Sequence of neuron origin and neocortical laminar fate: Relation to cell cycle of origin in the developing murine cerebral wall

Journal of Neuroscience

Volumn 19, Issue 23, 1999, Pages 10357-10371

  Takahashi, Takao ^a,b   Goto, T ^a,b   Miyama, S ^a,b   Nowakowski, R S ^c   Caviness Jr , V S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

Cell cycle; Neocortical histogenesis; Neuronogenesis; Neuronogenetic sequence; Pseudostratified ventricular epithelium (PVE); Transverse neuronogenetic gradient

Indexed keywords

ARTICLE; BRAIN DEVELOPMENT; CELL CYCLE; CELL CYCLE S PHASE; CONTROLLED STUDY; HISTOGENESIS; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

EID: 0033492989     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-23-10357.1999     Document Type: Article

References (72)

1. Alexiades M, Cepko C (1997) Subsets of retinal progenitors display temporally regulated and distinct biases in the fates of their progeny. Development 124:1119-1131.
2. Anderson S, Eisenstat D, Shi L, Rubenstein J (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
3. Angevine J (1965) Time of neuron origin in the hippocampal region: an autoradiographic study in the mouse. Exp Neurol [Suppl] 2:1-71.
4. Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of the cerebral cortex in the mouse. Nature 192:766-768.
5. Bayer SA, Altman J (1991) Neocortical development. New York: Raven.
6. Bisconte J-C, Marty R (1975a) Analyse chronoarchitectonique du cerveau de rat par radioautographie. I. Histogenese du telencephale. J Hirnforsch 16:55-74.
7. Bisconte J-C, Marty R (1975b) Etude quantitative du marquage radioautographique dans le systeme nerveux du rat. II. Caracteristiques finales dans le cerveau de l'animal adulte. Exp Brain Res 22:37-56.
8. Bourgeois J-P, Rakic P (1993) Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13:2801-2860.
9. Bourgeois J-P, Goldman-Rakic PS, Rakic P (1994) Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4:78-96.
10. Cai L, Hayes N, Nowakowski R (1997) Local homogeneity of cell cycle length in developing mouse cortex. J Neurosci 17:2079-2087.
11. Caviness Jr VS (1975) Architectonic map of neocortex of the normal mouse. J Comp Neurol 164:247-263.
12. Caviness Jr VS (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Dev Brain Res 4:293-302.
13. Caviness Jr VS, Rakic P (1978) Mechanisms of cortical development: a view from mutations in mice. Annu Rev Neurosci 1:297-326.
14. Caviness Jr VS, Takahashi T, Nowakowski R (1995) Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci 18:379-383.
15. Caviness Jr VS, Takahashi T, Nowakowski R (1999) Neuronogenesis and the early events of neocortical histogenesis. In: Development of the neocortex (Goffinet A, Rakic P, eds). Berlin: Springer, in press.
16. Chang W, Harris W (1998) Sequential genesis and determination of cone and rod photoreceptors in Xenopus. J Neurobiol 35:227-244.
17. De Carlos JA, Lopez-Mascaraque L, Valverde F (1996) Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16:6146-6156.
18. Dehay C, Giroud P, Berland M, Smart I, Kennedy H (1993) Modulation of the cell cycle contributes to the parcellation of the primate visual cortex. Nature 366:464-466.
19. Fernandez V, Bravo H (1974) Autoradiographic study of the cerebral cortex in the rabbit. Brain Behav Evol 9:317-332.
20. Ferrar I, Soriano E, Del Rio JA, Alcantara S, Auladell C (1992) Cell death and removal in the cerebral cortex during development. Prog Neurobiol 39:1-43.
21. Finlay BL, Pallas SL (1989) Control of cell number in the developing mammalian visual system. Prog Neurobiol 32:207-234.
22. Finlay BL, Slattery M (1983) Local differences in the amount of early cell death in neocortex predict adult local specializations. Science 219:1349-1351.
23. Goto T, Caviness VS Jr, Nowakowski R, Takahashi T (1999) Altered pattern of neuron production in p27kip1 knockout mouse (p27ko). Soc Neurosci Abstr 25:1541.
24. Granger B, Tekaia F, Le Sourd A, Rakic P, Bourgeois J-P (1995) Tempo of neurogenesis and Synaptogenesis in the primate cingulate mesocortex: comparison with the neocortex. J Comp Neurol 360:363-376.
25. Hayes N, Nowakowski R (1999) Exploiting the dynamics of S-phase tracers in developing brain: interkinetic nuclear migration for cells entering vs leaving the S-phase. Dev Neurosci, in press.
26. Hicks SP, D'Amato CJ (1968) Cell migration to the isocortex in the rat. Anat Rec 160:619-634.
27. Kornack DR, Rakic P (1995) Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15:311-321.
28. Kornack D, Rakic P (1998) Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci USA 95:1242-1246.
29. Lavdas A, Grigoriou M, Pachnis V, Parnavelas J (1998) The medial ganglionic eminence is a source of the early neurons of the developing cerebral cortex. Soc Neurosci Abstr 24:282.
30. Leuba G, Heumann D, Rabinowicz T (1977) Postnatal development of the mouse cerebral neocortex. I. Quantitative cytoarchitectonics of some motor and sensory areas. J Hirnforsch 18:461-481.
31. Luskin MB, Shatz CJ (1985) Neurogenesis of the cat's primary visual cortex. J Comp Neurol 242:611-631.
32. McConnell SK (1988) Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J Neurosci 8:945-974.
33. McConnell SK (1989) The determination of neuronal fate in the cerebral cortex. Trends Neurosci 12:342-349.
34. McConnell SK (1991) The generation of neuronal diversity in the central nervous system. Ann Rev Neurosci 14:269-300.
35. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
36. McSherry GM (1984) Mapping of cortical histogenesis in the ferret. J Embryol Exp Morphol 81:239-252.
37. McSherry GM, Smart IHM (1986) Cell production gradients in the developing ferret isocortex. J Anat 1-14.
38. Meyer G, Soria J, Martinez-G, Talan J, Marrtin-Clemente B, Fairen 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.
39. Miller M (1995) Relationship of the time of origin and death of neurons in rat somatosensory cortex: barrel versus septal cortex and projection versus local circuit neurons. J Comp Neurol 355:6-14.
40. Mione MC, Danevic C, Boardman P, Harris B, Parnavelas JG (1994) Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons. J Neurosci 14:107-123.
41. Mione MC, Cavanagh J, Harris B, Parnavelas J (1997) Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J Neurosci 17:2018-2029.
42. Misson J-P, Austin C, Takahashi T, Cepko C, Caviness Jr VS (1991) The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. Cereb Cortex 1:221-229.
43. Miyama S, Takahashi T, Nowakowski RS, Caviness Jr VS (1997) A gradient in the duration of the G1 phase in the murine neocortical proliferative epithelium. Cereb Cortex 7:678-689.
44. Perron M, Kanekar S, Vetter M, Harris W (1998) The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev Biol 199:185-200.
45. Pinto-Lord MC, Caviness Jr VS (1979) Determinants of cell shape and orientation: a comparative Golgi analysis of cell-axon interrelationships in the developing neocortex of normal and reeler mice. J Comp Neurol 187:49-69.
46. Polleux F, Dehay C, Kennedy H (1997a) The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J Comp Neurol 385:95-116.
47. Polleux F, Dehay C, Moraillon B, Kennedy H (1997b) Regulation of neuroblast cell-cycle kinetics plays a crucial role in the generation of unique features of neocortical areas. J Neurosci 17:7763-7783.
48. Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61-84.
49. Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425-427.
50. Rakic P (1976) Differences in the time of origin and in eventual distribution of neurons in areas 17 and 18 of visual cortex in Rhesus monkey. Exp Brain Res [Suppl] 1:244-248.
51. Rakic P (1978) Neuronal migration and contact guidance in the primate telencephalon. Postgrad Med J 54:25-40.
52. Rakic P (1981) Developmental events leading to laminar and areal organization of the neocortex. In: The organization of the cerebral cortex (Schmitt FO, Worden FG, Adelman G, Dennis SG, eds), pp 7-28. Cambridge, MA: MIT.
53. Rakic P (1982) Early developmental events: cell lineages, acquisition of neuronal positions and areal and laminar development. Neurosci Res Prog Bull 20:439-452.
54. Rakic P, Bourgeois J-P, Goldman-Rakic PS (1994) Synaptic development of the cerebral cortex: implications for learning, memory and mental illness. In: The self-organizing brain: from growth cones to functional networks (van Pelt J, Corner MA, Uylings HBM, Lopes da Silva FH, eds), pp 227-243. Amsterdam: Elsevier.
55. Rice FL, van der Loos H (1977) Development of barrels and barrel field in the somatosensory cortex of the mouse. J Comp Neurol 171:545-560.
56. Sauer FC (1935) Mitosis in the neural tube. J Comp Neurol 62:377-405.
57. Schüz A, Palm G (1989) Density of neurons and synapses in the cerebral cortex of the mouse. J Comp Neurol 286:442-455.
58. Sidman RL (1970) Autoradiographic methods and principles for study of the nervous system with thymidine-H3. In: Contemporary research methods in neuroanatomy (Nauta WJH, Ebbesson SOE, eds), pp 252-274. New York: Springer.
59. Sidman RL, Miale IL, Feder N (1959) Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol 1:322-333.
60. Smart IHM, McSherry GM (1982) Growth patterns in the lateral wall of the mouse telencephalon. II. Histological changes during and subsequent to the period of isocortical neuron production. J Anat 131:415-442.
61. Smart IHM, Smart M (1982) Growth patterns in the lateral wall of the mouse telencephalon. I. Autoradiographic studies of the histogenesis of the iso-cortex and adjacent areas. J Anat 134:273-298.
62. Spreafico R, Frassoni C, Arcelli P, Selvaggio M, De Biasi S (1995) In situ labeling of apoptotic cell death in the cerebral cortex and thalamus of rats during development. J Comp Neurol 363:281-295.
63. Takahashi T, Nowakowski R, Caviness Jr VS (1992) BUdR as an S-phase marker for quantitative studies of cytokinetic behaviour in the murine cerebral ventricular zone. J Neurocytol 21:185-197.
64. Takahashi T, Tsai L-H, Harlow E, Caviness Jr VS (1993) Cyclin dependent kinases in the developing nervous system. Soc Neurosci Abstr 19:30.
65. Takahashi T, Nowakowski R, Caviness Jr VS (1994) Mode of cell proliferation in the developing mouse neocortex. Proc Natl Acad Sci USA 91:375-379.
66. Takahashi T, Nowakowski R, Caviness Jr VS (1995) The cell cycle of the pseudostratified ventricular epithelium of the murine cerebral wall. J Neurosci 15:6046-6057.
67. Takahashi T, Nowakowski R, Caviness Jr VS (1996a) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general computational model of neocortical neuronogenesis. J Neurosci 16:6181-6196.
68. Takahashi T, Nowakowski RS, Caviness Jr VS (1996b) Interkinetic and migratory behavior of a cohort of neocortical neurons arising in the early embryonic murine cerebral wall. J Neurosci 16:5762-5776.
69. Tamamaki N, Fujimori K, Kakauji R (1997) Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17:8313-8323.
70. Theiler K (1972) The house mouse. Development and normal stages from fertilization to 4 weeks of age. Berlin: Springer.
71. Verney C, Takahashi T, Bhide PG, Nowakowski RS, Caviness Jr VS (1999) Independent controls for neocortical neuron production and histogenetic cell death. Dev Neurosci, in press.
72. Walsh C, Cepko C (1990) Cell lineage and cell migration in the developing cerebral cortex. Experientia 46:940-947.