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Science 15 October 1999:
Vol. 286. no. 5439, pp. 548 - 552
DOI: 10.1126/science.286.5439.548

Reports

Neurogenesis in the Neocortex of Adult Primates

Elizabeth Gould, * Alison J. Reeves, Michael S. A. Graziano, Charles G. Gross

In primates, prefrontal, inferior temporal, and posterior parietal cortex are important for cognitive function. It is shown that in adult macaques, new neurons are added to these three neocortical association areas, but not to a primary sensory area (striate cortex). The new neurons appeared to originate in the subventricular zone and to migrate through the white matter to the neocortex, where they extended axons. These new neurons, which are continually added in adulthood, may play a role in the functions of association neocortex.

Department of Psychology, Princeton University, Princeton, NJ 08544, USA.
*   To whom correspondence should be addressed. E-mail: goulde{at}princeton.edu


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   Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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W. Jiang, W. Gu, T. Brannstrom, R. Rosqvist, and P. Wester (2001)
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   Abstract »    Full Text »    PDF »
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K. Jin, M. Minami, J. Q. Lan, X. O. Mao, S. Batteur, R. P. Simon, and D. A. Greenberg (2001)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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   Abstract »    Full Text »
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   Abstract »    PDF »
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M. A. Gates, R. A. Fricker-Gates, S. S. Magavi, and J. D. Macklis (2000)
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   Abstract »    PDF »
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   Abstract »    PDF »
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   Abstract »    PDF »
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   Full Text »
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(2000)
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   PDF »
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F. H. Gage (2000)
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   Abstract »    Full Text »
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D. van der Kooy and a. S. Weiss (2000)
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   Abstract »    Full Text »    PDF »
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V. Ourednik, J. Ourednik, J. D. Flax, W. M. Zawada, C. Hutt, C. Yang, K. I. Park, S. U. Kim, R. L. Sidman, C. R. Freed, et al. (2001)
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   Abstract »    Full Text »    PDF »
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N. Jain, S. L. Florence, H.-X. Qi, and J. H. Kaas (2000)
PNAS 97, 5546-5550
   Abstract »    Full Text »    PDF »
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E. Gould, N. Vail, M. Wagers, and C. G. Gross (2001)
PNAS 98, 10910-10917
   Abstract »    Full Text »    PDF »



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