Interneurons in the developing human neocortex

Developmental Neurobiology

Volumn 71, Issue 1, 2011, Pages 18-33

  Zecevic, Nada ^a   Hu, Frances ^a   Jakovcevski, Igor ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Cerebral cortex; Cortical interneurons; Human fetal brain; Immunohistochemistry

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; CALRETININ; NEUROPEPTIDE Y; PARVALBUMIN; SOMATOSTATIN;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL PROLIFERATION; GANGLION; GESTATION PERIOD; GRANULAR CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTERNEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STEM CELL; SUBVENTRICULAR ZONE;

FETUS; HUMANS; INTERNEURONS; NEOCORTEX; NEURAL STEM CELLS; NEUROGENESIS; SPECIES SPECIFICITY; STEM CELLS; TELENCEPHALON;

EID: 78650047405     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20812     Document Type: Article

References (71)

1. Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney WEJr, Jones EG. 1995. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52: 258-266.
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. 1997. Interneuron migration from basal forebrain to neocortex: Dependence on Dlx genes. Science 278: 474-476.
3. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JLR. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128: 353-363.
4. Baraban SC, Tallent MK. 2004. Interneuron diversity series: Interneuronal neuropeptides-endogenous regulators of neuronal excitability. Trends Neurosci 27: 135-142.
5. Bayatti N, Moss JA, Sun L, Ambrose P, Ward JFH, Lindsay S, Clowry GJ. 2008. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex 18: 1536-1548.
6. Ben-Ari Y. 2002. Excitatory actions of GABA during development: The nature of the nurture. Nat Rev Neurosci 3: 728-739.
7. Brun A. 1965. The subpial granular layer of the fetal cerebral cortex in man. Its ontogeny and significance in congenital cortical malformations. Acta Pathol Microbiol Scand Suppl 179: 1-98.
8. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G. 2005. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48: 591-604.
9. Butt SJB, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G, Kimura S, Fishell G. 2008. The Requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59: 722-732.
10. Cao QL, Yan XX, Luo XG, Garey LJ. 1996. Prenatal development of parvalbumin immunoreactivity in the human striate cortex. Cereb Cortex 6: 620-630.
11. Cherubini E, Gaiarsa JL, Ben-Ari Y. 1991. GABA: An excitatory transmitter in early postnatal life. Trends Neurosci 14: 515-519.
12. DeFelipe J. 1999. Chandelier cells and epilepsy. Brain 122: 1807-1822.
13. DeFelipe J. 2002. Cortical interneurons: From Cajal to 2001. Prog Brain Res 136: 215-238.
14. DeFelipe J, Ballesteros-Yanez I, Inda MC, Munoz A. 2006. Double-bouquet cells in the monkey and human cerebral cortex with special reference to areas 17 and 18. Prog Brain Res 154: 15-32.
15. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nature 8: 438-450.
16. Del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E. 1995. Wide distribution, glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the developing murine cortex as identified with calretinin immunocytochemistry. Cereb Cortex 5: 13-21.
17. Delalle I, Evers P, Kostovic I, Uylings HBM. 1997. Laminar distribution of neuropeptide Y-immunoreactive neurons in human prefrontal cortex during development. J Comp Neurol 379: 515-522.
18. Fertuzinhos S, Krsnik Z, Kawasawa YI, Rasin MR, Kwan KY, Chen JG, Judas M, et al. 2009. Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia. Cereb Cortex 19: 2196-2207.
19. Gabbott PLA, Jays PRL, Bacon SJ. 1997. Calretinin neurons in human medial prefrontal cortex (Areas 24a, b, c, 32, and 25). J Comp Neurol 381: 389-410.
20. 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.
21. Gleeson JG, Walsh CA. 2000. Neuronal migration disorders: From genetic diseases to developmental mechanisms. Trends Neurosci 23: 352-359.
22. Gonchar Y, Burkhalter A. 1997. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7: 347-358.
23. Gonchar Y, Wang Q, Burkhalter A. 2008. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat 1: 1-11.
24. Haydar TF, Wang F, Schwartz ML, Rakic P. 2000. Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20: 5764-5774.
25. Hill RS, Walsh CA. 2005. Molecular insights into human brain evolution. Nature 437: 64-67.
26. Inta D, Alfonso J, von Engelhardt J, Kreuzberg MM, Meyer AH, van Hooft JA, Monyer H. 2008. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA 105: 20994-20999.
27. Jones EG. 2009. The origins of cortical interneurons: Mouse vs. monkey and human. Cereb Cortex 19: 1953-1956.
28. Kanatani S, Yozu M, Tabata H, Nakajima K. 2008. COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J Neurosci 28: 13582-13591.
29. Khazipov R, Luhmann H. 2006. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 29: 414-418.
30. Knable MB. 1999. Schizophrenia and bipolar disorder: Findings from studies of the Stanley Foundation Brain Collection. Schizophr Res 39: 149-152.
31. Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, et al. 2007. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci 27: 6878-6891.
32. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297: 441-470.
33. Kostovic I, Stefulj-Fucic A, Mrzljak L, Jukic S, Delalle I. 1991. Prenatal and perinatal development of the somatostatin-immunoreactive neurons in the human prefrontal cortex. Neurosci Lett 124: 153-156.
34. Letinic K, Zoncu R, Rakic P. 2002. Origin of GABAergic neurons in the human neocortex. Nature 417: 645-649.
35. Levitt P. 2003. Genetic disruption of cortical interneuron development causes region- and GABA cell type specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 23: 622-631.
36. Lewis DA, Hashimoto T, Volk DW. 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6: 312-324.
37. Lewis DA, Levitt P. 2002. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25: 409-432.
38. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M, Kennedy H, et al. 2006. The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas. Cereb Cortex 16 (Suppl 1): 26-34.
39. Marin O, Rubenstein JLR. 2001. A long remarkable journey: Tangential migration in the telencephalon. Nat Rev Neurosci 2: 780-790.
40. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807.
41. Meyer G, Schaaps J-P, Moreau L, Goffinet AM. 2000. Embryonic and early fetal development of the human neocortex. J Neurosci 20: 1858-1868.
42. Meyer G, Wahle P. 1999. The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex. Eur J Neurosci 11: 3937-3944.
43. Miyoshi G, Butt SJ, Takebayashi H, Fishell G. 2007. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 27: 7786-7798.
44. Molnár Z, Métin C, Stoykova A, Tarabykin V, Price DJ, Francis F, Meyer G, et al. 2006. Comparative aspects of cerebral cortical development. Eur J Neurosci 23: 921-934.
45. Nery S, Fishell G, Corbin JG. 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5: 1279-1287.
46. Owens DF, Kriegstein AR. 2002. Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3: 715-727.
47. Parnavelas JG, Anderson SA, Lavdas AA, Grigoriou M, Pachnis V, Rubenstein JL. 2000. The contribution of the ganglionic eminence to the neuronal cell types of the cerebral cortex. Novartis Found Symp 228: 129-139.
48. Petanjek Z, Berger B, Esclapez M. 2009. Origins of cortical GABAergic neurons in the cynomolgus monkey. Cereb Cortex 19: 249-262.
49. Preuss TM, Coleman GQ. 2002. Human-specific organization of primary visual cortex: Alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb Cortex 12: 671-691.
50. Rakic P. 1974. Neurons in rhesus monkey visual cortex: Systematic relation between time of origin and eventual disposition. Science 183: 425-427.
51. Rakic P. 2009. Evolution of the neocortex: A perspective from developmental biology. Nat Rev Neurosci 10: 724-735.
52. Rakic S, Zecevic N. 2003. Emerging complexity of cortical layer I in humans. Cereb Cortex 13: 1072-1083.
53. Smart IHM, Dehay C, Giroud P, Berland M, Kennedy H. 2002. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extra striate cortex in the monkey. Cereb Cortex 12: 37-53.
54. Tamamaki N, Fujimori KE, Takauji R. 1997. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17: 8313-8323.
55. Ulfig N. 2002. Ganglionic eminence of the human fetal brain-new vistas. Anat Rec 267: 191-195.
56. 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.
57. Wonders C, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci 7: 687-696.
58. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. 2004. Origins of cortical interneuron subtypes. J Neurosci 24: 2612-2622.
59. Xu X, Roby K, Callaway EM. 2006. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499: 144-160.
60. Yan XX, Cao QL, Luo XG, Garey LJ. 1997. Prenatal development of calbindin D-28K in human visual cortex. Cereb Cortex 7: 57-62.
61. Yanez IB, Munoz A, Contreras J, Gonzalez J, Rodriguez-Veiga E, DeFelipe J. 2005. Double bouquet cell in the human cerebral cortex and a comparison with other mammals. J Comp Neurol 486: 344-360.
62. Yang Z. 2008. Postnatal subventricular zone progenitors give rise not only to granular and periglomerular interneurons but also to interneurons in the external plexiform layer of the rat olfactory bulb. J Comp Neurol 506: 347-358.
63. Yozu M, Tabata H, Nakajima K. 2005. The caudal migratory stream: A novel migratory stream of interneurons derived from the caudal ganglionic eminence in the developing mouse forebrain. J Neurosci 25: 7268-7277.
64. Yu X, Jakovcevski I, Mo Z, Zecevic N. 2009. Cortical origin of calretinin-expressing neurons in the human fetal forebrain. Program No. 807.12/A12 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience.
65. Zaitsev AV, Gonzalez-Burgos G, Povysheva NV, Kroner S, Lewis DA, Krimer LS. 2005. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb Cortex 15: 1178-1186.
66. Zaitsev AV, Povysheva NV, Gonzalez-Burgos G, Rotaru D, Fish KN, Krimer LS, Lewis DA. 2009. Interneuron diversity in layers 2-3 of monkey prefrontal cortex. Cereb Cortex 19: 1597-1615.
67. Zecevic N. 1998. Synaptogenesis in layer I of the human cerebral cortex in the first half of gestation. Cereb Cortex 8: 245-252.
68. Zecevic N, Chen Y, Filipovic R. 2005. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol 491: 109-122.
69. Zecevic N, Milosevic A. 1997. Initial development of gamma-aminobutyric acid immunoreactivity in the human cerebral cortex. J Comp Neurol 380: 495-506.
70. Zecevic N, Milosevic A, Rakic S, Marin-Padilla M. 1999. The human neocortex: Early development and composition of the primordial plexiform layer. An immunohistochemical study. J Comp Neurol 412: 241-254.
71. Zecevic N, Rakic P. 2001. Development of layer I neurons in the primate cerebral cortex. J Neurosci 21: 5607-5619.