Abstract
Abstract1. After weaning, human hunter-gatherer juveniles receive substantial (≈3.5-7 MJ day^-1^), extended (≈15 years) and reliable (kin and nonkin food pooling) energy provision.2. The childhood (pediatric) and the adult human brain takes a very high share of both basal metabolic rate (BMR) (child: 50-70%; adult: ≈20%) and total energy expenditure (TEE) (child: 30-50%; adult: ≈10%).3. The pediatric brain for an extended period (≈4-9 years-of-age) consumes roughly 50% more energy than the adult one, and after this, continues during adolescence, at a high but declining rate. Within the brain, childhood cerebral gray matter has an even higher 1.9 to 2.2-fold increased energy consumption. 4. This metabolic expensiveness is due to (i) the high cost of synapse activation (74% of brain energy expenditure in humans), combined with (ii), a prolonged period of exuberance in synapse numbers (up to double the number present in adults). Cognitive development during this period associates with volumetric changes in gray matter (expansion and contraction due to metabolic related size alterations in glial cells and capillary vascularization), and in white matter (expansion due to myelination). 5. Amongst mammals, anatomically modern humans show an unique pattern in which very slow musculoskeletal body growth is followed by a marked adolescent size/stature spurt. This pattern of growth contrasts with nonhuman primates that have a sustained fast juvenile growth with only a minor period of puberty acceleration. The existence of slow childhood growth in humans has been shown to date back to 160,000 BP. 6. Human children physiologically have a limited capacity to protect the brain from plasma glucose fluctuations and other metabolic disruptions. These can arise in adults, during prolonged strenuous exercise when skeletal muscle depletes plasma glucose, and produces other metabolic disruptions upon the brain (hypoxia, hyperthermia, dehydration and hyperammonemia). These are proportional to muscle mass.7. Children show specific adaptations to minimize such metabolic disturbances. (i) Due to slow body growth and resulting small body size, they have limited skeletal muscle mass. (ii) They show other adaptations such as an exercise specific preference for free fatty acid metabolism. (iii) While children are generally more active than adolescents and adults, they avoid physically prolonged intense exertion. 8. Childhood has a close relationship to high levels of energy provision and metabolic adaptations that support prolonged synaptic neurodevelopment.
Highlights
The proportion of the body’s basal metabolic rate (BMR) devoted to the central nervous system (CNS) is highly conserved across mature vertebrates being 2.7-7.7% irrespective of vertebrate class, size, and thermoregulatory status (Mink, Blumenschine, & Adams, 1981). (The size BMR allometric function is unity (Mink et al, 1981) allowing discussion of percentages independent of body size.) In this context, it is notable that the proportion of energy allocated to the adult CNS is markedly increased in primates (>10%), and in modern humans (20%)
Volumetric MRI research shows that volume changes to gray matter have (i) a trajectory of initial increase followed by decrease, (ii) that these trajectory changes differ according to particular cerebral cortex area, and (iii) that these different trajectories in their thickening and thinning link with human specific cognitive capacities (Lenroot & Giedd, 2006; Shaw, 2007; Sowell et al, 2002)
The opportunity and the need for such complex integration and differentiation exists in part due to large brains in humans since size increases the number of cortical areas that have to be coordinated together: cortex area numbers expand at roughly the square root of the number of cerebral cortex neurons and so brain size (Changizi & Shimojo, 2005)
Summary
Modern humans (Homo sapiens sapiens) are often viewed as biologically unique in regard to possessing articulate thought, language and symbolic culture (human specific cognitive capabilities). Childhood cerebral gray matter has an even higher 1.9- to 2.2-fold increase in energy consumption (Chugani, 1998; Chugani, Phelps, & Mazziotta, 1987). This metabolic expensiveness is due to: i. Anatomically modern humans show an unique pattern in which of slow musculoskeletal body growth following by an adolescent size/stature spurt. (i) Due to its limited mass as result of slow growth and small body size. (ii) Its exertion metabolism is less anaerobic (i.e. nonoxidative glucose using) than in adults (Boisseau & Delamarche, 2000) (iii) Its exercise aerobic oxidization is biased to the metabolism of free fatty acids rather than the uptake of glucose (Timmons, Bar-Or, & Riddell, 2003). (iv) while children are more active than adolescents and adults (Sigmund, De Ste Croix, Miklankova, & Fromel, 2007), they minimize engagement in prolonged intense physical exertion (Bailey et al, 1995; Gilliam, Freedson, Geenen, & Shahraray, 1981)
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