Lineage origins of GABAergic versus glutamatergic neurons in the neocortex

Current Opinion in Neurobiology

Volumn 26, Issue , 2014, Pages 132-141

  Marín, Oscar ^a   Müller, Ulrich ^b  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID DERIVATIVE;

ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; GABAERGIC NEURONS; GLUTAMATES; HUMANS; NEOCORTEX; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84893943964     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.01.015     Document Type: Review

References (67)

1. Greig L.C., Woodworth M.B., Galazo M.J., Padmanabhan H., Macklis J.D. Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 2013, 14:755-769.
2. Franco S.J., Müller U. Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex. Neuron 2013, 77:19-34.
3. DeFelipe J., Lopez-Cruz P.L., Benavides-Piccione R., Bielza C., Larranaga P., Anderson S., Burkhalter A., Cauli B., Fairén A., Feldmeyer D., et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 2013, 14:202-216.
4. Rakic P. Specification of cerebral cortical areas. Science 1988, 241:170-176.
5. Rakic P. The radial edifice of cortical architecture: from neuronal silhouettes to genetic engineering. Brain Res Rev 2007, 55:204-219.
6. Anderson S.A., Eisenstat D.D., Shi L., Rubenstein J.L.R. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997, 278:474-476.
7. Marín O. Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur J Neurosci 2013, 38:2019-2029.
8. Pearson B.J., Doe C.Q. Specification of temporal identity in the developing nervous system. Annu Rev Cell Dev Biol 2004, 20:619-647.
9. Malatesta P., Hartfuss E., Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000, 127:5253-5263.
10. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409:714-720.
11. Miyata T., Kawaguchi A., Okano H., Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001, 31:727-741.
12. Noctor S.C., Martinez-Cerdeno V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004, 7:136-144.
13. Miyata T., Kawaguchi A., Saito K., Kawano M., Muto T., Ogawa M. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004, 131:3133-3145.
14. Haubensak W., Attardo A., Denk W., Huttner W.B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A 2004, 101:3196-3201.
15. Tyler W.A., Haydar T.F. Multiplex genetic fate mapping reveals a novel route of neocortical neurogenesis, which is altered in the Ts65Dn mouse model of Down syndrome. J Neurosci 2013, 33:5106-5119.
16. Stancik E.K., Navarro-Quiroga I., Sellke R., Haydar T.F. Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex. J Neurosci 2010, 30:7028-7036.
17. Gal J.S., Morozov Y.M., Ayoub A.E., Chatterjee M., Rakic P., Haydar T.F. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci 2006, 26:1045-1056.
18. Wu S.X., Goebbels S., Nakamura K., Nakamura K., Kometani K., Minato N., Kaneko T., Nave K.A., Tamamaki N. Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc Natl Acad Sci U S A 2005, 102:17172-17177.
19. Smart I.H., Dehay C., Giroud P., Berland M., Kennedy H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 2002, 12:37-53.
20. Lukaszewicz A., Savatier P., Cortay V., Giroud P., Huissoud C., Berland M., Kennedy H., Dehay C. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 2005, 47:353-364.
21. Hansen D.V., Lui J.H., Parker P.R., Kriegstein A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464:554-561.
22. Fietz S.A., Kelava I., Vogt J., Wilsch-Brauninger M., Stenzel D., Fish J.L., Corbeil D., Riehn A., Distler W., Nitsch R., et al. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 2010, 13:690-699.
23. Wang X., Tsai J.W., LaMonica B., Kriegstein A.R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 2011, 14:555-561.
24. Martínez-Cerdeno V., Cunningham C.L., Camacho J., Antczak J.L., Prakash A.N., Cziep M.E., Walker A.I., Noctor S.C. Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS ONE 2012, 7:e30178.
25. Betizeau M., Cortay V., Dorothee P., Pfister S., Gautier E., Bellemin-Menard A., Afanassieff M., Huissoud C., Douglas R.J., Kennedy H., et al. Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 2013, 80:442-467.
26. Kriegstein A., Noctor S., Martinez-Cerdeno V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 2006, 7:883-890.
27. Zimmer C., Tiveron M.C., Bodmer R., Cremer H. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 2004, 14:1408-1420.
28. Tarabykin V., Stoykova A., Usman N., Gruss P. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 2001, 128:1983-1993.
29. Nieto M., Monuki E.S., Tang H., Imitola J., Haubst N., Khoury S.J., Cunningham J., Gotz M., Walsh C.A. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 2004, 479:168-180.
30. Kowalczyk T., Pontious A., Englund C., Daza R.A., Bedogni F., Hodge R., Attardo A., Bell C., Huttner W.B., Hevner R.F. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 2009, 19:2439-2450.
31. Franco S.J., Gil-Sanz C., Martinez-Garay I., Espinosa A., Harkins-Perry S.R., Ramos C., Müller U. Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 2012, 337:746-749.
32. Guo C., Eckler M.J., McKenna W.L., McKinsey G.L., Rubenstein J.L., Chen B. Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 2013, 80:1167-1174.
33. Arlotta P., Molyneaux B.J., Chen J., Inoue J., Kominami R., Macklis J.D. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 2005, 45:207-221.
34. Srinivasan K., Leone D.P., Bateson R.K., Dobreva G., Kohwi Y., Kohwi-Shigematsu T., Grosschedl R., McConnell S.K. A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc Natl Acad Sci U S A 2012, 109:19071-19078.
35. Deck M., Lokmane L., Chauvet S., Mailhes C., Keita M., Niquille M., Yoshida M., Yoshida Y., Lebrand C., Mann F., et al. Pathfinding of corticothalamic axons relies on a rendezvous with thalamic projections. Neuron 2013, 77:472-484.
36. Bedogni F., Hodge R.D., Elsen G.E., Nelson B.R., Daza R.A., Beyer R.P., Bammler T.K., Rubenstein J.L., Hevner R.F. Tbr1 regulates regional and laminar identity of postmitotic neurons in developing neocortex. Proc Natl Acad Sci U S A 2010, 107:13129-13134.
37. Alcamo E.A., Chirivella L., Dautzenberg M., Dobreva G., Farinas I., Grosschedl R., McConnell S.K. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 2008, 57:364-377.
38. Molyneaux B.J., Arlotta P., Hirata T., Hibi M., Macklis J.D. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 2005, 47:817-831.
39. Chen B., Schaevitz L.R., McConnell S.K. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci U S A 2005, 102:17184-17189.
40. Han W., Kwan K.Y., Shim S., Lam M.M., Shin Y., Xu X., Zhu Y., Li M., Sestan N. TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc Natl Acad Sci U S A 2011, 108:3041-3046.
41. McKenna W.L., Betancourt J., Larkin K.A., Abrams B., Guo C., Rubenstein J.L., Chen B. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci 2011, 31:549-564.
42. Zong H., Espinosa J.S., Su H.H., Muzumdar M.D., Luo L. Mosaic analysis with double markers in mice. Cell 2005, 121:479-492.
43. Gelman D.M., Marín O. Generation of interneuron diversity in the mouse cerebral cortex. Eur J Neurosci 2010, 31:2136-2141.
44. Pilz G.A., Shitamukai A., Reillo I., Pacary E., Schwausch J., Stahl R., Ninkovic J., Snippert H.J., Clevers H., Godinho L., et al. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat Commun 2013, 4:2125.
45. Brown K.N., Chen S., Han Z., Lu C.H., Tan X., Zhang X.J., Ding L., Lopez-Cruz A., Saur D., Anderson S.A., et al. Clonal production and organization of inhibitory interneurons in the neocortex. Science 2011, 334:480-486.
46. Halliday A.L., Cepko C.L. Generation and migration of cells in the developing striatum. Neuron 1992, 9:15-26.
47. Beier K.T., Samson M.E., Matsuda T., Cepko C.L. Conditional expression of the TVA receptor allows clonal analysis of descendents from Cre-expressing progenitor cells. Dev Biol 2011, 353:309-320.
48. Ciceri G., Dehorter N., Sols I., Huang Z.J., Maravall M., Marín O. Lineage-specific laminar organization of cortical GABAergic interneurons. Nat Neurosci 2013, 16:1199-1210.
49. Valcanis H., Tan S.S. Layer specification of transplanted interneurons in developing mouse neocortex. J Neurosci 2003, 23:5113-5122.
50. Fairén A., Cobas A., Fonseca M. Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J Comp Neurol 1986, 251:67-83.
51. Miller M.W. Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex. Brain Res 1985, 355:187-192.
52. Hammond V., So E., Gunnersen J., Valcanis H., Kalloniatis M., Tan S.S. Layer positioning of late-born cortical interneurons is dependent on Reelin but not p35 signaling. J Neurosci 2006, 26:1646-1655.
53. Kriegstein A.R., Noctor S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 2004, 27:392-399.
54. Miyoshi G., Fishell G. GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development. Cereb Cortex 2011, 21:845-852.
55. Pla R., Borrell V., Flames N., Marín O. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J Neurosci 2006, 26:6924-6934.
56. Lodato S., Rouaux C., Quast K.B., Jantrachotechatchawan C., Studer M., Hensch T.K., Arlotta P. Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 2011, 69:763-779.
57. Hevner R.F., Daza R.A., Englund C., Kohtz J., Fink A. Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration. Neuroscience 2004, 124:605-618.
58. Bartolini G., Ciceri G., Marin O. Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults. Neuron 2013, 79:849-864.
59. Miyoshi G., Hjerling-Leffler J., Karayannis T., Sousa V.H., Butt S.J., Battiste J., Johnson J.E., Machold R.P., Fishell G. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 2010, 30:1582-1594.
60. Xu Q., Cobos I., De La Cruz E., Rubenstein J.L., Anderson S.A. Origins of cortical interneuron subtypes. J Neurosci 2004, 24:2612-2622.
61. Walsh C., Cepko C.L. Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 1992, 255:434-440.
62. Walsh C., Cepko C.L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 1993, 362:632-635.
63. Yu Y.C., Bultje R.S., Wang X., Shi S.H. Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 2009, 458:501-504.
64. Torii M., Hashimoto-Torii K., Levitt P., Rakic P. Integration of neuronal clones in the radial cortical columns by EphA and ephrin-A signalling. Nature 2009, 461:524-528.
65. Dimidschstein J., Passante L., Dufour A., van den Ameele J., Tiberi L., Hrechdakian T., Adams R., Klein R., Lie D.C., Jossin Y., et al. Ephrin-b1 controls the columnar distribution of cortical pyramidal neurons by restricting their tangential migration. Neuron 2013, 79:1123-1135.
66. Clandinin T.R., Feldheim D.A. Making a visual map: mechanisms and molecules. Curr Opin Neurobiol 2009, 19:174-180.
67. Li H., Fertuzinhos S., Mohns E., Hnasko T.S., Verhage M., Edwards R., Sestan N., Crair M.C. Laminar and columnar development of barrel cortex relies on thalamocortical neurotransmission. Neuron 2013, 79:970-986.