The complexity of the calretinin-expressing progenitors in the human cerebral cortex

Frontiers in Neuroanatomy

Volumn 8, Issue AUG, 2014, Pages

  Radonjić, Nevena V ^a,b   Ortega, Juan A ^a   Memi, Fani ^a   Dionne, Krista ^a   Jakovcevski, Igor ^c,d   Zecevic, Nada ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Cortical development; Cortical interneurons; GABA; Gsx2; Transcription factors

Indexed keywords

4 AMINOBUTYRIC ACID; CALRETININ; CD15 ANTIGEN; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; CYCLOPAMINE; LIPID BINDING PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; SONIC HEDGEHOG PROTEIN; SP8 TRANSCRIPTION FACTOR; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR NKX2.1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANTIBODY LABELING; ARTICLE; BRAIN CORTEX; CELL PROLIFERATION; CONTROLLED STUDY; ECHOGRAPHY; FEMALE; FETUS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION; GSX2 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOMAGNETIC SEPARATION; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; NEURAL STEM CELL; NEUROPATHOLOGY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SENSITIVITY AND SPECIFICITY; TELENCEPHALON; WESTERN BLOTTING;

EID: 84919837379     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00082     Document Type: Article

References (84)

1. Alcántara, S., Ferrer, I., and Soriano, E. (1993). Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat. Embryol. (Berl.) 188, 63-73. doi: 10.1007/BF00191452
2. Al-Jaberi, N., Lindsay, S., Sarma, S., Bayatti, N., and Clowry, G. J. (2013). The early fetal development of human neocortical GABAergic interneurons. Cereb. Cortex doi: 10.1093/cercor/bht254 [Epub ahead of print].
3. Anderson, S. A., Eisenstat, D. D., Shi, L., and Rubenstein, J. L. R. (1997). Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476. doi: 10.1126/science.278.5337.474
4. Baraban, S. C., and Tallent, M. K. (2004). Interneuron diversity series: interneuronal neuropeptides-endogenous regulators of neuronal excitability. Trends Neurosci. 27, 135-142. doi: 10.1016/j.tins.2004.01.008
5. Bayatti, N., Moss, J. A., Sun, L., Ambrose, P., Ward, J. F. H., Lindsay, S., et al. (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 xone. Cereb. Cortex 18, 1536-1548. doi: 10.1093/cercor/bhm184
6. Borello, U., Madhavan, M., Vilinsky, I., Faedo, A., Pierani, A., Rubenstein, J., et al. (2013). Sp8 and COUP-TF1 reciprocally regulate patterning and Fgf signaling in cortical progenitors. Cereb. Cortex 24, 1409-1421. doi: 10.1093/cercor/bhs412
7. Brandt, M. D., Jessberger, S., Steiner, B., Kronenberg, G., Reuter, K., Bick-Sander, A., et al. (2003). Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol. Cell. Neurosci. 24, 603-613. doi: 10.1016/S1044-7431(03)00207-0
8. Brun, A. (1965). The subpial granular layer of the foetal cerebral cortex in man. Its ontogeny and significance in congenital cortical malformations. Acta Pathol. Microbiol. Scand. 179, 3-98.
9. Butt, S. J. B., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J. G., et al. (2005). The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48, 591-604. doi: 10.1016/j.neuron.2005.09.034
10. Cai, Y., Zhang, Y., Shen, Q., Rubenstein, J. L., and Yang, Z. (2013). A subpopulation of individual neural progenitors in the mammalian dorsal pallium generates both projection neurons and interneurons in vitro. Stem Cells 31, 1193-1201. doi: 10.1002/stem.1363
11. Carney, R. S., Mangin, J. M., Hayes, L., Mansfield, K., Sousa, V. H., Fishell, G., et al. (2010). Sonic hedgehog expressing and responding cells generate neuronal diversity in the medial amygdala. Neural Dev. 5, 14. doi: 10.1186/1749-8104-5-14
12. Condé, F., Lund, J., Jacobowitz, D., Baimbridge, K., and Lewis, D. (1994). Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J. Comp. Neurol. 341, 95-116. doi: 10.1002/cne.903410109
13. Corbin, J. G., Rutlin, M., Gaiano, N., and Fishell, G. (2003). Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning. Development 130, 4895-4906. doi: 10.1242/dev.00717
14. Dahmane, N., and Ruiz-i-Altaba, A. (1999). Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100.
15. DeFelipe, J. (1997). Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 14, 1-19. doi: 10.1016/S0891-0618(97)10013-8
16. DeFelipe, J. (1999). Chandelier cells and epilepsy. Brain 122, 1807-1822. doi: 10.1093/brain/122.10.1807
17. DeFelipe, J., Alonso-Nanclares, L., and Arellano, J. (2002). Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31, 299-316. doi: 10.1023/A:1024130211265
18. DeFelipe, J., Ballesteros-Yáñez, I., Inda, M. C., and Muñoz, A. (2006). "Double-bouquet cells in the monkey and human cerebral cortex with special reference to areas 17 and 18, " in Progress in Brain Research, eds S. Martinez-Conde, S. L. Macknik, L. M. Martinez, J.-M. Alonso, and P. U. Tse (Amsterdam: Elsevier), 15-32.
19. DeFelipe, J., González-Albo, M. C., Del Río, M. R., and Elston, G. N. (1999). Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J. Comp. Neurol. 412, 515-526. doi: 10.1002/(SICI)1096-9861(19990927)412:3<515::AID-CNE10>3.0.CO;2-1
20. Del Río, M. R., and DeFelipe, J. (1994). A study of SMI 32-stained pyramidal cells, parvalbumin-immunoreactive chandelier cells, and presumptive thalamocortical axons in the human temproal neocortex. J. Comp. Neurol. 342, 389-408. doi: 10.1002/cne.903420307
21. Fogarty, M., Grist, M., Gelman, D., Marín, O., Pachnis, V., and Kessaris, N. (2007). Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935-10946. doi: 10.1523/JNEUROSCI.1629-07.2007
22. Gabbott, P. L. A., Jays, P. R. L., and Bacon, S. J. (1997). Calretinin neurons in human medial prefrontal cortex (areas 24a, b, c, 32', and 25). J. Comp. Neurol. 381, 389-410. doi: 10.1002/(SICI)1096-9861(19970519)381:4<389::AID-CNE1>3.0.CO;2-Z
23. Gadisseux, J., Goffinet, A., Lyon, G., and Evrard, P. (1992). The human transient subpial granular layer: an optical, immunohistochemical, and ultrastructural analysis. J. Comp. Neurol. 324, 94-114. doi: 10.1002/cne.903240108
24. González-Gómez, M., and Meyer, G. (2014). Dynamic expression of calretinin in embryonic and early fetal human cortex. Front. Neuroanat. 8:41. doi: 10.3389/fnana.2014.00041
25. Grateron, L., Cebada-Sanchez, S., Marcos, P., Mohedano-Moriano, A., Insausti, A., Muñoz, M., et al. (2003). Postnatal development of calcium-binding proteins immunoreactivity (parvalbumin, calbindin, calretinin) in the human entorhinal cortex. J. Chem. Neuroanat. 26, 311-316. doi: 10.1016/j.jchemneu.2003.09.005
26. Hansen, D., Lui, J., Flandin, P., Yoshikawa, K., Rubenstein, J., Alvarez-Buylla, A., et al. (2013). Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat. Neurosci. 16, 1576-1587. doi: 10.1038/nn.3541
27. Hansen, D., Lui, J., Parker, P., and Kriegstein, A. R. (2010). Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554-561. doi: 10.1038/nature08845
28. Hill, R. S., and Walsh, C. A. (2005). Molecular insights into human brain evolution. Nature 437, 64-67. doi: 10.1038/nature04103
29. Hsieh-Li, H. M., Witte, D. P., Szucsik, J. C., Weinstein, M., Li, H., and Potter, S. S. (1995). Gsh-2, a murine homeobox gene expressed in the developing brain. Mech. Dev. 50, 177-186. doi: 10.1016/0925-4773(94)00334-J
30. Jakovcevski, I., Mayer, N., and Zecevic, N. (2011). Multiple origins of human neocortical interneurons are supported by distinct expression of transcription factors. Cereb. Cortex 21, 1771-1782. doi: 10.1093/cercor/bhq245
31. Jones, E. G. (2009). The origins of cortical interneurons: mouse versus monkey and human. Cereb. Cortex 19, 1953-1956. doi: 10.1093/cercor/bhp088
32. Kanatani, S., Yozu, M., Tabata, H., and 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. doi: 10.1523/JNEUROSCI.2132-08.2008
33. Kohtz, J. D., Baker, D. P., Corte, G., and Fishell, G. (1998). Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to Sonic hedgehog. Development 125, 5079-5089.
34. Letinic, K., Zoncu, R., and Rakic, P. (2002). Origin of GABAergic neurons in the human neocortex. Nature 417, 645-649. doi: 10.1038/nature00779
35. Lewis, D. A., Hashimoto, T., and Volk, D. W. (2005). Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324. doi: 10.1038/nrn1648
36. Lui, J. H., Hansen, D. V., and Kriegstein, A. R. (2011). Development and evolution of the human neocortex. Cell 146, 18-36. doi: 10.1016/j.cell.2011.06.030
37. Ma, T., Wang, C., Wang, L., Zhou, X., Tian, M., Zhang, Q., et al. (2013). Subcortical origins of human and monkey neocortical interneurons. Nat. Neurosci. 16, 1588-1597. doi: 10.1038/nn.3536
38. Ma, T., Zhang, Q., Cai, Y., You, Y., Rubenstein, J. L. R., and Yang, Z. (2012). A subpopulation of dorsal lateral/caudal ganglionic eminence-derived neocortical interneurons expresses the transcription factor Sp8. Cereb. Cortex 22, 2120-2130. doi: 10.1093/cercor/bhr296
39. Mariani, J., Simonini, M. V., Palejev, D., Tomasini, L., Coppola, G., Szekely, A. M., et al. (2012). Modeling human cortical development in vitro using induced pluripotent stem cells. Proc. Natl. Acad. Sci. U.S.A. 109, 12770-12775. doi: 10.1073/pnas.1202944109
40. Marin, O. (2012). Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120. doi: 10.1038/nrn3155
41. Marin, O., and Rubenstein, J. L. (2001). A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 11, 780-790. doi: 10.1038/35097509
42. Maroof, A., Keros, S., Tyson, J., Ying, S., Ganat, Y., Merkle, F., et al. (2013). Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12, 559-572. doi: 10.1016/j.stem.2013.04.008
43. Meyer, G., Schaaps, J. P., Moreau, L., and Goffinet, A. M. (2000). Embryonic and early fetal development of the human neocortex. J. Neurosci. 20, 1858-1868.
44. Meyer, G., and 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. doi: 10.1046/j.1460-9568.1999.00818.x
45. Mione, M., Danevic, C., Boardman, P., Harris, B., and Parnavelas, J. (1994). Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons. J. Neurosci. 14, 107-123.
46. Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., et al. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582-1594. doi: 10.1523/JNEUROSCI.4515-09.2010
47. Mo, Z., Moore, A. R., Filipovic, R., Ogawa, Y., Kazuhiro, I., Antic, S. D., et al. (2007). Human cortical neurons originate from radial glia and neuron-restricted progenitors. J. Neurosci. 27, 4132-4145. doi: 10.1523/JNEUROSCI.0111-07.2007
48. Mo, Z., and Zecevic, N. (2008). Is Pax6 critical for neurogenesis in the human fetal brain? Cereb. Cortex 18, 1455-1465. doi: 10.1093/cercor/bhm181
49. Nery, S., Wichterle, H., and Fishell, G. (2001). Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540.
50. O'Leary, D. D., and Sahara, S. (2008). Genetic regulation of arealization of the neocortex. Curr. Opin. Neurobiol. 18, 90-100. doi: 10.1016/j.conb.2008.05.011
51. Ortega, J., Radonjic, N., and Zecevic, N. (2013). Sonic hedgehog promotes generation and maintenance of human forebrain Olig2 progenitors. Front. Cell. Neurosci. 7:254. doi: 10.3389/fncel.2013.00254
52. Pappas, I. S., and Parnavelas, J. G. (1998). Basic fibroblast growth factor promotes the generation and differentiation of calretinin neurons in the rat cerebral cortex in vitro. Eur. J. Neurosci. 10, 1436-1445. doi: 10.1046/j.1460-9568.1998.00147.x
53. Parnavelas, J. G. (2000). The origin and migration of cortical neurones: new vistas. Trends Neurosci. 23, 126-131. doi: 10.1016/S0166-2236(00)01553-8
54. Petanjek, Z., Berger, B., and Esclapez, M. (2009a). Origins of cortical GABAergic neurons in the cynomolgus monkey. Cereb. Cortex 19, 249-262. doi: 10.1093/cercor/bhn078
55. Petanjek, Z., Kostovic, I., and Esclapez, M. (2009b). Primate-specific origins and migration of cortical GABAergic neurons. Front. Neuroanat. 3:26. doi: 10.3389/neuro.05.026.2009
56. Petilla Interneuron Nomenclature Group1, Ascoli, G., Alonso-Nanclares, L., Anderson, S., Barrionuevo, G., Benavides-Piccione, R., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi: 10.1038/nrn2402
57. Porter, J. T., Cauli, B., Staiger, J. F., Lambolez, B., Rossier, J., and Audinat, E. (1998). Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur. J. Neurosci. 10, 3617-3628. doi: 10.1046/j.1460-9568.1998.00367.x
58. Radonjic, N., Memi, F., Ortega, J., Glidden, N., Zhang, H., and Zecevic, N. (in press). The role of Sonic hedgehog in the specification of human cortical progenitors in vitro. Cereb. Cortex
59. Rakic, P. (2009). Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724-735. doi: 10.1038/nrn2719
60. Rakic, S., and Zecevic, N. (2003). Emerging complexity of layer I in human cerebral cortex. Cereb. Cortex 13, 1072-1083. doi: 10.1093/cercor/13.10.1072
61. Reinchisi, G., Ijichi, K., Glidden, N., Jakovcevski, I., and Zecevic, N. (2012). COUP-TFII expressing interneurons in human fetal forebrain. Cereb. Cortex 22, 2820-2830. doi: 10.1093/cercor/bhr359
62. Sahara, S., Kawakami, Y., Izpisua Belmonte, J., and O'leary, D. D. M. (2007). Sp8 exhibits reciprocal induction with Fgf8 but has an opposing effect on anterior-posterior cortical area patterning. Neural Dev. 2, 10. doi: 10.1186/1749-8104-2-10
63. Schlösser, B., Klausa, G., Prime, G., and Ten Bruggencate, G. (1999). Postnatal development of calretinin-and parvalbumin-positive interneurons in the rat neostriatum: an immunohistochemical study. J. Comp. Neurol. 405, 185-198. doi: 10.1002/(SICI)1096-9861(19990308)405:2<185::AID-CNE4>3.0.CO;2-B
64. Smart, I. H. M., Dehay, C., Giroud, P., Berland, M., and Kennedy, H. (2002). 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 12, 37-53. doi: 10.1093/cercor/12.1.37
65. Stenman, J., Toresson, H., and 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.
66. Sussel, L., Marin, O., Kimura, S., and Rubenstein, J. L. (1999). Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359-3370.
67. Tamamaki, N., Fujimori, K. E., and Takauji, R. (1997). Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J. Neurosci. 17, 8313-8323.
68. Ulfig, N. (2001). Expression of calbindin and calretinin in the human ganglionic eminence. Pediatr. Neurol. 24, 357-360. doi: 10.1016/S0887-8994(01)00263-6
69. Waclaw, R., Allen, Z., Bell, S., Erdelyi, F., Szabo, G., Potter, S., et al. (2006). The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49, 503-516. doi: 10.1016/j.neuron.2006.01.018
70. Waclaw, R. R., Wang, B., Pei, Z., Ehrman, L. A., and Campbell, K. (2009). Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 63, 451-465. doi: 10.1016/j.neuron.2009.07.015
71. Wang, B., Waclaw, R., Allen, Z., Guillemot, F., and Campbell, K. (2009). Ascl1 is a required downstream effector of Gsx gene function in the embryonic mouse telencephalon. Neural Dev. 4, 5. doi: 10.1186/1749-8104-4-5
72. Wu, S., Esumi, S., Watanabe, K., Chen, J., Nakamura, K. C., Nakamura, K., et al. (2011). Tangential migration and proliferation of intermediate progenitors of GABAergic neurons in the mouse telencephalon. Development 138, 2499-2509. doi: 10.1242/dev.063032
73. Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L., and Anderson, S. A. (2004). Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612-2622. doi: 10.1523/JNEUROSCI.5667-03.2004
74. Xu, Q., Guo, L., Moore, H., Waclaw, R. R., Campbell, K., and Anderson, S. A. (2010). Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 65, 328-340. doi: 10.1016/j.neuron.2010.01.004
75. Xu, Q., Wonders, C. P., and Anderson, S. A. (2005). Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon. Development 132, 4987-4998. doi: 10.1242/dev.02090
76. Yan, Y., Van Brederode, J., and Hendrickson, A. (1995). Developmental changes in calretinin expression in GABAergic and nonGABAergic neurons in monkey striate cortex. J. Comp. Neurol. 363, 78-92. doi: 10.1002/cne.903630108
77. Yan, Y., Winarto, A., Mansjoer, I., and Hendrickson, A. (1996). Parvalbumin, calbindin, and calretinin mark distinct pathways during development of monkey dorsal lateral geniculate nucleus. J. Neurobiol. 31, 189-209. doi: 10.1002/(SICI)1097-4695(199610)31:2<189::AID-NEU5>3.0.CO;2-7
78. Yozu, M., Tabata, H., and 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. doi: 10.1523/JNEUROSCI.2072-05.2005
79. Yu, X., and Zecevic, N. (2011). Dorsal radial glial cells have the potential to generate cortical interneurons in human but not in mouse brain. J. Neurosci. 31, 2413-2420. doi: 10.1523/JNEUROSCI.5249-10.2011
80. Zaitsev, A. V., Gonzalez-Burgos, G., Povysheva, N. V., Kröner, S., Lewis, D. A., and Krimer, L. S. (2005). Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb. Cortex 15, 1178-1186. doi: 10.1093/cercor/bhh218
81. Zecevic, N., Chen, Y., and Filipovic, R. (2005). Contributions of cortical subventricular zone to the development of the human cerebral cortex. J. Comp. Neurol. 491, 109-122. doi: 10.1002/cne.20714
82. Zecevic, N., Hu, F., and Jakovcevski, I. (2011). Interneurons in the developing human neocortex. Dev. Neurobiol. 71, 18-33. doi: 10.1002/dneu.20812
83. Zecevic, N., Milosevic, A., Rakic, S., and Marin-Padilla, M. (1999). Early development and composition of the human primordial plexiform layer: an immunohistochemical study. J. Comp. Neurol. 412, 241-254. doi: 10.1002/(SICI)1096-9861(19990920)412:2<241::AID-CNE5>3.0.CO;2-X
84. Zecevic, N., and Rakic, P. (2001). Development of layer I neurons in the primate cerebral cortex. J. Neurosci. 21, 5607-5619.