Brain growth, life history, and cognition in primate and human evolution

Leigh, Steven R.

doi:10.1002/ajp.20012

Cited by 331 publications

(297 citation statements)

References 49 publications

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“…To directly assess the extent of metabolic changes between human brain and brains of other primate species, we measured metabolite levels in postmortem PFC and CBC samples from 49 humans, 11 chimpanzees, and 45 rhesus macaques, using GC-MS (Table S1). Many phenotypic parameters, such as maximal life span, age of sexual maturity, and brain growth curves differ between humans, chimpanzees, and rhesus macaques (19,20). This makes it difficult to match samples with respect to age among these three species.…”

Section: Resultsmentioning

confidence: 99%

Rapid metabolic evolution in human prefrontal cortex

Giavalisco

Liu

et al. 2011

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

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Human evolution is characterized by the rapid expansion of brain size and drastic increase in cognitive capabilities. It has long been suggested that these changes were accompanied by modifications of brain metabolism. Indeed, human-specific changes on gene expression or amino acid sequence were reported for a number of metabolic genes, but actual metabolite measurements in humans and apes have remained scarce. Here, we investigate concentrations of more than 100 metabolites in the prefrontal and cerebellar cortex in 49 humans, 11 chimpanzees, and 45 rhesus macaques of different ages using gas chromatography-mass spectrometry (GC-MS). We show that the brain metabolome undergoes substantial changes, both ontogenetically and evolutionarily: 88% of detected metabolites show significant concentration changes with age, whereas 77% of these metabolic changes differ significantly among species. Although overall metabolic divergence reflects phylogenetic relationships among species, we found a fourfold acceleration of metabolic changes in prefrontal cortex compared with cerebellum in the human lineage. These human-specific metabolic changes are paralleled by changes in expression patterns of the corresponding enzymes, and affect pathways involved in synaptic transmission, memory, and learning.H uman evolution is characterized by rapid expansion of brain size and increase in cognitive capabilities, leading to the emergence of unique and complex cognitive skills. These changes have long been associated with changes in brain metabolism, in particular with respect to increased energy demand (1). Large brains are metabolically costly. Thus, humans allocate approximately 20% of their total energy to the brain, compared with 11-13% for apes and 2-8% for other mammalian species (2). This increased metabolic demand has been associated with elevated expression of genes involved in neuronal functions and energy metabolism (3, 4). These changes may have been evolutionary advantageous, as indicated by signatures of positive selection reported for the amino acid changes, which occur in the mitochondrial electron-transport chain proteins, in anthropoid primates and humans, as well as elevated expression of the energy metabolism pathways in the human brain (5, 6). On the histological level, human brains show the largest density of glia cells relative to neurons in the prefrontal cortex, which provides an indirect indication of increased neuronal metabolic demand (7).Changes in brain metabolism are also implicated in neuropsychiatric disorders, such as schizophrenia, which affect some of the human-specific cognitive abilities (8, 9). Furthermore, direct measurements of 21 metabolites in the prefrontal cortex of adult human controls compared with human schizophrenia patients, chimpanzees, and rhesus macaques, carried out using proton NMR spectroscopy have shown significant overlap between human-specific evolutionary changes and metabolic differences between controls and schizophrenia patients (10). Notably, this study has identified not ...

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Section: Resultsmentioning

confidence: 99%

Rapid metabolic evolution in human prefrontal cortex

Giavalisco

Liu

et al. 2011

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

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“…Humans are born in an altricial state and undergo both rapid and extended brain growth compared with that of macaques and chimpanzees (Leigh 2004). A related view is that human ontogeny has acquired a novel phase, between 3 and 7 yr of age, when human infants are not being breast-fed but are still highly dependent on adults (Bogin 1997).…”

Section: Discussionmentioning

confidence: 99%

“…The other lines and symbols show timing of life history landmarks: Lower and upper black dashed lines show the diagonal line passing through the origin and the maximum lifespan point, respectively. Empty gray circles represent the timing of human brain growth relative to that of chimpanzees, using the dynamic time warping algorithm (data from Leigh 2004). The symbols represent the following life history landmarks: maximum lifespan (orange), female sexual maturity (green), and eruption of first deciduous and last permanent dentition (dark and light purple, respectively) (data from Smith et al 1994;de Magalhães and Costa 2009).…”

Section: Regulation Of Human-specific Expression Patternsmentioning

confidence: 99%

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Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques

Liu¹,

Somel²,

Tang³

et al. 2012

Genome Res.

215

216

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Over the course of ontogenesis, the human brain and human cognitive abilities develop in parallel, resulting in a phenotype strikingly distinct from that of other primates. Here, we used microarrays and RNA-sequencing to examine human-specific gene expression changes taking place during postnatal brain development in the prefrontal cortex and cerebellum of humans, chimpanzees, and rhesus macaques. We show that the most prominent human-specific expression change affects genes associated with synaptic functions and represents an extreme shift in the timing of synaptic development in the prefrontal cortex, but not the cerebellum. Consequently, peak expression of synaptic genes in the prefrontal cortex is shifted from <1 yr in chimpanzees and macaques to 5 yr in humans. This result was supported by protein expression profiles of synaptic density markers and by direct observation of synaptic density by electron microscopy. Mechanistically, the human-specific change in timing of synaptic development involves the MEF2A-mediated activity-dependent regulatory pathway. Evolutionarily, this change may have taken place after the split of the human and the Neanderthal lineages.

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“…Energetic or material constraints during development have been recognized in several different model systems (e.g., Aiello and Wheeler, 1995;Nijhout and Emlen, 1998;Nowicki et al, 2002;Fish and Lockwood, 2003;Nowicki and Searcy, 2004;Leigh, 2004) and further study of potential constraints on marsupial brain development may provide an interesting case study of this general phenomenon.…”

Section: Discussion Conclusion and Prospective For Future Workmentioning

confidence: 99%

Craniofacial development in marsupial mammals: Developmental origins of evolutionary change

Smith

2006

Developmental Dynamics

102

119

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Biologists have long studied the evolutionary consequences of the differences in reproductive and life history strategies of marsupial and eutherian mammals. Over the past few decades, the impact of these strategies on the development of the marsupial embryo and neonate has received attention. In this review, the differences in development in the craniofacial region in marsupial and eutherian mammals will be discussed. The review will highlight differences at the organogenic and cellular levels, and discuss hypotheses for shifts in the expression of important regulatory genes. The major difference in the organogenic period is a whole-scale shift in the relative timing of central nervous system structures, in particular those of the forebrain, which are delayed in marsupials, relative to the structures of the oral-facial apparatus. Correlated with the delay in development of nervous system structures, the ossification of the bones of the neurocranium are delayed, while those of the face are accelerated. This study will also review work showing that the neural crest, which provides much of the cellular material to the facial skeleton and may also carry important patterning information, is notably accelerated in its development in marsupials. Potential consequences of these observations for hypotheses on constraint, evolutionary integration, and the existence of developmental modules is discussed. Finally, the implications of these results for hypotheses on the genetic modulation of craniofacial patterning are presented.

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Brain growth, life history, and cognition in primate and human evolution

Cited by 331 publications

References 49 publications

Rapid metabolic evolution in human prefrontal cortex

Rapid metabolic evolution in human prefrontal cortex

Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques

Craniofacial development in marsupial mammals: Developmental origins of evolutionary change

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