Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans

Bianchi, Serena; Stimpson, Cheryl D.; Duka, Tetyana; Larsen, Michael; Janssen, William G.M.; Collins, Zachary; Bauernfeind, Amy L.; Schapiro, Steven J.; Baze, Wallace B.; McArthur, Mark J.; Hopkins, William D.; Wildman, Derek E.; Lipovich, Leonard; Kuzawa, Christopher W.; Jacobs, Bob; Hof, Patrick R.; Sherwood, Chet C.

doi:10.1073/pnas.1301224110

Cited by 117 publications

(118 citation statements)

References 68 publications

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“…In all three species neocortical synapse densities are doubled during growth, compared with densities at birth. In macaques the period of peak synaptic density occurs during infancy, whereas in humans and chimpanzees peak synaptic densities take place during the midjuvenile or (in humans) childhood period (44). Brain energetics are thus not likely to impose a strong constraint on later juvenile body growth in macaques, whereas in chimpanzees growth is predicted to be slowed in the juvenile period, but to a lesser degree than in humans because of their smaller brains and corresponding lower brain metabolic needs (22).…”

Section: Discussionmentioning

confidence: 99%

Metabolic costs and evolutionary implications of human brain development

Kuzawa

Chugani

Grossman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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356

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The high energetic costs of human brain development have been hypothesized to explain distinctive human traits, including exceptionally slow and protracted preadult growth. Although widely assumed to constrain life-history evolution, the metabolic requirements of the growing human brain are unknown. We combined previously collected PET and MRI data to calculate the human brain's glucose use from birth to adulthood, which we compare with body growth rate. We evaluate the strength of brain-body metabolic trade-offs using the ratios of brain glucose uptake to the body's resting metabolic rate (RMR) and daily energy requirements (DER) expressed in glucose-gram equivalents (glucose rmr% and glucose der% ). We find that glucose rmr% and glucose der% do not peak at birth (52.5% and 59.8% of RMR, or 35.4% and 38.7% of DER, for males and females, respectively), when relative brain size is largest, but rather in childhood (66.3% and 65.0% of RMR and 43.3% and 43.8% of DER). Body-weight growth (dw/dt) and both glucose rmr% and glucose der% are strongly, inversely related: soon after birth, increases in brain glucose demand are accompanied by proportionate decreases in dw/dt. Ages of peak brain glucose demand and lowest dw/dt co-occur and subsequent developmental declines in brain metabolism are matched by proportionate increases in dw/dt until puberty. The finding that human brain glucose demands peak during childhood, and evidence that brain metabolism and body growth rate covary inversely across development, support the hypothesis that the high costs of human brain development require compensatory slowing of body growth rate.neuroimaging | diabetes | human evolution | neuronal plasticity | anthropology A prolonged period of childhood and juvenile growth is a defining feature of human life history (1-3). Compared with other great apes, human offspring are weaned early, leading to an extended period of dependence on procured resources rather than breast milk (1, 4). Although this unique human reproductive pattern is viewed as shortening the interbirth interval and thus increasing fertility (5, 6), what is less clear is why humans also grow so slowly during childhood. Although most primates grow slower than other mammals (7), human childhood and juvenile growth stand out as unusually slow even by primate and great ape standards, during which it proceeds at a pace more typical of reptiles than of mammals (8, 9). In humans, a sizeable percentage of preadult growth is deferred until the pubertal growth spurt, when growth rate markedly increases and adult size is achieved (1).Many hypotheses have been proposed to explain this slow and prolonged preadult life-stage, with most pointing to the extra time and energy required for human learning and brain development (5, 10-12). It has long been assumed that human cultural practices are sufficiently complex that they take many years to learn, which could have selected for a slowing down and extension of preadult development (13). A recent variant of this idea notes the importance of ...

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Section: Discussionmentioning

confidence: 99%

Metabolic costs and evolutionary implications of human brain development

Kuzawa

Chugani

Grossman

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

404

356

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“…However, few data exist on the ontogenetic neural development of the apes that are more closely related to humans. By means of an experimental analysis, Serena Bianchi et al (11) show for the first time how Pan paniscus synaptogenesis matches the human case, with a peak of synapse density during the juvenile period (2-5 y of age). Also, chimpanzees and humans share a late development of dendrites of prefrontal pyramidal neurons, compared with sensorimotor areas, offering a common potential for enhanced developmental plasticity.…”

Section: Primate Evolutionary Continuitymentioning

confidence: 98%

In the light of evolution VII: The human mental machinery

Cela‐Conde¹,

Lombardo²,

Avise³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Overproduction of synapses and associated dendrites and axons is observed across all mammalian species and is followed by pruning (i.e. selective elimination of connections) (Bianchi et al, 2013;Innocenti and Price, 2005). The latter process spans childhood and adolescence and occurs as a result of competition for neurotrophic factors including brain-derived neurotropic factor (BDNF) and the need for afferent input to stabilize immature, labile connections (Hua and Smith, 2004;Innocenti and Price, 2005;Stiles and Jernigan, 2010;Webb et al, 2001).…”

Section: Postnatal Brain Developmentmentioning

confidence: 99%

The emergence of functional architecture during early brain development

2017

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Early human brain development constitutes a sequence of intricate processes resulting in the ontogeny of functionally operative neural circuits. Developmental trajectories of early brain network formation are genetically programmed and can be modified by epigenetic and environmental influences. Such alterations may exert profound effects on neurodevelopment, potentially persisting throughout the lifespan. This review focuses on the critical period of fetal and early postnatal brain development. Here we collate findings from neuroimaging studies, with a particular focus on functional MRI research that interrogated early brain network development in both health and high-risk or disease states. First, we will provide an overview of the developmental processes that take place from the embryonic period through early infancy in order to contextualize brain network formation. Second, functional brain network development in the typically developing brain will be discussed. Third, we will touch on prenatal and perinatal risk factors that may interfere with the trajectories of functional brain wiring, including prenatal substance exposure, maternal mental illness and preterm

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Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans

Cited by 117 publications

References 68 publications

Metabolic costs and evolutionary implications of human brain development

Metabolic costs and evolutionary implications of human brain development

In the light of evolution VII: The human mental machinery

The emergence of functional architecture during early brain development

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