Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage
Open accessAbstract
The kinetics of synaptogenesis in the primary visual cortex (Brodmann's area 17) were analyzed by electron microscopy in 33 rhesus monkeys, ranging in age from the 50th embryonic day (E50) to 20 years. A series of overlapping electron micrographs (vertical probes) were examined at each age on sections of the upper bank of the calcarine fissure. Synaptic contacts were first observed in the E50 specimen in the subplate and marginal zone (prospective layer I). In the cortical plate itself, synapses appear between E65 and E89 starting in the prospective layer VI. By E112, after all cortical neurons have assumed their laminar positions, synapses situated predominantly on dendritic shafts were present at a low density throughout the full thickness of the cortical plate. Thereafter, synapses accumulate more rapidly on dendritic spines and by E144 an equal number of contacts are found on both spines and shafts. The density of synapses continues to increase exponentially in all layers and reaches the mean maximum density of about 90 synapses per 100 microns 3 of neuropil by the third postnatal month. During the next 2 postnatal years the density of synaptic contacts decreases only slightly to a mean of 80/100 microns 3 of neuropil. Around the time of puberty, however, synaptic density decreases more rapidly to reach the adult level of about 40–50/100 microns 3 of neuropil. The 40% decrease in the density of synaptic contacts occurring between 2.7 and 5 years represents a loss of about 5000 synapses per second in the primary visual cortex of the two hemispheres, due primarily to the loss of asymmetric synapses situated on dendritic spines. The transient phase of high density of synaptic contacts located on dendrospines is shorter in thalamo-recipient layer IV than in either supra- or intragranular layers and is completed within the first postnatal year. It ends earlier in sublayer IVC than in layers IVAB and II-III, for example, reflecting biochemical and functional maturation of the different visual subsystems.
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Synaptic pruning of excitatory contacts is the signature morphologic event of late brain maturation during adolescence.
“Synaptic pruning of excitatory contacts is the signature morphologic event of late brain maturation during adolescence.”
From A role for synaptic plasticity in the adolescent development of executive function (2013) · cites this paper as [37]
The paper reports substantial synapse loss during puberty in the macaque primary visual cortex, primarily involving asymmetric contacts on dendritic spines. That supports adolescent pruning of excitatory contacts, but the paper does not establish that it is the signature morphologic event of late maturation throughout the brain. The decisive passages are in the paper’s opening summary and “Decrease of the density of synapses during puberty”; page numbers are not available in the supplied copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn the non-human primate, synaptic density in multiple cortical areas synchronously increases, peaks during the postnatal 3rd month, declines slowly (10%) until ∼2 years of age, with a steeper decline (40%) occurring between 2.7 and 5 years (adulthood).
“Quantitative analyses of synapses in the non-human primate uncovered a synchronous increase in synaptic density in multiple cortical areas that peaks during the postnatal 3rd month, declines slowly (10%) until∼2 years of age with a steeper decline (40%) occurring between 2.7 and 5 years (adulthood).35, 36, 37, 38”
From A role for synaptic plasticity in the adolescent development of executive function (2013) · cites this paper as [37]
The 'Phase of high synaptic density' section (page unavailable) reports a peak in the third postnatal month followed by a slight decrease over the next two years. The paper also reports a 40% decrease between 2.7 and 5 years and says simultaneous increases across visual-cortex layers had been observed in other cortical areas. It does not quantify the earlier decrease as 10% or establish that the full stated time course applies synchronously across multiple cortical areas. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe main argument in support of the hypothesis that synaptic elimination adjusts excitatory/inhibitory balance stems from the specificity of the loss: excitatory synapses are selectively degenerated whereas inhibitory synapses are spared.
“The main argument in support of this hypothesis stems from the specificity of the loss: excitatory synapses are selectively degenerated whereas inhibitory synapses are spared.35, 37”
From A role for synaptic plasticity in the adolescent development of executive function (2013) · cites this paper as [37]
In “Decrease of the density of synapses during puberty” (page unavailable), the paper reports predominant loss of synapses on dendritic spines, while contacts on dendritic shafts remain relatively steady. But it does not establish that the lost synapses are exclusively excitatory or that inhibitory synapses are spared; its “Ratio between asymmetric and symmetric synaptic contacts” section reports mixed contact types on shafts. The cited evidence supports selective loss by synapse location, not the claim’s categorical excitatory/inhibitory distinction. (LLM, conf=0.85)
Experimental — accuracy not yet measuredTypical brain development in nonhuman primates is marked by an initial period of overproduction of synapses, followed by selective stabilization and elimination of a substantial proportion of synapses.
“Nonhuman primate studies show that typical brain development is marked by an initial period of overproduction of synapses, followed by selective stabilization and elimination of a substantial proportion of synapses (Huttenlocher, 1979, Huttenlocher et al., 1982, Bourgeois and Rakic, 1993 LaMantia and Rakic, 1994).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Bourgeois and Rakic, 1993 LaMantia and Rakic, 1994
Grey matter decline may reflect an artefact of increased myelination of intra-cortical axons rather than synaptic pruning.
“Instead, grey matter decline may reflect an artefact of increased myelination of intra-cortical axons (Bourgeois and Rakic, 1993, Paus, 2005, Paus et al., 2008).”
From Neurocognitive bases of emotion regulation development in adolescence (2015) · cites this paper as Bourgeois and Rakic, 1993
Histological studies have shown evidence for synaptic proliferation in certain brain regions at around the start of adolescence, with protracted synaptic pruning occurring across the remainder of adolescence.
“Histological studies have shown evidence for synaptic proliferation in certain brain regions at around the start of adolescence, with protracted synaptic pruning occurring across the remainder of adolescence (e.g. human frontal cortex: Huttenlocher and Dabholkar, 1998; primate: Bourgeois and Rakic, 1993; Rakic et al., 1986).”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Bourgeois and Rakic, 1993
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Cites
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · see citing works
Self-citationConcurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · cited 9× · see citing works
“The density of synaptic contacts per unit volume of neuropil in the striate cortex of adult monkeys is comparable to that in other areas counted from the same set of animals ( Rakic et al., 1986 ).”
BackgroundMethodInfluentialSelf-citationThe development of ocular dominance columns in normal and visually deprived monkeys
Le Vay, S., Wiesel, T. N., & Hubel, D. H. (1980) · Journal of Comparative Neurology · doi:10.1002/cne.901910102 · Cited by 1,123 · see citing works
Colonnier, M. (1968) · Brain Research · doi:10.1016/0006-8993(68)90234-5 · Cited by 946 · see citing works
The development of synapses in the visual system of the cat
Cragg, B. G. (1975) · Journal of Comparative Neurology · doi:10.1002/cne.901600202 · Cited by 520 · see citing works
Elimination of neurons from the rhesus monkey's lateral geniculate nucleus during development
Williams, R. W., & Rakic, P. (1988) · Journal of Comparative Neurology · doi:10.1002/cne.902720310 · Cited by 124 · see citing works
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Flagged first, then by citations
Research works printed but not linked: 7
- Colonnier M (198 1) The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In: The organization ofthe cerebral cortex (Schmitt FO, Worden FG, Dennis SD, eds), pp 125-l 52. Cam- bridge, MA: MIT Press.
- Billings-Gagliardy S, Chan-Palay V, Palay SL (1974) A review of Foote SL, Morrison JH (1984) Postnatal development of laminar in- nervation patterns by monoaminergic fibers in monkey (Macacafas- cicularis) primary visual cortex. J Neurosci 4:2667-2680.
- LeVay S, Stryker MP (I 979) The development of ocular dominance columns in the cat. In: Symposium: aspects of developmental neu- robiology (Femandelli JA, ed), pp 83-98, Society for Neuroscience.
- Peters A (1987) Number of neurons and synapses in primary visual cortex. In: Cerebral cortex, Vol 6, Chap 7 (Peters A, Jones EG, eds), pp 267-294. New York: Plenum.
- Peters A, Palay SL, Webster Hide F (1976) The fine structure of the nervous system. Philadelphia: Saunders. Plant TM (1988) Neuroendocrine basis of puberty in the monkey (Mucucu muluttu). In: Frontiers of neuroendocrinology, Vol 10 (Mar- tin L, Ganong WF, eds), pp 215-238. New York: Raven.
- Purves D (1988) Body and brain: a trophic theory of neuronal con- nections. Cambridge, MA: Harvard UP.
- Small JV (1968) Measurements of section thickness. In: Proceedings of the 4th European Congress on Electron Microscopy, Vol 1 (Boc- ciarelli DS, ed), p 609. Rome: Tipografia Poliglotta Vaticana.
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Rice, D., & Barone, S. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108s3511 · Cited by 2,944 · see citing works
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Burnett, S., Sebastian, C., Cohen Kadosh, K., & Blakemore, S.-J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.011 · Cited by 391 · see citing works
Lewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388 · see citing works
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Oades, R. D., Dauvermann, M. R., Schimmelmann, B. G., Schwarz, M. J., & Myint, A.-M. (2010) · Behavioral and Brain Functions · doi:10.1186/1744-9081-6-29 · Cited by 151 · see citing works
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- Authors
- Bourgeois, J., & Rakic, P.
- Affiliations
- Institut Pasteur (FR)
- ORCID
- Rakic, P
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1993-07-01
- Volume
- 13
- Issue
- 7
- Pages
- 2801-2820
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6576672
- OpenAlex
- W1950026089
- Cited by
- 567
- References
- 6
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 15 · 2023: 16 · 2022: 14 · 2021: 14 · 2020: 58 · 2019: 14 · 2018: 21 · 2017: 19 · 2016: 14 · 2015: 25 · 2014: 20 · 2013: 28 · 2012: 17
- FWCI
- 3.61
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Yale University
- National Institutes of Health (5p01ns022807-15)
- National Eye Institute (EY02593, R01EY002593)
- National Institute of Neurological Disorders and Stroke (NS-22807)
- National Center for Research Resources (P51RR0016)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- synaptic density, primary visual cortex, synaptogenesis, synaptic pruning, dendritic spines, calcarine fissure, rhesus monkeys, cortical development, postnatal development, puberty, layer 4, subplate, cortical lamination
- MeSH terms
- Aging, Animals, Female, Embryonic and Fetal Development, Fetus, Macaca mulatta, Male, Microscopy, Electron, Sexual Maturation, Synapses, Visual Cortex
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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