Skip Navigation

This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (180)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Bourgeois, J.-P.
Right arrow Articles by Rakic, P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Bourgeois, J.-P.
Right arrow Articles by Rakic, P.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

Cerebral Cortex 1994; 4:78-96
© Oxford University Press 1994

research-article

Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys

Jean-Pierre Bourgeois1, Patricia S. Goldman-Rakic2 and Pasko Rakic2

1Laboratoire de Neurobiologie Moléculaire, Département des Biotechnologies, Institut Pasteur 75724 Paris Cedex 15, France, 2Section of Neurobiology, School of Medicine, Yale University New Haven, Connecticut 06510

Since the turn of the century, the prefrontal association areas of the cerebral cortex have been thought to be among the last regions of the cortical mantle to develop. We have examined the course of synaptogenesis in the macaque prefrontal cortex by quantitative electron microscopic analysis in 25 rhesus monkeys ranging in age from embryonic day 47 (E47) to 20 years of age. A series of overlapping electron micrographs spanning the whole cortical thickness in each animal provided data on the number, the proportion, and the density of synapses per unit area (NA) and per unit volume (NV) of neuropil.

The tempo and kinetics of synapse formation in prefrontal cortex closely resemble those described for sensory and motor areas, particularly during the stages of synapse acquisition and overproduction (Rakic et al., 1986). In young embryos, we describe a precortical phase (E47-E78), when synapses are found only above and below, but not within, the cortical plate. Following that, there is an early cortical phase, from E78 to E104, during which synapses accumulate within the cortical plate, initially exclusively on dendritic shafts. The next rapid phase of synaptogenesis begins at 2 months before birth and ends approximately at 2 months after birth, culminating with a mean density of 750 million synapses per cubic micrometer. This accumulation is largely accounted for by a selective increase in axospine synapses in the supragranular layers. The period of explosive synaptic density is followed by a protracted plateau stage that lasts from 2 months to 3 years of age when synaptic density remains relatively constant. The final period of decline, from 3 years through over 20 years of age, is marked by a slight but statistically significant decline in synaptic density.

Concurrent recruitment of synapses with that of sensory and motor areas supports the concept that the initial establishment of cortical circuitry is governed by general mechanisms common to all areas, independent of their specific functional domain. The finding that synaptic density is relatively stable from early adolescence through puberty (the plateau period) is indicative of the importance, in primates, of a consistent and high synaptic density during the formative years when learning experiences are most intense.


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Cereb CortexHome page
A.M. C. Kelly, A. Di Martino, L. Q. Uddin, Z. Shehzad, D. G. Gee, P. T. Reiss, D. S. Margulies, F. X. Castellanos, and M. P. Milham
Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood
Cereb Cortex, August 26, 2008; (2008) bhn117v2.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
S. Neufang, K. Specht, M. Hausmann, O. Gunturkun, B. Herpertz-Dahlmann, G. R. Fink, and K. Konrad
Sex Differences and the Impact of Steroid Hormones on the Developing Human Brain
Cereb Cortex, June 11, 2008; (2008) bhn100v1.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
Z. Petanjek, M. Judas, I. Kostovic, and H. B.M. Uylings
Lifespan Alterations of Basal Dendritic Trees of Pyramidal Neurons in the Human Prefrontal Cortex: A Layer-Specific Pattern
Cereb Cortex, April 1, 2008; 18(4): 915 - 929.
[Abstract] [Full Text] [PDF]

Home page
 Ann. N. Y. Acad. Sci.Home page
B.J. CASEY, R. M. JONES, and T. A. HARE
The Adolescent Brain
Ann. N.Y. Acad. Sci., March 1, 2008; 1124(1): 111 - 126.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
G. Gonzalez-Burgos, S. Kroener, A. V. Zaitsev, N. V. Povysheva, L. S. Krimer, G. Barrionuevo, and D. A. Lewis
Functional Maturation of Excitatory Synapses in Layer 3 Pyramidal Neurons during Postnatal Development of the Primate Prefrontal Cortex
Cereb Cortex, March 1, 2008; 18(3): 626 - 637.
[Abstract] [Full Text] [PDF]

Home page
 Schizophr BullHome page
C. Arango, C. Moreno, S. Martinez, M. Parellada, M. Desco, D. Moreno, D. Fraguas, N. Gogtay, A. James, and J. Rapoport
Longitudinal Brain Changes in Early-Onset Psychosis
Schizophr Bull, March 1, 2008; 34(2): 341 - 353.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
M. A. Henson, A. C. Roberts, K. Salimi, S. Vadlamudi, R. M. Hamer, J. H. Gilmore, L. F. Jarskog, and B. D. Philpot
Developmental Regulation of the NMDA Receptor Subunits, NR3A and NR1, in Human Prefrontal Cortex
Cereb Cortex, February 21, 2008; (2008) bhn017v1.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
M. Abitz, R. D. Nielsen, E. G. Jones, H. Laursen, N. Graem, and B. Pakkenberg
Excess of Neurons in the Human Newborn Mediodorsal Thalamus Compared with That of the Adult
Cereb Cortex, November 1, 2007; 17(11): 2573 - 2578.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
J. H. Gilmore, W. Lin, M. W. Prastawa, C. B. Looney, Y. S. K. Vetsa, R. C. Knickmeyer, D. D. Evans, J. K. Smith, R. M. Hamer, J. A. Lieberman, et al.
Regional Gray Matter Growth, Sexual Dimorphism, and Cerebral Asymmetry in the Neonatal Brain
J. Neurosci., February 7, 2007; 27(6): 1255 - 1260.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. PsychiatryHome page
J. H. Barnett, J. Heron, S. M. Ring, J. Golding, D. Goldman, K. Xu, and P. B. Jones
Gender-Specific Effects of the Catechol-O-Methyltransferase Val108/158Met Polymorphism on Cognitive Function in Children
Am J Psychiatry, January 1, 2007; 164(1): 142 - 149.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
S Lippe, M-S Roy, C Perchet, and M Lassonde
Electrophysiological Markers of Visuocortical Development
Cereb Cortex, January 1, 2007; 17(1): 100 - 107.
[Abstract] [Full Text] [PDF]

Home page
 PediatricsHome page
A. U.J. Mewes, P. S. Huppi, H. Als, F. J. Rybicki, T. E. Inder, G. B. McAnulty, R. V. Mulkern, R. L. Robertson, M. J. Rivkin, and S. K. Warfield
Regional Brain Development in Serial Magnetic Resonance Imaging of Low-Risk Preterm Infants
Pediatrics, July 1, 2006; 118(1): 23 - 33.
[Abstract] [Full Text] [PDF]

Home page
 J. Exp. Biol.Home page
J. Jelsing, R. Nielsen, A. K. Olsen, N. Grand, R. Hemmingsen, and B. Pakkenberg
The postnatal development of neocortical neurons and glial cells in the Gottingen minipig and the domestic pig brain
J. Exp. Biol., April 15, 2006; 209(8): 1454 - 1462.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
M. R. Milad, B. T. Quinn, R. K. Pitman, S. P. Orr, B. Fischl, and S. L. Rauch
Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory
PNAS, July 26, 2005; 102(30): 10706 - 10711.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. PsychiatryHome page
N. Kolluri, Z. Sun, A. R. Sampson, and D. A. Lewis
Lamina-Specific Reductions in Dendritic Spine Density in the Prefrontal Cortex of Subjects With Schizophrenia
Am J Psychiatry, June 1, 2005; 162(6): 1200 - 1202.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
J. Bock, M. Gruss, S. Becker, and K. Braun
Experience-induced Changes of Dendritic Spine Densities in the Prefrontal and Sensory Cortex: Correlation with Developmental Time Windows
Cereb Cortex, June 1, 2005; 15(6): 802 - 808.
[Abstract] [Full Text] [PDF]

Home page
 Ann. N. Y. Acad. Sci.Home page
D. A. LEWIS, D. CRUZ, S. EGGAN, and S. ERICKSON
Postnatal Development of Prefrontal Inhibitory Circuits and the Pathophysiology of Cognitive Dysfunction in Schizophrenia
Ann. N.Y. Acad. Sci., June 1, 2004; 1021(1): 64 - 76.
[Abstract] [Full Text] [PDF]

Home page
 Ann. N. Y. Acad. Sci.Home page
A. F. T. ARNSTEN and R. M. SHANSKY
Adolescence: Vulnerable Period for Stress-Induced Prefrontal Cortical Function? Introduction to Part IV
Ann. N.Y. Acad. Sci., June 1, 2004; 1021(1): 143 - 147.
[Abstract] [Full Text] [PDF]

Home page
 Ann. N. Y. Acad. Sci.Home page
H. P. BLUMBERG, J. KAUFMAN, A. MARTIN, D. S. CHARNEY, J. H. KRYSTAL, and B. S. PETERSON
Significance of Adolescent Neurodevelopment for the Neural Circuitry of Bipolar Disorder
Ann. N.Y. Acad. Sci., June 1, 2004; 1021(1): 376 - 383.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
N. Gogtay, J. N. Giedd, L. Lusk, K. M. Hayashi, D. Greenstein, A. C. Vaituzis, T. F. Nugent III, D. H. Herman, L. S. Clasen, A. W. Toga, et al.
From the Cover: Dynamic mapping of human cortical development during childhood through early adulthood
PNAS, May 25, 2004; 101(21): 8174 - 8179.
[Abstract] [Full Text] [PDF]

Home page
 Ann. N. Y. Acad. Sci.Home page
D. A. LEWIS, L. A. GLANTZ, J. N. PIERRI, and R. A. SWEET
Altered Cortical Glutamate Neurotransmission in Schizophrenia: Evidence from Morphological Studies of Pyramidal Neurons
Ann. N.Y. Acad. Sci., November 1, 2003; 1003(1): 102 - 112.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
H. Duan, S. L. Wearne, A. B. Rocher, A. Macedo, J. H. Morrison, and P. R. Hof
Age-related Dendritic and Spine Changes in Corticocortically Projecting Neurons in Macaque Monkeys
Cereb Cortex, September 1, 2003; 13(9): 950 - 961.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. PsychiatryHome page
H. P. Blumberg, A. Martin, J. Kaufman, H.-C. Leung, P. Skudlarski, C. Lacadie, R. K. Fulbright, J. C. Gore, D. S. Charney, J. H. Krystal, et al.
Frontostriatal Abnormalities in Adolescents With Bipolar Disorder: Preliminary Observations From Functional MRI
Am J Psychiatry, July 1, 2003; 160(7): 1345 - 1347.
[Abstract] [Full Text] [PDF]

Home page
 Learn. Mem.Home page
V. Vuontela, M.-R. Steenari, S. Carlson, J. Koivisto, M. Fjallberg, and E. T. Aronen
Audiospatial and Visuospatial Working Memory in 6-13 Year Old School Children
Learn. Mem., January 1, 2003; 10(1): 74 - 81.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
E. K. Lambe, L. S. Krimer, and P. S. Goldman-Rakic
Differential Postnatal Development of Catecholamine and Serotonin Inputs to Identified Neurons in Prefrontal Cortex of Rhesus Monkey
J. Neurosci., December 1, 2000; 20(23): 8780 - 8787.
[Abstract] [Full Text] [PDF]

Home page
 NeurologyHome page
W. D. Gaillard, L. Hertz-Pannier, S. H. Mott, A. S. Barnett, D. LeBihan, and W. H. Theodore
Functional anatomy of cognitive development: fMRI of verbal fluency in children and adults
Neurology, January 11, 2000; 54(1): 180 - 180.
[Abstract] [Full Text] [PDF]

Home page
 Arch Gen PsychiatryHome page
L. A. Glantz and D. A. Lewis
Decreased Dendritic Spine Density on Prefrontal Cortical Pyramidal Neurons in Schizophrenia
Arch Gen Psychiatry, January 1, 2000; 57(1): 65 - 73.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
T. Takahashi, T. Goto, S. Miyama, R. S. Nowakowski, and V. S. Caviness Jr
Sequence of Neuron Origin and Neocortical Laminar Fate: Relation to Cell Cycle of Origin in the Developing Murine Cerebral Wall
J. Neurosci., December 1, 1999; 19(23): 10357 - 10371.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. PsychiatryHome page
J. N. Pierri, A. S. Chaudry, T.-U. W. Woo, and D. A. Lewis
Alterations in Chandelier Neuron Axon Terminals in the Prefrontal Cortex of Schizophrenic Subjects
Am J Psychiatry, November 1, 1999; 156(11): 1709 - 1719.
[Abstract] [Full Text]

Home page
 ScienceHome page
E. Gould, A. J. Reeves, M. S. Graziano, and C. G. Gross
Neurogenesis in the Neocortex of Adult Primates
Science, October 15, 1999; 286(5439): 548 - 552.
[Abstract] [Full Text]

Home page
 Cereb CortexHome page
J. DeFelipe, P. Marco, I. Busturia, and A. Merchan-Perez
Estimation of the Number of Synapses in the Cerebral Cortex: Methodological Considerations
Cereb Cortex, October 1, 1999; 9(7): 722 - 732.
[Abstract] [Full Text] [PDF]

Home page
 Cereb CortexHome page
V. A. Magnotta, N. C. Andreasen, S. K. Schultz, G. Harris, T. Cizadlo, D. Heckel, P. Nopoulos, and M. Flaum
Quantitative In Vivo Measurement of Gyrification in the Human Brain: Changes Associated with Aging
Cereb Cortex, March 1, 1999; 9(2): 151 - 160.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
M. Ernst, A. J. Zametkin, J. A. Matochik, P. H. Jons, and R. M. Cohen
DOPA Decarboxylase Activity in Attention Deficit Hyperactivity Disorder Adults. A [Fluorine-18]Fluorodopa Positron Emission Tomographic Study
J. Neurosci., August 1, 1998; 18(15): 5901 - 5907.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
S. M. Catalano, C. K. Chang, and C. J. Shatz
Activity-Dependent Regulation of NMDAR1 Immunoreactivity in the Developing Visual Cortex
J. Neurosci., November 1, 1997; 17(21): 8376 - 8390.
[Abstract] [Full Text] [PDF]

Home page
 J PsychopharmacolHome page
A. F. T. Arnsten
Catecholamine regulation of the prefrontal cortex
J Psychopharmacol, January 1, 1997; 11(2): 151 - 162.
[Abstract] [PDF]

Home page
 J. Neurosci.Home page
G. N. Elston, R. Benavides-Piccione, and J. DeFelipe
The Pyramidal Cell in Cognition: A Comparative Study in Human and Monkey
J. Neurosci., September 1, 2001; 21(17): RC163 - RC163.
[Abstract] [Full Text] [PDF]


Disclaimer:
Please note that abstracts for content published before 1996 were created through digital scanning and may therefore not exactly replicate the text of the original print issues. All efforts have been made to ensure accuracy, but the Publisher will not be held responsible for any remaining inaccuracies. If you require any further clarification, please contact our Customer Services Department.