Neonatal Brain Size Research Articles

Brain size growth in Australopithecus

Postnatal growth is one of the proximate means by which humans attain massive adult brain size. Humans are characterized by the maintenance of prenatal brain growth rates into the first postnatal year, as well as an overall extended period of growth. The evolution of this pattern is difficult to assess due to its relatively brief duration and the underrepresentation of well-preserved fossil individuals who died during this short period. In this study, I use Monte Carlo methods to reconstruct postnatal brain growth rates in Australopithecus afarensis and Australopithecus africanus, based on estimates of neonatal brain size and of likely brain size and age at death of infant specimens (A.L. 333-105, DIK-1-1, and Taung). Neonatal brain size is reconstructed from the empirical scaling relationship among catarrhines which humans follow, and conservative estimates of fossils' chronological ages and brain sizes are drawn from the literature. Simulated distributions of these values are used to calculate average annual rates (ARs) of brain growth and proportional size change from birth (PSC), which are compared to resampled statistics from humans, chimpanzees and gorillas of known age and sex. Simulated ARs and PSCs for A. afarensis are significantly lower than those of chimpanzees and gorillas. Both ARs and PSCs for A. africanus are similar to chimpanzee and gorilla values. These results indicate that although these early hominins were derived in some aspects of brain anatomy, high rates of brain growth did not appear until later in human evolution. Moreover, findings also imply that brain growth rates are not a simple function of adult brain size. This study provides important new information about the evolution of brain growth, despite limitations inherent in fossil samples.

Reconstruction of Two Mother-Infant Dyads and Obstetrical Consequences of the Mesolithic-Neolithic Transition: A Case Study from Lepenski Vir and Vlasac (Serbia)

The current world population of approximately seven billion people shows that despite the complexities of human birthing, the human species is thriving. Changes in human pelvic morphology resulting from bipedalism and encephalisation, often described as the “obstetric dilemma”, have made the birthing process extremely difficult and risky for both mothers and neonates. The major Mesolithic- Neolithic shift in lifestyle could have had important obstetric consequences. It is often hypothesised that the shift to an agricultural diet, with a lower protein content and higher glycaemic loading than the hunter-gatherer diet, could have led to a decrease in maternal height and an increase in neonatal birth weight, brain size and foetal-pelvic strain, which may have exacerbated the obstetric dilemma. The Mesolithic-Neolithic osteological collection from the Danube Gorges (7400-5500 cal BC, Balkans) provides material (2 pelvises and a neonate skull) to test this hypothesis by virtually reconstructing the fossil dyads and their foetal-pelvic relationship.We compared these dyads with a large obstetrical sample of mother-child dyads with a known birthing history, conducting a lineardiscriminant analysis in order to predict the most probable delivery outcomes for the prehistoric dyads. The results suggest that delivery was dystocic for the Mesolithic motherchild dyad and eutocic for the Neolithic mother-child dyad; obstetrically, the former is notably more efficient. However, due to the small sample size, further research is required with a larger series in order to determine whether the development of obstetrically efficient pelvic bones in the Neolithic was widespread and whether it had an impact on the birthing process and thus potentially contributed to the increasing size of the population.

Prenatal and early postnatal measures of brain development and childhood sleep patterns.

BackgroundBrain development underlies maturation of sleep patterns throughout childhood. Intrauterine head growth-marker of early neurodevelopment-has not been associated with childhood sleep characteristics. We explored associations between ultrasonographic measures of prenatal and early postnatal neurodevelopment and childhood sleep.MethodsA total of 6,808 children from a population-based birth cohort (Generation R) were included. Head circumference (HC) and lateral ventricles size were assessed with mid- and late-pregnancy fetal ultrasounds, and with cranial ultrasound 3-20 weeks postnatally. Mothers reported children's sleep duration at 2 and 3 years, and sleep problems at 1.5, 3, and 6 years.ResultsLarger ventricular size, but not HC, was related to longer sleep duration at 3 years (β=0.06 h, 95% confidence interval (CI): 0.02; 0.10 in late-pregnancy and β=0.11 h, 95% CI: 0.02; 0.20 in early infancy, mid-pregnancy parameters were unrelated to sleep duration). Larger HC in mid-pregnancy was associated with a reduced risk for being a "problematic sleeper" up to the age of 6 years (odds ratio (OR): 0.94, 95% CI: 0.89; 0.99). Consistently, children with larger HC in early infancy were less likely to be "problematic sleepers" at 3 and 6 years.ConclusionsThis study shows that variations in fetal and neonatal brain size may underlie behavioral expression of sleep in childhood. Albeit small effect estimates, these associations provide evidence for neurodevelopmental origins of sleep.

Delphinid brain development from neonate to adulthood with comparisons to other cetaceans and artiodactyls

AbstractWhy do neonatal and adult delphinids have much larger brains than artiodactyls when they have common ancestors? We explore relationships between neonatal brain size, gestation duration, maternal body mass, and body growth. Cetacean brains grow fast in the womb and longer gestation results in a larger brain. Allometry shows that the larger the mother's body mass, the larger the neonatal brain. After birth, delphinid bodies grow much faster than brains, and the index of encephalization decreases even as brains grow beyond maturity. Delphinids’ larger brain growth during life at sea may be explained by at least three differences from artiodactyls’ life on land. First, the sea offers high calorie prey to support growth of a large brain. Second, life in water offers relief from gravity, allowing for a large head to contain a large brain. Third, sound in water may pass through an immersed body. This allows sounds from the water to reach the fetus, driving early development of delphinoid auditory brain parts. As an example of this, the dolphin ear bone is very large at birth. Furthermore, the auditory nervous system appears mature well before birth. Compared with artiodactyls, these three differences likely result in a larger delphinid brain.

Minimal variation in eutherian brain growth rates during fetal neurogenesis.

A central question in the evolution of brain development is whether species differ in rates of brain growth during fetal neurogenesis. Studies of neonatal data have found allometric evidence for brain growth rate differences according to physiological variables such as relative metabolism and placental invasiveness, but these findings have not been tested against fetal data directly. Here, we measure rates of exponential brain growth acceleration in 10 eutherian mammals, two marsupials, and two birds. Eutherian brain acceleration exhibits minimal variation relative to body and visceral organ growth, varies independently of correlated growth patterns in other organs, and is unrelated to proposed physiological constraints such as metabolic rate or placental invasiveness. Brain growth rates in two birds overlap with eutherian variation, while marsupial brain growth is exceptionally slow. Peak brain growth velocity is linked in time with forebrain myelination and eye opening, reliably separates altricial species born before it from precocial species born afterwards, and is an excellent predictor of adult brain size (r2 = 0.98). Species with faster body growth exhibit larger relative brain size in early ontogeny, while brain growth is unrelated to allometric measures. These findings indicate a surprising conservation of brain growth rates during fetal neurogenesis in eutherian mammals, clarify sources of variation in neonatal brain size, and suggest that slow body growth rates cause species to be more encephalized at birth.

Rapid and reliable tract-based spatial statistics pipeline for diffusion tensor imaging in the neonatal brain: Applications to the white matter development and lesions

PurposeThe relatively poor image contrast and variation in the neonatal brain size are technical challenges associated with the typical tract-based spatial statistics (TBSS) for the target identification and normalization. This study aimed to develop a rapid and reliable pipeline for the neonatal TBSS. Materials and methodsA rapid TBSS strategy was proposed based on the group-wise target choice for fractional anisotropy (FA) derived from diffusion tensor imaging (DTI). The most representative subject of the entire group was identified via (a) initial group-averaged template creation (b) followed by identification of the target with the minimum warp displacement score between the individual and the group-averaged template. The computation time, registration quality, measurement of regional values, and statistical analyses were evaluated in two applications: brain white matter development in normal term neonates, and alterations in preterm neonates with white matter lesions compared to the matched controls. These performances in the proposed pipeline were compared with those in the typical and previous neonatal TBSS workflows. ResultsTarget choice using the proposed strategy is faster, compared with the previous TBSS pipelines, especially with the increase of the sample size. Registration errors between individuals and the target are assessed through warp displacement scores. Smaller warp displacement scores are observed for the proposed method than the typical pipeline. Due to the relatively accurate registration, the proposed method results in lower standard deviations and higher averaged values of FA across subjects. Additionally, more areas with significant changes related to the development and white matter lesions are detected using the proposed method than previous TBSS pipelines. The proposed pipeline provides stronger correlation between FA and gestational age, and larger difference between preterm neonates with white matter lesions and controls. ConclusionThe proposed TBSS pipeline improves the efficiency and reliability of the DTI analysis in the neonatal brain.

The evolution of the human pelvis: changing adaptations to bipedalism, obstetrics and thermoregulation.

The fossil record of the human pelvis reveals the selective priorities acting on hominin anatomy at different points in our evolutionary history, during which mechanical requirements for locomotion, childbirth and thermoregulation often conflicted. In our earliest upright ancestors, fundamental alterations of the pelvis compared with non-human primates facilitated bipedal walking. Further changes early in hominin evolution produced a platypelloid birth canal in a pelvis that was wide overall, with flaring ilia. This pelvic form was maintained over 3-4 Myr with only moderate changes in response to greater habitat diversity, changes in locomotor behaviour and increases in brain size. It was not until Homo sapiens evolved in Africa and the Middle East 200 000 years ago that the narrow anatomically modern pelvis with a more circular birth canal emerged. This major change appears to reflect selective pressures for further increases in neonatal brain size and for a narrow body shape associated with heat dissipation in warm environments. The advent of the modern birth canal, the shape and alignment of which require fetal rotation during birth, allowed the earliest members of our species to deal obstetrically with increases in encephalization while maintaining a narrow body to meet thermoregulatory demands and enhance locomotor performance.

Microcephaly genes evolved adaptively throughout the evolution of eutherian mammals

BackgroundGenes associated with the neurodevelopmental disorder microcephaly display a strong signature of adaptive evolution in primates. Comparative data suggest a link between selection on some of these loci and the evolution of primate brain size. Whether or not either positive selection or this phenotypic association are unique to primates is unclear, but recent studies in cetaceans suggest at least two microcephaly genes evolved adaptively in other large brained mammalian clades.ResultsHere we analyse the evolution of seven microcephaly loci, including three recently identified loci, across 33 eutherian mammals. We find extensive evidence for positive selection having acted on the majority of these loci not just in primates but also across non-primate mammals. Furthermore, the patterns of selection in major mammalian clades are not significantly different. Using phylogenetically corrected comparative analyses, we find that the evolution of two microcephaly loci, ASPM and CDK5RAP2, are correlated with neonatal brain size in Glires and Euungulata, the two most densely sampled non-primate clades.ConclusionsTogether with previous results, this suggests that ASPM and CDK5RAP2 may have had a consistent role in the evolution of brain size in mammals. Nevertheless, several limitations of currently available data and gene-phenotype tests are discussed, including sparse sampling across large evolutionary distances, averaging gene-wide rates of evolution, potential phenotypic variation and evolutionary reversals. We discuss the implications of our results for studies of the genetic basis of brain evolution, and explicit tests of gene-phenotype hypotheses.

Pandora's growing box: Inferring the evolution and development of hominin brains from endocasts

The brain of modern humans is an evolutionary and developmental outlier: At birth, it has the size of an adult chimpanzee brain and expands by a factor of 2 during the first postnatal year. Large neonatal brain size and rapid initial growth contrast with slow maturation, which extends well into adolescence. When, how, and why this peculiar pattern of brain ontogeny evolved and how it is correlated with structural changes in the brain are key questions of paleoanthropology. Because brains and their ontogenies do not fossilize, indirect evidence from fossil hominin endocasts needs to be combined with evidence from modern humans and our closest living relatives, the great apes. New fossil finds permit a denser sampling of hominin endocranial morphologies along ontogenetic and evolutionary time lines. New brain imaging methods provide the basis for quantifying endocast-brain relationships and tracking endocranial and brain growth and development noninvasively. Combining this evidence with ever-more detailed knowledge about actual and fossil "brain genes," we are now beginning to understand how brain ontogeny and structure were modified during human evolution and what the adaptive significance of these modifications may have been.

L’accouchement de nos ancêtres était-il dystocique ?

The aim of this study was to assess the risk of foetal-pelvic disproportion in extinct hominins through a comparison of current obstetrical data with fossil data. For the modern sample, we collected pelvic diameters, foetal cranial diameters and delivery outcomes from 92 obstetrical cases (spontaneous vaginal, N = 43; c-section for foetal-pelvic disproportion, N = 34; operative vaginal, N = 15). For the fossil sample, the diameters of 12 pelvises and 6 juvenile skulls were gathered from the literature. Our estimations of neonatal skull sizes were based on (1) juvenile skull measurements and cranial growth curves and (2) the neonatal brain size estimations of DeSilva and Lesnik (2008). A linear discriminant analysis (LDA) was performed on the obstetrical cases. Despite a 35% misclassification error, the results showed a vaginal delivery range, an obstructed delivery range and an intermediate range where delivery outcomes were unpredictable. The multiple combinations between pelvic reconstructions and neonatal cranial estimations were projected onto the LDA and were mostly within the range of normal labour, with probabilities being within the range of normal labour (eutocia) at 0.99 ± 0.01 for Australopithecines; 0.76 ± 0.15 for Homo erectus s.l.; and 0.86 ± 0.08 for Neandertals.

Positive selection on NIN, a gene involved in neurogenesis, and primate brain evolution

A long-held dogma in comparative neurobiology has been that the number of neurons under a given area of cortical surface is constant. As such, the attention of those seeking to understand the genetic basis of brain evolution has focused on genes with functions in the lateral expansion of the developing cerebral cortex. However, new data suggest that cortical cytoarchitecture is not constant across primates, raising the possibility that changes in radial cortical development played a role in primate brain evolution. We present the first analysis of a gene with functions relevant to this dimension of brain evolution. We show that NIN, a gene necessary for maintaining asymmetric, neurogenic divisions of radial glial cells (RGCs), evolved adaptively during anthropoid evolution. We explored how this selection relates to neural phenotypes and find a significant association between selection on NIN and neonatal brain size in catarrhines. Our analyses suggest a relationship with prenatal neurogenesis and identify the human data point as an outlier, possibly explained by postnatal changes in development on the human lineage. A similar pattern is found in platyrrhines, but the highly encephalized genus Cebus departs from the general trend. We further show that the evolution of NIN may be associated with variation in neuron number not explained by increases in surface area, a result consistent with NIN's role in neurogenic divisions of RGCs. Our combined results suggest a role for NIN in the evolution of cortical development.

Placentation and Maternal Investment in Mammals

The mammalian placenta exhibits striking interspecific morphological variation, yet the implications of such diversity for reproductive strategies and fetal development remain obscure. More invasive hemochorial placentas, in which fetal tissues directly contact the maternal blood supply, are believed to facilitate nutrient transfer, resulting in higher fetal growth rates, and to be a state of relative fetal advantage in the evolution of maternal-offspring conflict. The extent of interdigitation between maternal and fetal tissues has received less attention than invasiveness but is also potentially important because it influences the surface area for exchange. We show that although increased placental invasiveness and interdigitation are both associated with shorter gestations, interdigitation is the key variable. Gestation times associated with highly interdigitated labyrinthine placentas are 44% of those associated with less interdigitated villous and trabecular placentas. There is, however, no relationship between placental traits and neonatal body and brain size. Hence, species with more interdigitated placentas produce neonates of similar body and brain size but in less than half the time. We suggest that the effects of placental interdigitation on growth rates and the way that these are traded off against gestation length may be promising avenues for understanding the evolutionary dynamics of parent-offspring conflict.

Adaptive Evolution of Four Microcephaly Genes and the Evolution of Brain Size in Anthropoid Primates

The anatomical basis and adaptive function of the expansion in primate brain size have long been studied; however, we are only beginning to understand the genetic basis of these evolutionary changes. Genes linked to human primary microcephaly have received much attention as they have accelerated evolutionary rates along lineages leading to humans. However, these studies focus narrowly on apes, and the link between microcephaly gene evolution and brain evolution is disputed. We analyzed the molecular evolution of four genes associated with microcephaly (ASPM, CDK5RAP2, CENPJ, MCPH1) across 21 species representing all major clades of anthropoid primates. Contrary to prevailing assumptions, positive selection was not limited to or intensified along the lineage leading to humans. In fact we show that all four loci were subject to positive selection across the anthropoid primate phylogeny. We developed clearly defined hypotheses to explicitly test if selection on these loci was associated with the evolution of brain size. We found positive relationships between both CDK5RAP2 and ASPM and neonatal brain mass and somewhat weaker relationships between these genes and adult brain size. In contrast, there is no evidence linking CENPJ and MCPH1 to brain size evolution. The stronger association of ASPM and CDK5RAP2 evolution with neonatal brain size than with adult brain size is consistent with these loci having a direct effect on prenatal neuronal proliferation. These results suggest that primate brain size may have at least a partially conserved genetic basis. Our results contradict a previous study that linked adaptive evolution of ASPM to changes in relative cortex size; however, our analysis indicates that this conclusion is not robust. Our finding that the coding regions of two widely expressed loci has experienced pervasive positive selection in relation to a complex, quantitative developmental phenotype provides a notable counterexample to the commonly asserted hypothesis that cis-regulatory regions play a dominant role in phenotypic evolution.

On the genetic architecture of cortical folding and brain volume in primates

Understanding the evolutionary forces that produced the human brain is a central problem in neuroscience and human biology. Comparisons across primate species show that both brain volume and gyrification (the degree of folding in the cerebral cortex) have progressively increased during primate evolution and there is a strong positive correlation between these two traits across primate species. The human brain is exceptional among primates in both total volume and gyrification, and therefore understanding the genetic mechanisms influencing variation in these traits will improve our understanding of a landmark feature of our species. Here we show that individual variation in gyrification is significantly heritable in both humans and an Old World monkey (baboons, Papio hamadryas). Furthermore, contrary to expectations based on the positive phenotypic correlation across species, the genetic correlation between cerebral volume and gyrification within both humans and baboons is estimated as negative. These results suggest that the positive relationship between cerebral volume and cortical folding across species cannot be explained by one set of selective pressures or genetic changes. Our data suggest that one set of selective pressures favored the progressive increase in brain volume documented in the primate fossil record, and that a second independent selective process, possibly related to parturition and neonatal brain size, may have favored brains with progressively greater cortical folding. Without a second separate selective pressure, natural selection favoring increased brain volume would be expected to produce less folded, more lissencephalic brains. These results provide initial evidence for the heritability of gyrification, and possibly a new perspective on the evolutionary mechanisms underlying long-term changes in the nonhuman primate and human brain.

When did the modern human pattern of childbirth arise? New insights from an old Neandertal pelvis

Human birthing is difficult owing to a tradeoff between large neonatal brain size and maternal pelvic dimensions, which are constrained by aspects of bipedal biomechanics (1, 2). The net effect is that human neonatal head size closely matches maternal pelvic dimensions, unlike in our closest living relatives, the great apes, whose pelvic dimensions are larger than neonatal head sizes. This size relationship, along with a twisted birth canal shape, makes human parturition mechanically difficult and results in a unique pattern of “rotational” birth (Fig. 1). As in humans, and unlike great apes, monkey neonatal head size closely matches the mother's pelvic dimensions. Although birth rotation occurs in some monkeys, the rotation pattern is different from that in modern humans, with monkey neonates exiting the birth canal facing forward (1). Therefore, in both apes and monkeys, it is relatively easy for a mother to guide her infant out of the birth canal, keep the umbilical cord from wrapping around the neck, and extract mucous from the nose and mouth to facilitate breathing. All of these critical activities are much more difficult for a human mother, whose infant emerges facing backwards, and pulling on the infant from this position also risks serious neck injury. For these reasons, humans uniquely engage in assisted birth (obligate midwifery). Although unassisted birth, the norm for nonhuman primates, does occasionally occur in humans, assisted birth and its myriad social implications are the human norm cross-culturally (1).

Neanderthal brain size at birth provides insights into the evolution of human life history

From birth to adulthood, the human brain expands by a factor of 3.3, compared with 2.5 in chimpanzees [DeSilva J and Lesnik J (2006) Chimpanzee neonatal brain size: Implications for brain growth in Homo erectus. J Hum Evol 51: 207-212]. How the required extra amount of human brain growth is achieved and what its implications are for human life history and cognitive development are still a matter of debate. Likewise, because comparative fossil evidence is scarce, when and how the modern human pattern of brain growth arose during evolution is largely unknown. Virtual reconstructions of a Neanderthal neonate from Mezmaiskaya Cave (Russia) and of two Neanderthal infant skeletons from Dederiyeh Cave (Syria) now provide new comparative insights: Neanderthal brain size at birth was similar to that in recent Homo sapiens and most likely subject to similar obstetric constraints. Neanderthal brain growth rates during early infancy were higher, however. This pattern of growth resulted in larger adult brain sizes but not in earlier completion of brain growth. Because large brains growing at high rates require large, late-maturing, mothers [Leigh SR and Blomquist GE (2007) in Campbell CJ et al. Primates in perspective; pp 396-407], it is likely that Neanderthal life history was similarly slow, or even slower-paced, than in recent H. sapiens.

Brain size at birth throughout human evolution: A new method for estimating neonatal brain size in hominins

An increase in brain size is a hallmark of human evolution. Questions regarding the evolution of brain development and obstetric constraints in the human lineage can be addressed with accurate estimates of the size of the brain at birth in hominins. Previous estimates of brain size at birth in fossil hominins have been calculated from regressions of neonatal body or brain mass to adult body mass, but this approach is problematic for two reasons: modern humans are outliers for these regressions, and hominin adult body masses are difficult to estimate. To accurately estimate the brain size at birth in extinct human ancestors, an equation is needed for which modern humans fit the anthropoid regression and one in which the hominin variable entered into the regression equation has limited error. Using phylogenetically sensitive statistics, a resampling approach, and brain-mass data from the literature and from National Primate Research Centers on 362 neonates and 2802 adults from eight different anthropoid species, we found that the size of the adult brain can strongly predict the size of the neonatal brain ( r 2 = 0.97). This regression predicts human brain size, indicating that humans have precisely the brain size expected as an adult given the size of the brain at birth. We estimated the size of the neonatal brain in fossil hominins from a reduced major axis regression equation using published cranial capacities of 89 adult fossil crania. We suggest that australopiths gave birth to infants with cranial capacities that were on average 180 cc (95% CI: 158–205 cc), slightly larger than the average neonatal brain size of chimpanzees. Neonatal brain size increased in early Homo to 225 cc (95% CI: 198–257 cc) and in Homo erectus to approximately 270 cc (95% CI: 237–310 cc). These results have implications for interpreting the evolution of the birth process and brain development in all hominins from the australopiths and early Homo, through H. erectus, to Homo sapiens.

Chimpanzee neonatal brain size: Implications for brain growth in Homo erectus

Chimpanzee neonatal brain size: Implications for brain growth in Homo erectus

Evolution of the human menopause.

Menopause is an evolutionary puzzle since an early end to reproduction seems contrary to maximising Darwinian fitness. Several theories have been proposed to explain why menopause might have evolved, all based on unusual aspects of the human life history. One theory is that menopause follows from the extreme altriciality of human babies, coupled with the difficulty in giving birth due to the large neonatal brain size and the growing risk of child-bearing at older ages. There may be little advantage for an older mother in running the increased risk of a further pregnancy when existing offspring depend critically on her survival. An alternative theory is that within kin groups menopause enhances fitness by producing post-reproductive grandmothers who can assist their adult daughters. Such theories need careful quantitative assessment to see whether the fitness benefits are sufficient to outweigh the costs, particularly in circumstances of relatively high background mortality typical of ancestral environments. We show that individual theories fail this test, but that a combined model incorporating both hypotheses can explain why menopause may have evolved.

Pelvic sexual dimorphism and relative neonatal brain size really are related

Primate species in which the neonatal brain size is large relative to the birth canal tend to have more sexually dimorphic pelves: this is a classic comparative relation, discovered by Schultz and Leutenegger. The original work did not correct for phylogenetic nonindependence of the data points; it only partly corrected for body size; it used ratios in both variables, and the size of the female pubis featured in both x- and y-variables. A recent publication by Tague placed a question mark over the validity of the relation. I therefore retested it, correcting for all four statistical defects. A strongly significant statistical relation exists.