Evidence for a postnatal doubling of neuron number in the developing human cerebral cortex between 15 months and 6 years

Journal of Theoretical Biology

Volumn 191, Issue 2, 1998, Pages 115-140

  Shankle, W Rodman ^a   Landing, Benjamin H ^b   Rafii, Michael S ^c   Schiano, Allen ^a   Chen, James M ^d   Hara, Junko ^e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c BROWN UNIVERSITY   (United States)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL COUNT; CELL DENSITY; DNA SYNTHESIS; HUMAN; POSTNATAL DEVELOPMENT; PRIMATE; PRIORITY JOURNAL;

MACACA MULATTA; PRIMATES;

EID: 0032554557     PISSN: 00225193     EISSN: None     Source Type: Journal    
DOI: 10.1006/jtbi.1997.0570     Document Type: Article

References (97)

1. ABOVYAN, V. A., ARUTYUNOVA, A. S., GLEZER, I. I. & MOKHOVA, T. M. (1965). The temporal region. In: Development of the Child's Brain. (Sarkisov, S. A. ed.), pp. 109-128. Moscow.
2. ABOVYAN, V. A., GLEZER, I. I. & MOKHOVA, T. M. (1961). The structure of the central and transitional zones of the cortical end of the auditory analyzer. In: The Structure and Functions of Human Analyzers in Ontogenesis. (Sarkisov, S. A. ed.), pp. 202-211. Moscow.
3. ALBERS, K. M., WRIGHT D. E. & DAVIS, B.M. (1994). Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14, 1422-1432.
4. ALTMAN, J. & BAYER, S. A. (1988). The development of neurons. In: Handbook of Human Growth and Developmental Biology (Meisami, E. & Timiras, P. S. eds), Vol 1, pp. 8-9. Boca Raton: CRC Press.
5. BARDGETT, M. E., JACKSON, J. L., TAYLOR, G. T. & CSERNANSKY, J. G. (1995). Kainic acid decreases hippocampal neuron number and increases dopamine receptor binding in the nucleus accumbens: an animal model of schizophrenia. Behav. Brain Res. 70, 153-164.
6. BARTLETT, P. F., DUTTON, R., LIKIARDOPOULOS, V. & BROOKER, G. (1994). Regulation of neurogenesis in the embryonic and adult brain by fibroblast growth factors. Alcohol Alcohol. (Supplement) 2, 387-394.
7. BENSON, D. F. (1994). The Neurology of Thinking. New York: Oxford University Press.
8. BERMINGHAM-MCDONOUGH, O., MCCABE, K. L. & REH, T. A. (1996). Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erb32/neu expression in developing rat retina. Development 122, 1427-1438.
9. Biological Tables (Tabulae biologicae) (1941). Growth of Man, Volume 20.
10. BLINKOV, S. M. & GLEZER, I. I. (1968). The Human Brain in Figures and Tables: A Quantitative Handbook. New York: Plenum.
11. BOURGEOIS, J. P., GOLDMAN-RAKIC, P. S. & RAKIC, P. (1994). Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys. Cerebral Cortex 4, 78-96.
12. BRAAK, H. & BRAAK, E. (1996). Evolution of the neuropathology of Alzheimer's disease. Acta Neurol. Scand. suppl. 165, 3-12.
13. BRAITENBERG, V. & SCHUZ, A. (1991). Anatomy of the Cortex: Statistics and Geometry. Berlin: Springer-Verlag.
14. CAMPLEJOHN, R. S., GELFANT, S., CHALKER, D. & SITTAMPALAM, Y. (1984). Mitotic and labeling activity in normal human epidermis in vivo. Cell Tissue Kinet. 17, 315-322.
15. COGGESHALL, R. E. & LEKAN, H. A. (1996). Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J. Comp. Neurol. 364(1), 6-15.
16. CONEL, J. L. (1939). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Newborn, Volume 1. Cambridge, MA: Harvard University Press.
17. CONEL, J. L. (1941). Postnatal Development of the Human Cerebral Cortex: The Cortex of the One-Month Infant, Volume 2. Cambridge, MA: Harvard University Press.
18. CONEL, J. L. (1947). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Three-Month Infant, Volume 3. Cambridge, MA: Harvard University Press.
19. CONEL, J. L. (1951). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Six-Month Infant, Volume 4. Cambridge, MA: Harvard University Press.
20. CONEL, J. L. (1955). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Fifteen-Month Infant, Volume 5. Cambridge, MA: Harvard University Press.
21. CONEL, J. L. (1959). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Twenty-four-Month Infant, Volume 6. Cambridge, MA: Harvard University Press.
22. CONEL, J. L. (1963). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Forty-eight-Month Infant, Volume 7. Cambridge, MA: Harvard University Press.
23. CONEL, J. L. (1967). Postnatal Development of the Human Cerebral Cortex: The Cortex of the Seventy-two-Month Infant, Volume 8. Cambridge, MA: Harvard University Press.
24. COPPOLETTA, J. M. & WOLBACH, S. B. (1933). Body length and organ weights on infants and children: Study of body lengths and normal weights of more important vital organs of body between birth and 12 years of age. Am. J. Path. 9, 55-70.
25. CRAGG, B.G. (1967). The density of synapses and neurons in the motor and visual areas of the cerebral cortex. J. Anat. 101, 639-654.
26. CRAIG, C. G., TROPEPE, V., MORSHEAD, C. M., REYNOLDS, B. A., WEISS, S. & VAN DER KOOY, D. (1996). In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16, 2649-2658.
27. DIETRICH, D. R., CANDRIAN, R., MARSMAN, D. S., POPP, J. A., JAUFMANN, W. K. & SWENBERG, J. A. (1994). Retrospective assessment of liver cell proliferation via PCNA: a comparison with tritiated thymidine. Cancer Lett. 79, 45-51.
28. DOBBING, J. & SANDS, J. (1970). Timing of neuroblast multiplication in developing human brain. Nature 226, 639-640.
29. DUTRILLAUX, B., HILALI, A., ACHKAR, W. A., MARTINS, B., SABATIER, L., LEONARD, E. D. & LEONARD, A. (1991). Chromosome aberration dosimetry: addition of thymidine, an interesting means to increase the number of dividing cells. Strahlenther Onkol. 167, 319-321.
30. FOLEY, J., TON, T., MARONPOT, R., BUTTERWORTH, B. & GOLDSWORTHY, T. L. (1993). Comparison of Proliferating Cell Nuclear Antigen to tritiated thymidine as a marker of proliferating hepatocytes in rats. Environ. Health Perspect. 101 suppl. 5, 199-205.
31. FUJITA, S. (1962). Kinetics of cellular proliferation. Ex. Cell Res. 28, 52-60.
32. GAGE, F. H., COATES, P. W., PALMER, T. D., KUHN, H. G., FISHER, L. J., SUHONEN, J. O., PETERSON, D. A., SUHR, S. T. & RAY, J. (1995). Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc. Natl Acad. Sci. U.S.A. 92, 11879-11883.
33. GROBSTEIN, P. (1988). On beyond neuronal specificity: Problems in going from cells to networks and from networks to behaviors, In: Advances in Neural and Behavioral Development. (Shinkman, P. ed.), Vol. 3, pp. 1-47. New Jersey: Ablex.
34. HAASKJOLD, E., REFSUM, S. B., BJERKNES, R. & PAULSEN, T. O. (1988). The labelling index is not always reliable. Discrepancies between the labelling index and the mitotic rate in the rat corneal epithelium after intraperitoneal and topical administration of tritiated thymidine and colcemid. Cell Tissue Kinet. 21, 389-394.
35. HAUG, H. (1987). Brain sizes, surfaces and neuronal sizes of the cortex cerebri. A stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupialia, insectivores and one elephant). Am. J. Anat. 180, 126-142.
36. HEDREEN, J. C. (1996). Stereology and counting: estimation of object height in sections; this converts the Linderstrom-Lang/ Abercrombie equation ("Abercrombie correction") to the empirical method equation. Soc. for Neurosci. Abstracts 22, 1239.
37. HENDERSON, G., TOMLINSON, B. E. & GIBSON, P. H. (1980). Cell counts in human cerebral cortex in normal adults throughout life using an image analysing computer. J. Neurol. Sci. 46, 113-136.
38. HENDRY, S., SCHWARK, H., JONES, E. G. & FAN, J. (1987). Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J. Neurosci. 7, 1503-1519.
39. HENERY, C. C. & MAYHEW, T. M. (1989). The cerebrum and cerebellum of the fixed human brain: efficient and unbiased estimates of volumes and cortical surface areas. J. Anat. 167, 167-180.
40. HOY, C. A., LEWIS, E. D. & SCHIMKE, R. T. (1990). Perturbation of DNA replication and cell cycle progression by commonly used [3H] thymidine labeling protocols. Mol. Cell Biol. 10, 1584-1592.
41. HUTTENLOCHER, P. R., DE COURTEN, C., GAREY, L. & VAN DER LOOS, H. (1982). Synaptic development in human cerebral cortex. Int. J. Neur. 16, 144-154.
42. HUTTENLOCHER, P. R. & DE COURTEN, C. (1987). The development of synapses in striate cortex of man. Human Neurobiol. 6, 1-9.
43. HUTTENLOCHER, P. R. (1990). Morphometric study of human cerebral cortex development. Neuropsychologia 28, 517-527.
44. IDE, C. F., SCRIPTER, J. L., COLTMAN, B. W., DOTSON, R. S., SNYDER, D. C. & JELASO, A. (1996). Cellular and molecular correlates to plasticity during recovery from injury in the developing mammalian brain. Prog. Brain Res. 108, 365-377.
45. JACOBSON, M. (1991). Developmental Neurobiology, 3rd Edn, Plenum Press, NY.
46. JERISON, H. J. (1991). Brain size and the evolution of the mind. 59th James Arthur lecture on the evolution of the human brain, 1989. New York: American Museum of Natural History.
47. JOHNSON, M. H. (1996). Developmental Cognitive Neuroscience. 1st Edn, Blackwell Publishers, Cambridge.
48. KEMPERMANN, G., KUHN, H. G., GAGE, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495.
49. KIRSCHENBAUM, B., NEDERGAARD, M., PREUSS, A., BARAMI, K., FRASER, R. A. & GOLDMAN, S. A. (1994). In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain. Cerebral Cortex 4, 576-589.
50. KIRSCHENBAUM, B. & GOLDMAN, S. A. (1995). Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl Acad. Sci. U.S.A. 92, 210-214.
51. KONONOVA, E. P. (1948). Development of the frontal region of the human brain during intrauterine life. Tr. Inst. Mozga 6, 8.
52. KRIEG, W. (1966). Functional Neuroanatomy. Bloomington, Illinois: Pantagraph Printing.
53. KUHN, H. G., DICKINSON-ANSON, H. & GAGE, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033.
54. KUKUEV, L. A. (1955). Relationship between the cortical nucleus of the motor analyzer and the adjacent subcortex in the process of human development. Dissertation, Moscow.
55. LEISE, E. M. (1990). Modular construction of nervous systems: A basic principle of design for invertebrates and vertebrates. Brain Res. Rev. 15, 1-23.
56. LEUBA, G. & KRAFTSIK, R. (1994). Changes in volume, surface estimate, three-dimensional shape and total number of neurons of the human primary visual cortex from midgestation until old age. Anat. Embryol. 190, 351-366.
57. LEWIN, R. (1997). Molecular anthropology. In: Patterns in Evolution: The Molecular View, pp. 172-174. Scientific American Library, New York.
58. LOIS, C. A. & ALVAREZ-BUYLLA, (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
59. LOTURCO, J. J. & KRIEGSTEIN, A. R. (1995). Neurotransmitter signaling before the birth of neurons. In: The Cortical Neuron (Gutnick, M. J. & Mody, I., eds), pp. 197-209. Oxford University Press.
60. LUSKIN, M. B., PARNAVELAS, J. G. & BARFIELD, J. A. (1993). Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci. 13, 1730-1750.
61. LUSKIN, M. B. (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1, 173-189.
62. MEHTA, P. P., BERTRAM, J. J. & LOEWENSTEIN, W. R. (1986). Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell 44, 187-196.
63. MENEZES, J. R., SMITH, C. M., NELSON, K. C. & LUSKIN, M. B. (1995). The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Molec. and Cellular Neurosci. 6, 496-508.
64. MOUNT, H. T., DEAN, D. O., ALBERCH, J., DREYFUS, C. F. & BLACK, I. B. (1995). Glial cell line-derived neurotrophic factor promotes the survival and morphologic differentiation of Purkinje cells. Proc. Natl Acad. Sci. U.S.A. 92, 9092-9096.
65. OGATA, J., FEIGIN, I. (1973). The relative weight of the gray and white matter of the normal human brain. J. Neuropath. Exp. Neurol. 32, 585-588.
66. O'KUSKY, J. & COLONNIER, M. (1982). A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys. J. Comp. Neurol. 210, 278-290.
67. PAXINOS, G. (1990). The Human Nervous System. San Diego: Academic Press.
68. PINCUS, D., HARRISON, C., GOODMAN, R., LABAR, D., FRASER, R., NEDERGAARD, M. & GOLDMAN, S. (1996). Long-term survival of new neurons generated in vitro by precursors derived from adult human epileptic temporal neocortex. Soc. Neurosci. Abs. 22, 286.
69. PREOBRAZHENSKAYA, N. S. (1948). The postnatal development of the occipital region of the human brain. Tr. Inst. Mozga 6, 44-77.
70. PREOBRAZHENSKAYA, N. S. (1961). The development of occipital region. In: The Structure and Functions of Human Analyzers in Ontogenesis (Sarkisov, S. A. ed.), p. 246. Moscow.
71. PURVES, D. & LAMANTIA, A. S. (1990). Numbers of "blobs" in the primary visual cortex of neonatal and adult monkeys. Proc. Natl Acad. Sci. U.S.A. 87, 5764-5767.
72. RAADSHEER, F. C., OORSCHOT, D. E., BERWER, R. W. H., TILDERS, F. J. H & SWAAB, D. S. (1994). Age-related increase in the total number of corticotropin-releasing hormone neurons in the human paraventricular nucleus in controls and Alzheiemer's disease: comparison of the dissector with an unfolding method. J. Comp. Neurol. 339, 447-457.
73. RABINOWICZ, T. (1967). Techniques for the establishment of an atlas of the cerebral cortex of the premature. In: Regional Development of the Brain in Early Life (Minkowski, A. ed.), pp. 71-124. Oxford: Blackwell Scientific.
74. RAKIC, P. (1990). Principles of neural cell migration. Experientia 46, 882-891.
75. RAKIC, P. (1985a). DNA synthesis and cell division in the adult primate brain. Ann. NYAS 457, 193-211.
76. RAKIC, P. (1985b). Limits of neurogenesis in primates. Science 227, 1054-1056.
77. REN, J., HAMADA, J., TAKEICHI, N., FUJIKAWA, S. & KOBAYASHI, H. (1990). Ultrastructural differences in junctional intercellular communication between highly and weakly metastatic clones derived from rat mammary carcinoma. Cancer Res. 50, 358-362.
78. ROCKEL, A. J., HIORNS, R. W. & POWELL, T. P. (1980). The basic uniformity in structure of the neocortex. Brain 103, 221-244.
79. SCAMMON, R. & HESDORFER, H. (1935). Growth of the human nervous system. Proc. Soc. Exptl Biol. Med. 33.
80. SCHUZ, A. & PALM, G. (1989). Density of neurons and synapses in the cerebral cortex of the mouse. J. Comp. Neurol. 286, 442-455.
81. SHANKLE, W. R., LANDING, B. H. & GREGG, J. (1983). Normal organ weights of infants and children: graphs of values by age, with confidence intervals. Ped. Path. 1, 399-408.
82. SHIGENO, T., BROCK, M., SHIGENO, S., FRITSCHKA, E. & CERVOSNAVARRO, J. (1982). The determination of brain water content: microgravimitry versus drying-weighing method. J. Neurosurg. 57, 99-1107.
83. SIEGEL, G. J. (1976). Basic Neurochemistry. pp. 346-370. Boston: Little Brown.
84. SMALLWOOD, J. A., COOPER, A. & TAYLOR, I. (1983). The errors of thymidine labeling in breast cancer. Clin. Oncol. 9, 331-335.
85. STANKEVICH, I. A. (1948). Development of the insular region of the human brain in the postnatal period. Tr. Inst. Mozga. 6, 130-151.
86. STANKEVICH, I. A. (1961). Development of the insular region. In: The Structure and Functions of Human Analyzers in Ontogenesis. (Sarkisov, S. A., ed.), p. 86, Moscow.
87. STEVENS, C. (1989). How cortical interconnectedness varies with network size. Neural. Comp. 1, 473-479.
88. STEVENS, C. (1993). Two principles of brain organization: A challenge for artificial neural networks. In: The Neurobiology of Neural Networks. (Gardner, D., ed.), pp. 13-20. Cambridge, MA: MIT Press.
89. STOWELL, W. (1941). Effect on tissue volume of various methods of fixation, dehydration and embedding. Stain Technol. 16, 67-83.
90. VAN EERDENBURG, F. J. & RAKIC, P. (1994). Early neurogenesis in the anterior hypothalamus of the rhesus monkey. Brain Res. Dev. Brain Res. 79, 290-296.
91. VAN ESSEN, D. C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313-318.
92. VON ECONOMO, C. & KOSKINAS, (1929). The Cytoarchitectonics of the Human Cerebral Cortex. Oxford: Oxford University Press.
93. WALSH, C. & CEPKO, C. (1992). Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 255, 434-440.
94. WEIL, A. (1928). The measurement of cerebral and cerebellar surfaces. The determination of the shrinkage of the surface of different brains. Arch. Neurol. Psychiat. 20, 834-835.
95. YAMADA, M., ENOKIDO, Y., IKEUCHI, T. & HATANAKA, H. (1995). Epidermal growth factor prevents oxygen-triggered apoptosis and induces sustained signalling in cultured rat cerebral cortical neurons. Eur. J. Neurosci. 7, 2130-2138.
96. ZHU, D., CAVENEY, S., KIDDER, G. M. & NAUS, C. C. G. (1991). Transfection of C6 glioma cells with connexin 43 DNA: analysis of expression, intercellular coupling and cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 88, 1883-1887.
97. ZILLES, K. (1990). Cortex. In: The Human Nervous System. (Paxinos, G., ed.), pp. 757-802. Academic Press.