Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage

By J. Bourgeois, P. Rakić. 1993

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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Citations in the corpus

Structural Synaptic Plasticity Has High Memory Capacity and Can Explain Graded Amnesia, Catastrophic Forgetting, and the Spacing Effect (2014, background): “the total number of synaptic connections remains approximately constant over time [14,80,81].”
The Basics of Brain Development (2010, background): “At the macroscropic level, studies of both monkeys and humans have documented widespread exuberant production of connections throughout all brain regions in the early postnatal period (Zecevic et al. 1989; Bourgeois and Rakic 1993; Bourgeois et al. 1994; Huttenlocher and de Courten 1987; Huttenloche”
The brainstem reticular formation is a small-world, not scale-free, network (2006, background): “One dominant form of post-natal connectivity change is that of synaptic pruning (Bourgeois & Rakic 1993).”
Normal Development of Brain Circuits (2010, background): “In the mouse, neuropil, or axonal and dendritic processes, constitutes approximately 60% of cortical volume (Bourgeois and Rakic, 1993), and pruning of these processes may represent the source of cortical thinning detected using MRI (Paus et al, 2008).”
Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study (2009, background): “Synaptic pruning together with trophic glial changes has been shown associated with puberty both in primate and human cerebral development (Huttenlocher, 1979; Bourgeois and Rakic, 1993; Morrison and Hof, 1997; Chechik et al., 1999).”
Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. (2010, background): “The adolescent phase of cortical thinning may reflect pruning in the form of use-dependent selective synapse elimination (Bourgeois and Rakic 1993; Huttenlocher and Dabholkar 1997; Shaw et al. 2008).”
Development of the Cerebral Cortex across Adolescence: A Multisample Study of Inter-Related Longitudinal Changes in Cortical Volume, Surface Area, and Thickness (2017, background): “A second hypothesis is that synaptic pruning and dendritic arborization (Bourgeois and Rakic, 1993; Huttenlocher and Dabholkar, 1997; Petanjek et al., 2011) results in decreasing gyrification and flattening of the cortex during adolescence (Raznahan et al.”
Synaptic Pruning in Development: A Computational Account (1998, background): “[Bourgeois and Rakic, 1993] J.P. Bourgeois and P. Rakic.”
Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood (2002, methodology): “The changes in WM capacity coincide in time with several neuronal developmental processes, including a decrease in synaptic density (Bourgeois & Rakic, 1993; Huttenlocher, 1979), axonal elimination (LaMantia & Rakic, 1990), changes in global cerebral metabolism (Chugani & Phelps, 1986; Kennedy &…”
Incremental Learning in Biological and Machine Learning Systems (2002, background): “A “plateau” phase of high synaptic density lasts for about two years.(15,16) It is followed by a 2–3.”
Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. (2000, unknown): “For example, there has been extensive research on this issue in the rhesus monkey by Pasko Rakic and colleagues (181).”
Networks of anatomical covariance (2013, background): “As noted by Bourgeois and Rakic, the “… decline of synaptic number during puberty should have a rather small effect on theoverall volume of the cortex” (Bourgeois and Rakic (1993).”