Metabolic costs and evolutionary implications of human brain development

Abstract

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 ...

Middle Childhood: An Evolutionary-Developmental Synthesis

“…This developmental pattern (shared by chimpanzees and, to a lesser extent, gorillas; Bernstein et al 2012) results in a temporary decoupling between physical and behavioral development, consistent with the idea of middle childhood as a sexually differentiated phase of social learning and experimentation (Geary 2010). Moreover, adrenal androgens promote extended brain plasticity through synaptogenesis and may play an important role in shifting the allocation of the body's energetic resources away from brain development and toward the accumulation of muscle and fat in preparation for puberty (Campbell 2006(Campbell , 2011; see also Kuzawa et al 2014). …”

“…By age 6, the brain has almost reached its maximum size and receives a decreasing share of the body's glucose after the consumption peak of early childhood ( Fig. 1; Giedd and Rapoport 2010;Kuzawa et al 2014). …”

The evolutionary roles of nutrition selection and dietary quality in the human brain size and encephalization

“…Human brain sizes are some 2.5-3 times those of other primates, and, in caloric terms, this means that brain metabolism accounts for~20-25% of resting metabolic rate (RMR) in an adult human body, as compared to about 8-10% in other primate species, and roughly 3-5% for nonprimate mammals. In humans, costs are even greater in infancy, with our brains consuming about 50% of the resting energy as newborns, 66% of RMR at age 4 years, as compared with 20% for adults [38]. The high energetic costs of the human brain highlight the importance of strong selective benefits to having a larger brain and enhanced cognitive abilities in human evolution [39,40].…”

“…Following this, our brain consumes 50% of the total energy intake as newborns, and 66% of RMR by age 4 years, as compared with 20% for adults. To accommodate for these high energetic demands of brain early in life, human infants are born with large quantities of body fat and show marked reductions in body weight growth around 4 years-the time during which brain energy demands are greatest [38].…”

Skeletal muscle-induced hypoglycemia risk, not life history energy trade-off, links high child brain glucose use to slow body growth

“…Kuzawa et al (1) find an "inverse relationship between the brain's demand for glucose and body-weight growth rate" that supports "the hypothesis that human brain development is sufficiently costly to require a compensatory reduction in expenditure on body growth". However, energy expenditure on body growth is low.…”