer P, Derer M (1990) Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36:839–856CrossRefPubMedGoogle Scholar
  20. 20.
    Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES (2000) Reelin binds α3β1integrin and inhibits neuronal migration. Neuron 27:33–44CrossRefPubMedGoogle Scholar
  21. 21.
    Dvorzhak A, Unichenko P, Kirischuk S (2012) Glutamate transporters and presynaptic metabotropic glutamate receptors protect neocortical Cajal-Retzius cells against over-excitation. Pflugers Arch 464:217–225CrossRefPubMedGoogle Scholar
  22. 22.
    Falconer DS (1951) Two new mutants ‘trembler’ and ‘reeler’ with neurological actions in the house mouse. J Genet 50:192–201CrossRefPubMedGoogle Scholar
  23. 23.
    Forster E, Zhao ST, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259–267CrossRefPubMedGoogle Scholar
  24. 24.
    Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Müller U (2011) Reelin Regulates Cadherin Function via Dab1/Rap1 to Control Neuronal Migration and Lamination in the Neocortex. Neuron 69(3):482–497CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Frotscher M (2010) Role for Reelin in stabilizing cortical architecture. Trends Neurosci 33:407–414CrossRefPubMedGoogle Scholar
  26. 26.
    Frotscher M, Haas CA, Förster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13:634–640CrossRefPubMedGoogle Scholar
  27. 27.
    Frotscher M, Chai XJ, Bock HH, Haas CA, Forster E, Zhao ST (2009) Role of Reelin in the development and maintenance of cortical lamination. J Neural Transm 116:1451–1455CrossRefPubMedGoogle Scholar
  28. 28.
    Gil-Sanz C, Franco SJ, Martinez-Garay I, Espinosa A, Harkins-Perry S, Muller U (2013) Cajal-Retzius cells instruct neuronal migration by coincidence signaling between secreted and contact-dependent guidance cues. Neuron 79:461–477CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Gil V, Nocentini S, Del Rio JA (2014) Historical first descriptions of Cajal-Retzius cells: from pioneer studies to current knowledge. Front Neuroanat 8:32CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Griveau A, Borello U, Causeret F, Tissir F, Boggetto N, Karaz S, Pierani A (2010) A novel role for Dbx1-derived Cajal-Retzius cells in early regionalization of the cerebral cortical neuroepithelium. PLOS Biol 8:e1000440CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    von Haebler D, Stabel J, Draguhn A, Heinemann U (1993) Properties of horizontal cells transiently appearing in the rat dentate gyrus during ontogenesis. Exp Brain Res 94:33–42CrossRefGoogle Scholar
  32. 32.
    Gu XC, Liu B, Wu XJ, Yan Y, Zhang Y, Wei YQ, Pleasure SJ, Zhao CJ (2011) Inducible genetic lineage tracing of cortical hem derived Cajal-Retzius cells reveals novel properties. PLOS ONE 6:e28653CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hamburgh M (1963) Analysis of postnatal developmental effects of reeler, a neurological mutation in mice - a study in developmental genetics. Dev Biol 8:165CrossRefPubMedGoogle Scholar
  34. 34.
    Hestrin S, Armstrong WE (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16:5290–5300PubMedGoogle Scholar
  35. 35.
    Hevner RF, Neogi T, Englund C, Daza RA, Fink A (2003) Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Dev Brain Res 141:39–53CrossRefGoogle Scholar
  36. 36.
    Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481–489CrossRefPubMedGoogle Scholar
  37. 37.
    Honda T, Kobayashi K, Mikoshiba K, Nakajima K (2011) Regulation of cortical neuron migration by the Reelin signaling pathway. Neurochem Res 36:1270–1279CrossRefPubMedGoogle Scholar
  38. 38.
    Ina A, Sugiyama M, Konno J, Yoshida S, Ohmomo H, Nogami H, Shutoh F, Hisano S (2007) Cajal-Retzius cells and subplate neurons differentially express vesicular glutamate transporters 1 and 2 during development of mouse cortex. Eur J Neurosci 26:615–623CrossRefPubMedGoogle Scholar
  39. 39.
    Janusonis S, Gluncic V, Rakic P (2004) Early serotonergic projections to Cajal-Retzius cells: relevance for cortical development. J Neurosci 24:1652–1659CrossRefPubMedGoogle Scholar
  40. 40.
    Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert DR, Goffinet AM (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 24:514–521CrossRefPubMedGoogle Scholar
  41. 41.
    Judas M, Sedmak G, Pletikos M (2010) Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974). J Anat 217:344–367CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48CrossRefPubMedGoogle Scholar
  43. 43.
    Kilb W, Luhmann HJ (2000) Characterization of a hyperpolarization-activated inward current in Cajal-Retzius cells in rat neonatal neocortex. J Neurophysiol 84:1681–1691PubMedGoogle Scholar
  44. 44.
    Kilb W, Luhmann HJ (2001) Spontaneous GABAergic postsynaptic currents in Cajal-Retzius cells in neonatal rat cerebral cortex. Eur J Neurosci 13:1387–1390CrossRefPubMedGoogle Scholar
  45. 45.
    Kilb W, Ikeda M, Uchida K, Okabe A, Fukuda A, Luhmann HJ (2002) Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 112:299–307CrossRefPubMedGoogle Scholar
  46. 46.
    Kilb W, Hartmann D, Saftig P, Luhmann HJ (2004) Altered morphological and electrophysiological properties of Cajal-Retzius cells in cerebral cortex of embryonic Presenilin-1 knockout mice. Eur J Neurosci 20:2749–2756CrossRefPubMedGoogle Scholar
  47. 47.
    Kirischuk S, Luhmann HJ, Kilb W (2014) Cajal-Retzius cells: update on structural and functional properties of these mystic neurons that bridged the 20th century. Neuroscience 275:33–46CrossRefPubMedGoogle Scholar
  48. 48.
    Kirmse K, Grantyn R, Kirischuk S (2005) Developmental downregulation of low-voltage-activated Ca2+ channels in Cajal-Retzius cells of the mouse visual cortex. Eur J Neurosci 21:3269–3276CrossRefPubMedGoogle Scholar
  49. 49.
    Kirmse K, Dvorzhak A, Henneberger C, Grantyn R, Kirischuk S (2007) Cajal Retzius cells in the mouse neocortex receive two types of pre- and postsynaptically distinct GABAergic inputs. J Physiol 585:881–895CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Kolbaev SN, Achilles K, Luhmann HJ, Kilb W (2011) Effect of depolarizing GABA(A)-mediated membrane responses on excitability of Cajal-Retzius cells in the immature rat neocortex. J Neurophysiol 106:2034–2044CrossRefPubMedGoogle Scholar
  51. 51.
    Luhmann HJ, Reiprich RA, Hanganu IL, Kilb W (2000) Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. J Neurosci Res 62:574–584CrossRefPubMedGoogle Scholar
  52. 52.
    Ma J, Yao XH, Fu Y, Yu YC (2013) Development of layer 1 neurons in the mouse neocortex. Cereb Cortex 24:2604–2618Google Scholar
  53. 53.
    Marchionni I, Takacs VT, Nunzi MG, Mugnaini E, Miller RJ, Maccaferri G (2010) Distinctive properties of CXC chemokine receptor 4‑expressing Cajal-Retzius cells versus GABAergic interneurons of the postnatal hippocampus. JPhysiol 588:2859–2878CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Magdaleno S, Keshvara L, Curran T (2002) Rescue of ataxia and preplate splitting by ectopic expression of reelin in reeler mice. Neuron 33:573–586CrossRefPubMedGoogle Scholar
  55. 55.
    Marin-Padilla M (1990) Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study. J Comp Neurol 299:89–105CrossRefPubMedGoogle Scholar
  56. 56.
    Marin-Padilla M (1998) Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 21:64–71CrossRefPubMedGoogle Scholar
  57. 57.
    Marin-Padilla M (2015) Human cerebral cortex Cajal-Retzius neuron: development, structure and function. A Golgi study. Front Neuroanat 9:21PubMedPubMedCentralGoogle Scholar
  58. 58.
    Martinez-Cerdeno V, Noctor SC (2014) Cajal, Retzius, and Cajal-Retzius cells. Front Neuroanat 8:48PubMedPubMedCentralGoogle Scholar
  59. 59.
    Martinez-Galan JR, Lopez-Bendito G, Lujan R, Shigemoto R, Fairen A, Valdeolmillos M (2001) Cajal-Retzius cells in early postnatal mouse cortex selectively express functional metabotropic glutamate receptors. Eur J Neurosci 13:1147–1154CrossRefPubMedGoogle Scholar
  60. 60.
    Martinez-Galan JR, Moncho-Bogani J, Caminos E (2014) Expression of calcium-binding proteins in layer 1 Reelin-immunoreactive cells during rat and mouse neocortical development. J Histochem Cytochem 62:60–69CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Meyer G, Goffinet AM (1998) Prenatal development of reelin-immunoreactive neurons in the human neocortex. J Comp Neurol 397:29–40CrossRefPubMedGoogle Scholar
  62. 62.
    Meyer G, Goffinet AM, Fairén A (1999) What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex 9:765–775CrossRefPubMedGoogle Scholar
  63. 63.
    Meyer G, Perez-Garcia CG, Abraham H, Caput D (2002) Expression of p73 and Reelin in the developing human cortex. J Neurosci 22:4973–4986PubMedGoogle Scholar
  64. 64.
    Meyer G, Cabrera SA, Perez Garcia CG, Martinez Millan L, Walker N, Caput D (2004) Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J Neurosci 24:9878–9887CrossRefPubMedGoogle Scholar
  65. 65.
    Mienville JM (1998) Persistent depolarizing action of GABA in rat Cajal-Retzius cells. J Physiol (Lond) 512:809–817CrossRefGoogle Scholar
  66. 66.
    Mienville JM, Barker JL (1997) Potassium current expression during prenatal corticogenesis in the rat. Neuroscience 81:163–172CrossRefPubMedGoogle Scholar
  67. 67.
    Mienville JM, Pesold C (1999) Low resting potential and postnatal upregulation of NMDA receptors may cause Cajal-Retzius cell death. J Neurosci 19:1636–1646PubMedGoogle Scholar
  68. 68.
    Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582–1594CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Muralidhar S, Wang Y, Markram H (2014) Synaptic and cellular organization of layer 1 of the developing rat somatosensory cortex. Front Neuroanat 7:52CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Myakhar O, Unichenko P, Kirischuk S (2011) GABAergic projections from the subplate to Cajal-Retzius cells in the neocortex. Neuroreport 22:525–529CrossRefPubMedGoogle Scholar
  71. 71.
    Ogawa M, Miyata T, Nakajimat K, Yagyu K, Seike M, Ikenaka K et al (1995) The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14(5):899–912CrossRefPubMedGoogle Scholar
  72. 72.
    Perez-Garcia CG, Gonzalez-Delgado FJ, Suarez-Sola ML, Castro-Fuentes R, Martin-Trujillo JM, Ferres-Torres R, Meyer G (2001) Reelin-immunoreactive neurons in the adult vertebrate pallium. J Chem Neuroanat 21:41–51CrossRefPubMedGoogle Scholar
  73. 73.
    Pozas E, Paco S, Soriano E, Aguado F (2008) Cajal-Retzius cells fail to trigger the developmental expression of the Cl(-)extruding co-transporter KCC2. Brain Res 1239:85–91CrossRefPubMedGoogle Scholar
  74. 74.
    Quattrocolo G, Maccaferri G (2013) Novel GABAergic circuits mediating excitation/inhibition of Cajal- Retzius cells in the developing hippocampus. J Neurosci 33:5486–5498CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Quattrocolo G, Maccaferri G (2014) Optogenetic activation of Cajal-Retzius cells reveals their glutamatergic output and a novel feedforward circuit in the developing mouse hippocampus. J Neurosci 34:13018–13032CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Qian TZ, Chen RQ, Nakamura M, Furukawa T, Kumada T, Akita T, Kilb W, Luhmann HJ, Nakahara D, Fukuda A (2014) Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone of neonatal rats. Frontiers Cell Neurosci 8:33CrossRefGoogle Scholar
  77. 77.
    Radnikow G, Feldmeyer D, Lübke J (2002) Axonal projection, input and output synapses, and synaptic physiology of Cajal-Retzius cells in the developing rat neocortex. J Neurosci 22:6908–6919PubMedGoogle Scholar
  78. 78.
    Retzius G (1893) Die Cajal’schen Zellen der Grosshirnrinde beim Menschen und bei Säugetieren. Biol Untersuchungen 5:1–8Google Scholar
  79. 79.
    Sava BA, David CS, Teissier A, Pierani A, Staiger JF, Luhmann HJ, Kilb W (2010) Electrophysiological and morphological properties of Cajal-Retzius cells with different ontogenetic origins. Neuroscience 167:724–734CrossRefPubMedGoogle Scholar
  80. 80.
    Schwartz TH, Rabinowitz D, Unni V, Kumar VS, Smetters DK, Tsiola A, Yuste R (1998) Networks of coactive neurons in developing layer 1. Neuron 20:541–552CrossRefPubMedGoogle Scholar
  81. 81.
    Soda T, Nakashima R, Watanabe D, Nakajima K, Pastan I, Nakanishi S (2003) Segregation and coactivation of developing neocortical layer 1 neurons. J Neurosci 23:6272–6279PubMedGoogle Scholar
  82. 82.
    Soriano E, Del Rio JA (2005) The cells of Cajal-Retzius: still a mystery one century after. Neuron 46:389–394CrossRefPubMedGoogle Scholar
  83. 83.
    Soriano E, Del Rio JA, Martinez A, Super H (1994) Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 342:571–595CrossRefPubMedGoogle Scholar
  84. 84.
    Stanfield BB, Cowan WM (1979) Morphology of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:393–422CrossRefPubMedGoogle Scholar
  85. 85.
    Super H, Martínez A, Del Río JA, Soriano E (1998) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 18:4616–4626PubMedGoogle Scholar
  86. 86.
    Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, Goffinet AM (2009) DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci USA 106:16871–16876CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Tinnes S, Schafer MKE, Flubacher A, Munzner G, Frotscher M, Haas CA (2011) Epileptiform activity interferes with proteolytic processing of Reelin required for dentate granule cell positioning. FASEB J 25:1002–1013CrossRefPubMedGoogle Scholar
  88. 88.
    Trousse F, Poluch S, Pierani A, Dutriaux A, Bock HH, Nagasawa T, Verdier JM, Rossel M (2015) CXCR7 receptor controls the maintenance of subpial positioning of Cajal-Retzius cells. Cereb Cortex 25:3446–3457CrossRefPubMedGoogle Scholar
  89. 89.
    Valverde F, Facal-valverde MV, Santacana M, Heredia M (1989) Development and differentiation of early generated cells of sublayer VIb in the somatosensory cortex of the rat: A correlated Golgi and autoradiographic study. The Journal of Comparative Neurology 290 (1):118–140CrossRefPubMedGoogle Scholar
  90. 90.
    Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133:537–545CrossRefPubMedGoogle Scholar
  91. 91.
    Zecevic N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21:5607–5619PubMedGoogle Scholar
  92. 92.
    Zhao ST, Frotscher M (2010) Go or stop? Divergent roles of reelin in radial neuronal migration. Neuroscientist 16:421–434CrossRefPubMedGoogle Scholar
  93. 93.
    Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117–5125CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Institute of PhysiologyUniversity Medical Center of the Johannes Gutenberg UniversityMainzGermany
  2. 2.Institute for Structural NeurobiologyCenter for Molecular Neurobiology Hamburg (ZMNH)HamburgGermany

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