DOI: 10.1126/science.3952506. Concurrent Overproduction of Synapses in Diverse Regions of the Primate Cerebral Cortex

Concurrent Overproduction of Synapses in Diverse Regions of the Primate Cerebral Cortex

10.1126/science.3952506

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Synapses develop concurrently and at identical rates in different layers of the visual, somatosensory, motor, and prefrontal areas of the primate cerebral cortex. This isochronic course of synaptogenesis in anatomically and functionally diverse regions indicates that the entire cerebral cortex develops as a whole and that the establishment of cell-to-cell communication in this structure may be orchestrated by a single genetic or humoral signal. This is in contrast to the traditional view of hierarchical development of the cortical regions and provides new insight into the maturation of cortical functions.

Bibliography

Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986). Concurrent Overproduction of Synapses in Diverse Regions of the Primate Cerebral Cortex. Science, 232(4747), 232â235.

Authors 5

Pasko Rakic (first)
Jean-Pierre Bourgeois (additional)
Maryellen F. Eckenhoff (additional)
Nada Zecevic (additional)
Patricia S. Goldman-Rakic (additional)

References 64 Referenced 905

BACHEVALIER, J, AN EARLY AND A LATE DEVELOPING SYSTEM FOR LEARNING AND RETENTION IN INFANT MONKEYS, BEHAVIORAL NEUROSCIENCE 98: 770 (1984). (10.1037/0735-7044.98.5.770) / BEHAVIORAL NEUROSCIENCE (1984)
BENOIT, P, CONSEQUENCES OF TENOTOMY ON EVOLUTION OF MULTIINNERVATION IN DEVELOPING RAT SOLEUS MUSCLE, BRAIN RESEARCH 99: 354 (1975). (10.1016/0006-8993(75)90036-0) / BRAIN RESEARCH (1975)
BOOTHE, R.G., POSTNATAL-DEVELOPMENT OF VISION IN HUMAN AND NONHUMAN-PRIMATES, ANNUAL REVIEW OF NEUROSCIENCE 8: 495 (1985). (10.1146/annurev.ne.08.030185.002431) / ANNUAL REVIEW OF NEUROSCIENCE (1985)
BOOTHE, R, RHESUS MONKEY 1: 343 (1975). / RHESUS MONKEY (1975)
BRAND, S, ANAT EMBRYOL 169: 21 (1983). / ANAT EMBRYOL (1983)
BRAZIER MAB ARCHITECTRONICS CERE (1978).
BRODMANN K VERGLEICHENDE LOKALI (1909).
BROWN, M.C., SHORT-TERM AND LONG-TERM EFFECTS OF PARALYSIS ON THE MOTOR INNERVATION OF 2 DIFFERENT NEONATAL MOUSE MUSCLES, JOURNAL OF PHYSIOLOGY-LONDON 329: 439 (1982). (10.1113/jphysiol.1982.sp014312) / JOURNAL OF PHYSIOLOGY-LONDON (1982)
BUTTERS, N, ACTA NEUROBIOLOGIAE 32: 305 (1972). / ACTA NEUROBIOLOGIAE (1972)
CARLSON, M, DEVELOPMENT OF TACTILE DISCRIMINATION CAPACITY IN MACACA-MULATTA .1. NORMAL INFANTS, DEVELOPMENTAL BRAIN RESEARCH 16: 69 (1984). (10.1016/0165-3806(84)90064-6) / DEVELOPMENTAL BRAIN RESEARCH (1984)
10.1038/264705a0
CONEL J.L. POSTNATAL DEV HUMAN 1 (1939).
COOPER, M.L., GRADIENTS OF CELLULAR MATURATION AND SYNAPTOGENESIS IN THE SUPERIOR COLLICULUS OF THE FETAL RHESUS-MONKEY, JOURNAL OF COMPARATIVE NEUROLOGY 215: 165 (1983). (10.1002/cne.902150205) / JOURNAL OF COMPARATIVE NEUROLOGY (1983)
DIAMOND, A, SOC RES CHILD DEV AB 5: 85 (1985). / SOC RES CHILD DEV AB (1985)
DUFFY, C.J., J COMP NEUROL 214: 225 (1983). / J COMP NEUROL (1983)
ELLINGSON, R.J., DEVELOPMENT OF EVOKED RESPONSES IN VISUAL AND AUDITORY CORTICES OF KITTENS, JOURNAL OF NEUROPHYSIOLOGY 23: 363 (1960). (10.1152/jn.1960.23.4.363) / JOURNAL OF NEUROPHYSIOLOGY (1960)
FARKASBARGETON, E, ARCHITECTONICS CEREB: 175 (1978). / ARCHITECTONICS CEREB (1978)
FLECHSIG P ANATOMIE MENSCHLICHE (1920).
FRIEDE R.L. TOPOGRAPHIC BRAIN CH (1966).
Friedman S. L. Preterm Birth and Psychological Development (1981).
GOLDMAN, P.S., BRAIN RESEARCH 122: 393 (1977). (10.1016/0006-8993(77)90453-X) / BRAIN RESEARCH (1977)
GOLDMANRAKIC, P.S., LOCALIZATION OF FUNCTION WITHIN DORSOLATERAL PREFRONTAL CORTEX OF RHESUS MONKEY, EXPERIMENTAL NEUROLOGY 27: 291 (1970). (10.1016/0014-4886(70)90222-0) / EXPERIMENTAL NEUROLOGY (1970)
10.1126/science.186.4163.540
HARLOW, H.F., AMERICAN SCIENTIST 47: 459 (1959). / AMERICAN SCIENTIST (1959)
HINES, M, CONTRIBUTIONS TO EMBRYOLOGY 30: 153 (1942). / CONTRIBUTIONS TO EMBRYOLOGY (1942)
HUBEL, D.H., PLASTICITY OF OCULAR DOMINANCE COLUMNS IN MONKEY STRIATE CORTEX, PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES 278: 377 (1977). / PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES (1977)
HUTTENLOCHER, P.R., SYNAPTIC DENSITY IN HUMAN FRONTAL-CORTEX - DEVELOPMENTAL-CHANGES AND EFFECTS OF AGING, BRAIN RESEARCH 163: 195 (1979). (10.1016/0006-8993(79)90349-4) / BRAIN RESEARCH (1979)
HUTTENLOCHER, P.R., SYNAPTOGENESIS IN HUMAN VISUAL-CORTEX - EVIDENCE FOR SYNAPSE ELIMINATION DURING NORMAL DEVELOPMENT, NEUROSCIENCE LETTERS 33: 247 (1982). (10.1016/0304-3940(82)90379-2) / NEUROSCIENCE LETTERS (1982)
Jones, E. G., Dynamic Aspects of Neocortical Function: 7 (1984). / Dynamic Aspects of Neocortical Function (1984)
KENNEDY, C, LOCAL CEREBRAL GLUCOSE-UTILIZATION IN THE NEWBORN MACAQUE MONKEY, ANNALS OF NEUROLOGY 12: 333 (1982). (10.1002/ana.410120404) / ANNALS OF NEUROLOGY (1982)
LAWRENCE, D.G., DEVELOPMENT OF MOTOR CONTROL IN RHESUS-MONKEY - EVIDENCE CONCERNING ROLE OF CORTICOMOTONEURONAL CONNECTIONS, BRAIN 99: 235 (1976). (10.1093/brain/99.2.235) / BRAIN (1976)
LEVITT, P, REGION-SPECIFIC DISTRIBUTION OF CATECHOLAMINE AFFERENTS IN PRIMATE CEREBRAL-CORTEX - A FLUORESCENCE HISTOCHEMICAL ANALYSIS, JOURNAL OF COMPARATIVE NEUROLOGY 227: 23 (1984). (10.1002/cne.902270105) / JOURNAL OF COMPARATIVE NEUROLOGY (1984)
LUND, J.S., DEVELOPMENT OF NEURONS IN VISUAL-CORTEX (AREA 17) OF MONKEY (MACACA-NEMESTRINA) - GOLGI STUDY FROM FETAL DAY-127 TO POSTNATAL MATURITY, JOURNAL OF COMPARATIVE NEUROLOGY 176: 149 (1977). (10.1002/cne.901760203) / JOURNAL OF COMPARATIVE NEUROLOGY (1977)
Lund, J. S., The Organization of Cerebral Cortex: 106 (1981). / The Organization of Cerebral Cortex (1981)
MAHUT, H, ABSTRACTS. SOCIETY FOR NEUROSCIENCE 3: 428 (1977). / ABSTRACTS. SOCIETY FOR NEUROSCIENCE (1977)
Mahut H. The Hippocampus (1986).
MAUNSELL, JHR, THE CONNECTIONS OF THE MIDDLE TEMPORAL VISUAL AREA (MT) AND THEIR RELATIONSHIP TO A CORTICAL HIERARCHY IN THE MACAQUE MONKEY, JOURNAL OF NEUROSCIENCE 3: 2563 (1983). (10.1523/JNEUROSCI.03-12-02563.1983) / JOURNAL OF NEUROSCIENCE (1983)
10.1126/science.7123262
MENDELSON, M. J., DEVELOPMENTAL PSYCHOLOGY 19: 387 (1983). (10.1037/0012-1649.19.3.387) / DEVELOPMENTAL PSYCHOLOGY (1983)
MORRISON, J.H., LAMINAR, TANGENTIAL AND REGIONAL ORGANIZATION OF THE NORADRENERGIC INNERVATION OF MONKEY CORTEX - DOPAMINE-BETA-HYDROXYLASE IMMUNOHISTOCHEMISTRY, BRAIN RESEARCH BULLETIN 9: 309 (1982). (10.1016/0361-9230(82)90144-7) / BRAIN RESEARCH BULLETIN (1982)
Mountcastle, V. B., The Neurosciences, Fourth Study Program: 21 (1979). / The Neurosciences, Fourth Study Program (1979)
NISHIMURA, Y, DEVELOPMENT OF THE RHESUS-MONKEY RETINA .1. EMERGENCE OF THE INNER PLEXIFORM LAYER AND ITS SYNAPSES, JOURNAL OF COMPARATIVE NEUROLOGY 241: 420 (1985). (10.1002/cne.902410403) / JOURNAL OF COMPARATIVE NEUROLOGY (1985)
OKUSKY, J, A LAMINAR ANALYSIS OF THE NUMBER OF NEURONS, GLIA, AND SYNAPSES IN THE VISUAL-CORTEX (AREA-17) OF ADULT MACAQUE MONKEYS, JOURNAL OF COMPARATIVE NEUROLOGY 210: 278 (1982). (10.1002/cne.902100307) / JOURNAL OF COMPARATIVE NEUROLOGY (1982)
Peters A. Cerebral Cortex (1984).
RAKIC, P, EXPERIMENTAL BRAIN RESEARCH 1: 244 (1976). / EXPERIMENTAL BRAIN RESEARCH (1976)
10.1002/cne.901450105
RAKIC, P, JOURNAL OF COMPARATIVE NEUROLOGY 196: 99 (1981). (10.1002/cne.901960109) / JOURNAL OF COMPARATIVE NEUROLOGY (1981)
10.1038/261467a0
RAKIC, P, DEVELOPMENT AND MODIFIABILITY OF THE CEREBRAL-CORTEX, NEUROSCIENCES RESEARCH PROGRAM BULLETIN 20: 429 (1982). / NEUROSCIENCES RESEARCH PROGRAM BULLETIN (1982)
RAKIC, P, NEUROSCIENCES RESEARCH PROGRAM BULLETIN 13: 295 (1975). / NEUROSCIENCES RESEARCH PROGRAM BULLETIN (1975)
10.1098/rstb.1977.0040
10.1126/science.183.4123.425
10.1126/science.7302569
RILEY, D.A., TENOTOMY DELAYS POSTNATAL-DEVELOPMENT OF MOTOR INNERVATION OF RAT SOLEUS, BRAIN RESEARCH 143: 162 (1978). (10.1016/0006-8993(78)90760-6) / BRAIN RESEARCH (1978)
ROCKLAND, K.S., CORTICAL CONNECTIONS OF THE OCCIPITAL LOBE IN THE RHESUS-MONKEY - INTERCONNECTIONS BETWEEN AREAS 17, 18, 19 AND THE SUPERIOR TEMPORAL SULCUS, BRAIN RESEARCH 212: 249 (1981). (10.1016/0006-8993(81)90461-3) / BRAIN RESEARCH (1981)
Sarkisov S. A. Development of a Child's Brain (1965).
SCHMIDT, J.T., ACTIVITY SHARPENS THE MAP DURING THE REGENERATION OF THE RETINOTECTAL PROJECTION IN GOLDFISH, BRAIN RESEARCH 269: 29 (1983). (10.1016/0006-8993(83)90959-9) / BRAIN RESEARCH (1983)
Schmitt F. O. The Organization of the Cerebral Cortex (1981).
Snedecor, G. W., Statistical Methods: 419 (1967). / Statistical Methods (1967)
Stryker, M. P., Journal of Neuroscience 6: 2117 (1986). (10.1523/JNEUROSCI.06-08-02117.1986) / Journal of Neuroscience (1986)
THOMPSON, W.D., NEUROSCIENCE 2: 271 (1979). / NEUROSCIENCE (1979)
10.1038/299583a0
Yakovlev, P. I., Regional Development of the Brain in Early Life: 3 (1967). / Regional Development of the Brain in Early Life (1967)
ZECEVIC, N, ABSTRACTS. SOCIETY FOR NEUROSCIENCE 11: 1288 (1985). / ABSTRACTS. SOCIETY FOR NEUROSCIENCE (1985)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 4:28 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 4:31 a.m.)
Indexed	3 days, 23 hours ago (Aug. 28, 2025, 8:29 a.m.)
Issued	39 years, 4 months ago (April 11, 1986)
Published	39 years, 4 months ago (April 11, 1986)
Published Print	39 years, 4 months ago (April 11, 1986)

Funders 0

None

BibTeX

@article{Rakic_1986, title={Concurrent Overproduction of Synapses in Diverse Regions of the Primate Cerebral Cortex}, volume={232}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.3952506}, DOI={10.1126/science.3952506}, number={4747}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Rakic, Pasko and Bourgeois, Jean-Pierre and Eckenhoff, Maryellen F. and Zecevic, Nada and Goldman-Rakic, Patricia S.}, year={1986}, month=apr, pages={232–235} }

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