Metabolic costs and evolutionary implications of human brain development

In the paper

“Studies report interactions between fetal undernutrition or small birth size and childhood weight gain as predictors of diabetes risk”

What the sources say

• ?Not checked — no full text of the sourcecites [62] 62. Ong KK (2006) Size at birth, postnatal growth and risk of obesity. Horm Res 65:(Suppl 3):65-69. source
• Disputed

  The Results section, “SGA and the associations of weight gain with outcomes” (page unavailable), directly tested whether small-for-gestational-age status or birth weight interacted with conditional weight gain. It found no significant interactions at any age. The paper reports birth weight and later weight gain as separate risk factors, not interacting predictors. (LLM, conf=0.91)

  Checked by a reasoning model — may be wrong.

  cites [63] 63. Norris SA, et al.; COHORTS Group (2012) Size at birth, weight gain in infancy and childhood, and adult diabetes risk in five low-or middle-income country birth co- horts. Diabetes Care 35(1):72-79. sourceExperimental — accuracy not yet measured

In the paper

“Rudimentary hunting and gathering economies appeared with the emergence of the genus Homo and are believed to have been important in supporting early brain expansion (49)(50)(51).”

What the sources say

• ?Not checked — no full text of the sourcecites [49] 49. Bunn H (2006) Meat made us human. Evolution of the Human Diet: The Known, the Unknown, and the Unknowable, ed Unger P (Oxford Univ Press, New York), pp 191-211. source
• Supported

  The ‘Bridging Subsistence and Sociality’ section describes early Homo foraging that included hunting or scavenging and plant foods, and links its first major increase in cranial capacity possibly to more animal tissue in the diet. The Conclusions identify meat and nutrient-dense plant foods as the likely diet fueling brain expansion in Homo. Page numbers are unavailable in our copy. (LLM, conf=0.87)

  cites [50] 50. Plummer T (2004) Flaked stones and old bones: Biological and cultural evolution at the dawn of technology. Am J Phys Anthropol 125(Suppl 39):118-164. source
• ?Not checked — no full text of the sourcecites [51] 51. Pobiner BL, Rogers MJ, Monahan CM, Harris JW (2008) New evidence for hominin carcass processing strategies at 1.5 Ma, Koobi Fora, Kenya. J Hum Evol 55(1):103-130. source

In the paper

“Data on dental eruption point to coevolution between brain expansion and maturational delay (45,46), with a fully modern pattern of delayed physical growth not emerging until the origin of anatomically modern humans (47,48).”

What the sources say

• ?Not checked — no full text of the sourcecites [45] 45. Dean MC, Lucas VS (2009) Dental and skeletal growth in early fossil hominins. Ann Hum Biol 36(5):545-561. source
• ?Not checked — no full text of the sourcecites [46] 46. Dean C, et al. (2001) Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414(6864):628-631. source
• Partly supported

  The Abstract identifies a 160,000-year-old early H. sapiens juvenile as the oldest-known Homo specimen with dental development more similar to modern humans than to earlier Homo. But it explicitly says when the prolonged modern human developmental pattern originated is unknown. The paper therefore supports evidence of delayed development in early H. sapiens, not the categorical claim that it first emerged with anatomically modern humans. (LLM, conf=0.88)

  cites [47] 47. Smith TM, et al. (2007) Earliest evidence of modern human life history in North African early Homo sapiens. Proc Natl Acad Sci USA 104(15):6128-6133. sourceExperimental — accuracy not yet measured
• ?Not checked — no full text of the sourcecites [48] 48. Smith TM, et al. (2010) Dental evidence for ontogenetic differences between modern humans and Neanderthals. Proc Natl Acad Sci USA 107(49):20923-20928. source

In the paper

“Recent work shows that glucose uptake outpaces oxygen use in the human brain, and that this imbalance also peaks at the age of greatest glucose uptake in childhood”

What the sources say

• Supported

  The Results section’s meta-analysis reports that brain glucose consumption exceeds the amount expected from oxygen consumption and that this excess peaks around age 5, when total glucose consumption is also highest. The Methods section explains that oxygen consumption was converted to its glucose equivalent for this comparison; the claim is not comparing the raw quantities in different units. (LLM, conf=0.92)

  cites [28] 28. Goyal MS, Hawrylycz M, Miller JA, Snyder AZ, Raichle ME (2014) Aerobic glycolysis in the human brain is associated with development and neotenous gene expression. Cell Metab 19(1):49-57. source
• ?Not checked — no full text of the sourcecites [30] 30. Bauernfeind AL, et al. (2014) Aerobic glycolysis in the primate brain: Reconsidering the implications for growth and maintenance. Brain Struct Funct 219(4):1149-1167. source

In the paper

“These patterns suggest that peak brain glucose uptake during childhood reflects neuronal plasticity in the cerebral cortex (32), which involves overproliferation of energetically costly dendritic arbors and synapses before activity-dependent pruning (33,34).”

What the sources say

• ?Not checked — no full text of the sourcecites [32] 32. Chugani HT, Phelps ME, Mazziotta JC (1987) Positron emission tomography study of human brain functional development. Ann Neurol 22(4):487-497. source
• Partly supported

  The opening section (p. 1) describes initially overproduced cortical synapses followed by activity-dependent selective elimination, and reports that prefrontal dendritic spine density in childhood is two to three times adult levels. It does not establish overproliferation of dendritic arbors or describe these structures as energetically costly. The glucose-uptake interpretation is attached to citation (32), not to this source's citation (33 or 34). (LLM, conf=0.87)

  cites [33] 33. Petanjek Z, et al. (2011) Extraordinary neoteny of synaptic spines in the human pre- frontal cortex. Proc Natl Acad Sci USA 108(32):13281-13286. sourceExperimental — accuracy not yet measured
• ?Not checked — no full text of the sourcecites [34] 34. Huttenlocher PR (1979) Synaptic density in human frontal cortex -Developmental changes and effects of aging. Brain Res 163(2):195-205. source

In the paper

“Pontzer et al. (43) recently showed that humans and other primates have reduced TEEs for their body sizes, despite having basal metabolic rates (BMRs) consistent with those of other mammals.”

What the sources say

• Supported

  The Results and Discussion report that primate TEE was about half that expected for body mass, while primate BMR was similar to that of other placental mammals. The same section notes marginally lower BMR in strepsirrhines, and the Submission PDF states that humans fit the low-TEE primate pattern. (LLM, conf=0.93)

  cites [43] 43. Pontzer H, et al. (2014) Primate energy expenditure and life history. Proc Natl Acad Sci USA 111(4):1433-1437. source

In the paper

“An additional limitation is that our analyses are based on cross-sectional brain and body-weight data, which pool fast-and slow-maturing individuals; this pooling can attenuate the apparent magnitude of the pubertal growth spurt while also obscuring the variable timings of its onset (65).”

What the sources say

• Partly supported

  The paper’s Abstract (page not supplied) says cross-sectional standards can mislead because some children have adolescent growth spurts early and others late, supporting the concern that pooling obscures individual timing. It also says the difference from longitudinal standards is especially marked for growth velocity, but does not state that pooling attenuates the apparent magnitude of the spurt. The citing authors’ description of their own brain and body-weight data is not a finding attributed to this source. (LLM, conf=0.82)

  cites [65] 65. Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51(3):170-179. sourceExperimental — accuracy not yet measured

In the paper

“Although normative data on developmental changes in insulin sensitivity during child development are lacking (64)”

What the sources say

• Supported

  In the section headed “2. Insulin resistance is a continuum” (page unavailable), the paper says cohort sizes are insufficient to establish normative distributions for insulin sensitivity in children. It also says separate standards would need to be developed for different pubertal stages, supporting the claim that normative developmental data are lacking. (LLM, conf=0.87)

  cites [64] 64. Levy-Marchal C, et al.; ESPE-LWPES-ISPAD-APPES-APEG-SLEP-JSPE; Insulin Resistance in Children Consensus Conference Group (2010) Insulin resistance in children: Con- sensus, perspective, and future directions. J Clin Endocrinol Metab 95(12):5189-5198. source

In the paper

“These values represent 1.88-and 1.82-times the daily glucose use of the brain in adulthood”

In the paper

“Very similar results were obtained when brain glucose was evaluated in relation to DER”

In the paper

“The childhood peak in brain glucose uptake is greatest in the cerebrum, and less pronounced in the brainstem and cerebellum (32).”

What the sources say

• ?Not checked — no full text of the sourcecites [32] 32. Chugani HT, Phelps ME, Mazziotta JC (1987) Positron emission tomography study of human brain functional development. Ann Neurol 22(4):487-497. source

In the paper

“Starting at 6 mo, each increase in glucose rmr% is matched by a proportionate decrease in dw/dt, with peak glucose rmr% and the trough of dw/dt cooccurring.”

In the paper

“when the glucose used by the brain comprises the equivalent of 66% of the body's RMR, and roughly 43% of total expenditure.”

In the paper

“In males and females, respectively, total brain glucose uptake is the equivalent of 52.5% and 59.8% of RMR at birth”

In the paper

“Adult glucose rmr% was 19.1% and 24.0% whereas glucose der% was 10.9% and 15.0% in males and females, respectively.”

In the paper

“before rising to peak levels of 43.3% at 3.8 y (males) and 43.8% at 4 y (females)”

In the paper

“Both glucose rmr% and glucose der% decline in the first halfyear as a fast but decelerating pace of body growth established in utero initially outpaces postnatal increases in brain metabolism.”

In the paper

“A shift to calorically dense and easily digested foods, and greater food sharing among social groups, would have increased the nutritional quality and stability of the diet (14,15,20).”

What the sources say

• ?Not checked — no full text of the sourcecites [14] 14. Foley RA, Lee PC (1991) Ecology and energetics of encephalization in hominid evo- lution. Philos Trans R Soc Lond B Biol Sci 334(1270):223-231, discussion 232. source
• ?Not checked — no full text of the sourcecites [15] 15. Leonard WR, Robertson ML (1992) Nutritional requirements and human evolution: A bioenergetics model. Am J Hum Biol 4(2):179-195. source
• ?Not checked — no full text of the sourcecites [20] 20. Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: The brain and the di- gestive system in human and primate evolution. Curr Anthropol 36(2):199-221. source

In the paper

“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).”

What the sources say

• ?Not checked — no full text of the sourcecites [44] 44. Bianchi S, et al. (2013) Synaptogenesis and development of pyramidal neuron den- dritic morphology in the chimpanzee neocortex resembles humans. Proc Natl Acad Sci USA 110(Suppl 2):10395-10401. source

In the paper

“Whereas past attempts to quantify the contribution of the brain to the body's metabolic expenditure suggested that the brain accounted for a continuously decreasing fraction of RMR as the brain-to-body weight ratio declined with age (25,31)”

What the sources say

• ?Not checked — no full text of the sourcecites [25] 25. Holliday MA (1986) Body composition and energy needs during growth. Human Growth: A Comprehensive Treatise, Vol 2 Postnatal Growth, eds Falkner F, Tanner JM (Plenum, New York), 2 Ed, pp 117-139. source
• ?Not checked — no full text of the sourcecites [31] 31. Holliday MA (1971) Metabolic rate and organ size during growth from infancy to maturity and during late gestation and early infancy. Pediatrics 47(Suppl 2):169-179. source

In the paper

“It is notable that the increase in body growth rate at puberty-which is unusually pronounced in humans-is deferred to an age when brain glucose uptake is greatly reduced (1,26,41).”

What the sources say

• ?Not matched

  Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  cites [1] 1. Bogin B (1999) Patterns of Human Growth (Cambridge Univ Press, Cambridge, UK), 2nd Ed.
• ?Not checked — no full text of the sourcecites [26] 26. Aiello LC, Wells JCK (2002) Energetics and the evolution of the genus Homo. Annu Rev Anthropol 31:323-328. source
• ?Not checked — no full text of the sourcecites [41] 41. Leigh SR (1996) Evolution of human growth spurts. Am J Phys Anthropol 101(4): 455-474. source

In the paper

“We interpret our finding of an inverse relationship between the brain's demand for glucose and body-weight growth rate as support for the hypothesis that human brain development is sufficiently costly to require a compensatory reduction in expenditure on body growth, thus helping explain our unusually slow rate of childhood growth and resultant delay in attainment of adult size and sexual maturity”

In the paper

“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).”

What the sources say

• ?Not checked — no full text of the sourcecites [22] 22. Leigh SR (2004) Brain growth, life history, and cognition in primate and human evolution. Am J Primatol 62(3):139-164. source

In the paper

“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.”

In the paper

“despite having similar cranial capacities, dental eruption data suggest that Neanderthals grew more rapidly than modern humans (48).”

What the sources say

• ?Not checked — no full text of the sourcecites [48] 48. Smith TM, et al. (2010) Dental evidence for ontogenetic differences between modern humans and Neanderthals. Proc Natl Acad Sci USA 107(49):20923-20928. source

In the paper

“It has been noted that the high and inflexible glucose requirements of the developing human brain make it susceptible to impairment from nutritional shortfall (18).”

What the sources say

• ?Not checked — no full text of the sourcecites [18] 18. Kuzawa CW (1998) Adipose tissue in human infancy and childhood: An evolutionary perspective. Am J Phys Anthropol 107(Suppl 27):177-209. source

In the paper

“and the latest World Health Organization (WHO) report on human energy requirements similarly finds that caloric needs for body growth are lowest at 4-5 y (38).”

What the sources say

• ?Not matched

  Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  cites [38] 38. Food and Agriculture Organization & World Health Organization (2004) Human En- ergy Requirements: Report of a Joint FAO/WHO/UNU Expert Consultation (Food and Agricultural Organization of the United Nations, Rome).

In the paper

“A system in which extended social networks provisioned food for children, combined with shifts to calorically dense and easily digested foods procured through hunting (14,15), would have allowed the costs of human brain development to be widely distributed and also buffered against shortfall.”

What the sources say

• ?Not checked — no full text of the sourcecites [14] 14. Foley RA, Lee PC (1991) Ecology and energetics of encephalization in hominid evo- lution. Philos Trans R Soc Lond B Biol Sci 334(1270):223-231, discussion 232. source
• ?Not checked — no full text of the sourcecites [15] 15. Leonard WR, Robertson ML (1992) Nutritional requirements and human evolution: A bioenergetics model. Am J Hum Biol 4(2):179-195. source

In the paper

“Changes in insulin secretion are believed to help coordinate glucose delivery to the brain as brain size and energy requirements change during development (60,61).”

What the sources say

• ?Not checked — no full text of the sourcecites [60] 60. Kubera B, et al. (2013) Energy allocation between brain and body during ontogenetic development. Am J Hum Biol 25(6):725-732. source
• ?Not checked — no full text of the sourcecites [61] 61. Peters A, et al. (2004) The selfish brain: Competition for energy resources. Neurosci Biobehav Rev 28(2):143-180. source

In the paper

“The lCMRGlc values in the 29 children were compared with those of the seven healthy young adult volunteers, whose detailed neurological and psychological examinations disclosed no abnormalities.”

In the paper

“Because RMR was estimated from WHO age-and sex- specific predictive equations, there were discontinuities at the ages corre- sponding to changes in the predictive equations (at 3 and 10 y of age) (SI Appendix, Fig. S4).”

What the sources say

• ?Not matched

  Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  cites [38] 38. Food and Agriculture Organization & World Health Organization (2004) Human En- ergy Requirements: Report of a Joint FAO/WHO/UNU Expert Consultation (Food and Agricultural Organization of the United Nations, Rome).

In the paper

“Written informed consent for the PET procedures was obtained directly from adult participants, and for minors, from parents, with institutional review board oversight by the University of California at Los Angeles Human Subject Protection Committee.”