Variations and asymmetries in regional brain surface in the genus Homo

Paleoneurology is an important field of research within human evolution studies. Variations in size and shape of an endocast help to differentiate among fossil hominin species whereas endocranial asymmetries are related to behavior and cognitive function. Here we analyse variations of the surface of the frontal, parieto-temporal and occipital lobes among different species of Homo, including 39 fossil hominins, ten fossil anatomically modern Homo sapiens and 100 endocasts of extant modern humans. We also test for the possible asymmetries of these features in a large sample of modern humans and observe individual particularities in the fossil specimens.This study contributes important new information about the brain evolution in the genus Homo. Our results show that the general pattern of surface asymmetry for the different regional brain surfaces in fossil species of Homo does not seem to be different from the pattern described in a large sample of anatomically modern H. sapiens, i.e., the right hemisphere has a larger surface than the left, as do the right frontal, the right parieto-temporal and the left occipital lobes compared with the contra-lateral side. It also appears that Asian Homo erectus specimens are discriminated from all other samples of Homo, including African and Georgian specimens that are also sometimes included in that taxon. The Asian fossils show a significantly smaller relative size of the parietal and temporal lobes. Neandertals and anatomically modern H. sapiens, who share the largest endocranial volume of all hominins, show differences when considering the relative contribution of the frontal, parieto-temporal and occipital lobes. These results illustrate an original variation in the pattern of brain organization in hominins independent of variations in total size. The globularization of the brain and the enlargement of the parietal lobes could be considered derived features observed uniquely in anatomically modern H. sapiens.     

A Shared Pattern of Postnatal Endocranial Development in Extant Hominoids

By comparing species-specific developmental patterns, we can approach the question of how development shapes adult morphology and contributes to the evolution of novel forms. Studies of evolutionary changes to brain development in primates can provide important clues about the emergence of human cognition, but are hindered by the lack of preserved neural tissue in the fossil record. As a proxy, we study the shape of endocasts, virtual imprints of the endocranial cavity, using 3D geometric morphometrics. We have previously demonstrated that the pattern of endocranial shape development is shared by modern humans, chimpanzees and Neanderthals after the first year of life until adulthood. However, whether this represents a common hominoid mode of development is unknown. Here, we present the first characterization and comparison of ontogenetic endocranial shape changes in a cross-sectional sample of modern humans, chimpanzees, gorillas, orangutans and gibbons. Using developmental simulations, we demonstrate that from late infancy to adulthood ontogenetic trajectories are similar among all hominoid species, but differ in the amount of shape change. Furthermore, we show that during early ontogeny gorillas undergo more pronounced shape changes along this shared trajectory than do chimpanzees, indicative of a dissociation of size and shape change. As shape differences between species are apparent in even our youngest samples, our results indicate that the ontogenetic trajectories of extant hominoids diverged at an earlier stage of ontogeny but subsequently converge following the eruption of the deciduous dentition.     

Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts

Modern humans are characterized by their large, complex, and specialized brain. Human brain evolution can be addressed through direct evidence provided by fossil hominid endocasts (i.e. paleoneurology), or through indirect evidence of extant species comparative neurology. Here we use the second approach, providing an extant comparative framework for hominid paleoneurological studies. We explore endocranial size and shape differences among great apes and humans, as well as between sexes. We virtually extracted 72 endocasts, sampling all extant great ape species and modern humans, and digitized 37 landmarks on each for 3D generalized Procrustes analysis. All species can be differentiated by their endocranial shape. Among great apes, endocranial shapes vary from short (orangutans) to long (gorillas), perhaps in relation to different facial orientations. Endocranial shape differences among African apes are partly allometric. Major endocranial traits distinguishing humans from great apes are endocranial globularity, reflecting neurological reorganization, and features linked to structural responses to posture and bipedal locomotion. Human endocasts are also characterized by posterior location of foramina rotunda relative to optic canals, which could be correlated to lesser subnasal prognathism compared to living great apes. Species with larger brains (gorillas and humans) display greater sexual dimorphism in endocranial size, while sexual dimorphism in endocranial shape is restricted to gorillas, differences between males and females being at least partly due to allometry. Our study of endocranial variations in extant great apes and humans provides a new comparative dataset for studies of fossil hominid endocasts.     

Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo

Paleoneurology concerns the study and analysis of fossil endocasts. Together with cranial capacity and discrete anatomical features, shape can be analysed to consider the spatial relationships between structures and to investigate the endocranial structural system. A sample of endocasts from fossil specimens of the genus Homo has been analysed using traditional metrics and 2D geometric morphometrics based on lateral projections of endocranial shape. The maximum and frontal widths show a size-related pattern of variation shared by all the taxa considered. Furthermore, as cranial capacity increases in the non-modern morphotypes there is a general endocranial vertical stretching (mainly centred at the anterior ascending circumvolution) with flattening and relative shortening of the parietal areas. This pattern could have involved some structural stress between brain development and vault bones at the parietal midsagittal profile in the heavy encephalised Neandertals. In contrast, modern humans show a species-specific neomorphic hypertrophy of the parietal volumes, leading to a dorsal growth and ventral flexion (convolution) and consequent globularity of the whole structure. Brain tensors such as the falx cerebri have been hypothesised to represent one of the main physical constraints on morphogenetic trajectories, with additional influences from cranial base structures. The neurofunctional inferences discussed here stress the role of the parietal areas in the visuo-spatial coordination and integration, which can be involved in higher cerebral functions and related to conceptual thinking.     

Brain Size Growth and Life History in Human Evolution

Increases in endocranial volume (a measure of brain size) play a major role in human evolution. Despite the importance of brain size increase, the developmental bases of human brain size evolution remain poorly characterized. Comparative analyses of endocranial volume size growth illustrate that distinctions between humans and other primates are consequences of differences in rates of brain size growth, with little evidence for differences in growth duration. Evaluation of available juvenile fossils shows that earliest hominins do not differ perceptibly from chimpanzees (Pan). However, rapid and human-like early brain growth apparently characterized Homo erectus at about 1?Ma before present. Neandertals show patterns of brain growth consistent with modern humans during infancy, but reach larger sizes than modern humans as a result of differences in later growth. Growth analyses reveal commonalities in patterns of early brain size growth during the last million years human evolution, despite major increases in adult size. This result implies consistency across hominins in terms of maternal metabolic costs of infancy. Continued size growth past infancy in Neandertals and modern humans, when compared to earlier hominins, may have cognitive implications. Differences between Neandertals and modern humans are implied, but difficult to define with certainty.     

Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects

Compared to our closest living and extinct relatives, humans have a large, specialized, and complex brain embedded in a uniquely shaped braincase. Here, we quantitatively compare endocranial shape changes during ontogeny in humans and chimpanzees. Identifying shared and unique aspects in developmental patterns of these two species can help us to understand brain evolution in the hominin lineage.Using CT scans of 58 humans and 60 chimpanzees varying in age from birth to adulthood, we generated virtual endocasts to measure and analyze 29 three-dimensional endocranial landmarks and several hundred semilandmarks on curves and the endocranial surface; these data were then analyzed using geometric morphometric methods.The ontogenetic shape trajectories are nonlinear for both species, which indicates several developmental phases. Endocranial shape is already distinct at birth and there is no overlap between the two species throughout ontogeny. While some aspects of the pattern of endocranial shape change are shared between humans and chimpanzees, the shape trajectories differ substantially directly after birth until the eruption of the deciduous dentition: in humans but not in chimpanzees, the parietal and cerebellar regions expand relatively (contributing to neurocranial globularity) and the cranial base flexes within the first postnatal year when brain growth rates are high. We show that the shape changes associated with this early “globularization phase” are unique to humans and do not occur in chimpanzees before or after birth.     

Endocranial volume of Australopithecus africanus: new CT-based estimates and the effects of missing data and small sample size

Estimation of endocranial volume in Australopithecus africanus is important in interpreting early hominin brain evolution. However, the number of individuals available for investigation is limited and most of these fossils are, to some degree, incomplete and/or distorted. Uncertainties of the required reconstruction (‘missing data uncertainty’) and the small sample size (‘small sample uncertainty’) both potentially bias estimates of the average and within-group variation of endocranial volume in A. africanus.We used CT scans, electronic preparation (segmentation), mirror-imaging and semilandmark-based geometric morphometrics to generate and reconstruct complete endocasts for Sts 5, Sts 60, Sts 71, StW 505, MLD 37/38, and Taung, and measured their endocranial volumes (EV). To get a sense of the reliability of these new EV estimates, we then used simulations based on samples of chimpanzees and humans to: (a) test the accuracy of our approach, (b) assess missing data uncertainty, and (c) appraise small sample uncertainty.Incorporating missing data uncertainty of the five adult individuals, A. africanus was found to have an average adult endocranial volume of 454-461 ml with a standard deviation of 66-75 ml. EV estimates for the juvenile Taung individual range from 402 to 407 ml. Our simulations show that missing data uncertainty is small given the missing portions of the investigated fossils, but that small sample sizes are problematic for estimating species average EV. It is important to take these uncertainties into account when different fossil groups are being compared.     

The Evolution of Human Brain Development

The human brain is a large and complex organ, setting us apart from other primates. It allows us to exhibit highly sophisticated cognitive and behavioral abilities. Therefore, our brain??s size and morphology are defining features of our species and our fossil ancestors and relatives. Endocasts, i.e., internal casts of the bony braincase, provide evidence about brain size and morphology in fossils. Based on endocasts, we know that our ancestors?? brains increased overall in size and underwent several reorganizational changes. However, it is difficult to relate evolutionary changes of size and shape of endocasts to evolutionary changes of cognition and behavior. We argue here that an understanding of the tempo and mode of brain development can help to interpret the evolution of our brain and the associated cognitive and behavioral changes. To do so, we review structural brain development, cognitive development, and ontogenetic changes of endocranial size and shape in living individuals on the one hand, and ontogenetic patterns (size increase and shape change) in fossil hominins and their evolutionary change on the other hand. Tightly integrating our knowledge on these different levels will be the key of future work on the evolution of human brain development.     

Unconstrained cranial evolution in Neandertals and modern humans compared to common chimpanzees

A variety of lines of evidence support the idea that neutral evolutionary processes (genetic drift, mutation) have been important in generating cranial differences between Neandertals and modern humans. But how do Neandertals and modern humans compare with other species? And how do these comparisons illuminate the evolutionary processes underlying cranial diversification? To address these questions, we used 27 standard cranial measurements collected on 2524 recent modern humans, 20 Neandertals and 237 common chimpanzees to estimate split times between Neandertals and modern humans, and between Pan troglodytes verus and two other subspecies of common chimpanzee. Consistent with a neutral divergence, the Neandertal versus modern human split-time estimates based on cranial measurements are similar to those based on DNA sequences. By contrast, the common chimpanzee cranial estimates are much lower than DNA-sequence estimates. Apparently, cranial evolution has been unconstrained in Neandertals and modern humans compared with common chimpanzees. Based on these and additional analyses, it appears that cranial differentiation in common chimpanzees has been restricted by stabilizing natural selection. Alternatively, this restriction could be due to genetic and/or developmental constraints on the amount of within-group variance (relative to effective population size) available for genetic drift to act on.     

Where are inion and endinion? Variations of the exo- and endocranial morphology of the occipital bone during hominin evolution

The occipital bone is frequently investigated in paleoanthropological studies because it has several features that help to differentiate various fossil hominin species. Among these features is the separation between inion and endinion, which has been proposed to be an autapomorphic trait in (Asian) Homo erectus. Methodologies are developed here to quantify for the first time the location of these anatomical points, and to interpret their variation due to the complex interactions between exocranial and endocranial size and shape of the occipital and nuchal planes, as well as the occipital lobes and cerebellum. On the basis of our analysis, neither ‘the separation between inion and endinion’ nor ‘endinion below inion’ can be considered as an autapomorphic trait in H. erectus, since this feature is a condition shared by extant African great apes and fossil hominins. Moreover, our results show that the exo- and endocranial anatomy of the occipital bone differs between hominins (except Paranthropus boisei specimens and KNM-ER 1805) and great apes. For example, chimpanzees and bonobos are characterized by a very high position of inion and their occipital bone shows an antero-posterior compression. However, these features are partly correlated with their small size when compared with hominins. Asian H. erectus specimens have a thick occipital torus, but do not differ from other robust specimens, neither in this feature nor in the analysed exo- and endocranial proportions of the occipital bone. Finally, the apparent brain size reduction during the Late Pleistocene and variation between the sexes in anatomically modern humans (AMH) reflect that specimens with smaller brains have a relatively larger posterior height of the cerebellum. However, this trend is not the sole explanation for the ‘vertical shift’ of endinion above inion that appears occasionally and exclusively in AMH.     

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.     

Shared Pattern of Endocranial Shape Asymmetries among Great Apes,Anatomically Modern Humans,and Fossil Hominins

Anatomical asymmetries of the human brain are a topic of major interest because of their link with handedness and cognitive functions. Their emergence and occurrence have been extensively explored in human fossil records to document the evolution of brain capacities and behaviour. We quantified for the first time antero-posterior endocranial shape asymmetries in large samples of great apes, modern humans and fossil hominins through analysis of “virtual” 3D models of skull and endocranial cavity and we statistically test for departures from symmetry. Once based on continuous variables, we show that the analysis of these brain asymmetries gives original results that build upon previous analysis based on discrete traits. In particular, it emerges that the degree of petalial asymmetries differs between great apes and hominins without modification of their pattern. We indeed demonstrate the presence of shape asymmetries in great apes, with a pattern similar to modern humans but with a lower variation and a lower degree of fluctuating asymmetry. More importantly, variations in the position of the frontal and occipital poles on the right and left hemispheres would be expected to show some degree of antisymmetry when population distribution is considered, but the observed pattern of variation among the samples is related to fluctuating asymmetry for most of the components of the petalias. Moreover, the presence of a common pattern of significant directional asymmetry for two components of the petalias in hominids implicates that the observed traits were probably inherited from the last common ancestor of extant African great apes and Homo sapiens.These results also have important implications for the possible relationships between endocranial shape asymmetries and functional capacities in hominins. It emphasizes the uncoupling between lateralized activities, some of them well probably distinctive to Homo, and large-scale cerebral lateralization itself, which is not unique to Homo.     

Midsagittal cranial shape variation in the genus Homo by geometric morphometrics

Midsagittal profiles of crania referred to different taxa of the genus Homo have been analyzed by geometric morphometric techniques. Comparisons between single specimens using the thin-plate-spline function suggest a generalized reduction of the lower face, associated with antero-posterior development of the braincase occurring (possibly in parallel evolution) along distinct human lineages. Furthermore, Neandertals display a projection of the midface, and modern humans show a derived globularity of the vault associated with midsagittal parietal bulging. Principal Component Analysis demonstrates a bimodal pattern of variation, which describes an "archaic" pole (rather heterogeneous in terms of taxonomy) clearly distinguishable from the modern one. The first two principal components - that explain together 80% of the total variance in shape - involve respectively fronto-parietal expansion and midfacial prognathism. These results contribute to identify different structural patterns in human evolution, supporting discontinuity rather than continuity of cranial shape among different taxa of the genus Homo, especially when considering the differences between Neandertals and early modern humans.     

Mojokerto revisited: Evidence for an intermediate pattern of brain growth in Homo erectus

Brain development in Homo erectus is a subject of great interest, and the infant calvaria from Mojokerto, Indonesia, has featured prominently in these debates. Some researchers have suggested that the pattern of brain development in H. erectus resembled that of non-human apes, while others argue for a more human-like growth pattern. In this study, we retested hypotheses regarding brain ontogeny in H. erectus using new methods (resampling), and data from additional H. erectus crania. Our results reveal that humans achieve 62% (±10%) and chimpanzees 80% (±9%) of their adult endocranial volume by 0.5–1.5 years of age. Using brain mass data, humans achieve on average 65% and chimpanzees 81% of adult size by 0.5–1.5 years. When compared with adult H. erectus crania (n = 9) from Indonesian sites greater than 1.2 million years old, Mojokerto had reached ∼70% of its adult cranial capacity. Mojokerto thus falls almost directly between the average growth in humans and chimpanzees, and well within the range of both. We therefore suggest that brain development in H. erectus cannot be dichotomized as either ape-like or human-like; it was H. erectus-like. These data indicate that H. erectus may have had a unique developmental pattern that should be considered as an important step along the continuum of brain ontogeny between apes and humans.     

La parole à la portée du conduit vocal de l'homme de Neandertal. Nouvelles recherches,nouvelles perspectives

Investigations about the origin of articulated language result in different interpretations dealing with the phonetic capacity of our ancestors, namely after the discovery of the Neandertals. According to anatomic arguments now called to question, principally the position of the larynx as regard to the basis of skull, some authors claimed that these fossil humans could not be endowed with speech. From a new reconstruction of the estimated position of the larynx and the vocal tract, articulatory simulations were undertaken in order to propose some potential vocalic [i a u] prototypes for Neandertals. And we can show Neandertals could pronounce vowels as differentiated as those of modern humans. To cite this article: J.-L. Heim et al., C. R. Palevol 1 (2002) 129–134.     

A morphometric analysis of maxillary molar crowns of Middle-Late Pleistocene hominins

This study explores the significance of shape differences in the maxillary first molar crowns of Neandertals and anatomically modern humans. It uses morphometric analysis to quantify these differences and to investigate how the orientation of major cusps, relative cusp base areas and occlusal polygon area influence crown shape. The aims of this study were to 1) quantify these data to test whether the tooth shapes of Neandertals and anatomically modern humans differ significantly and 2) to explore if either of the shapes is derived relative to earlier fossil hominins. Data were collected from digital occlusal photographs using image-processing software. Cusp angles, relative cusp base areas and occlusal polygon areas were measured on Neandertals (n=15), contemporary modern humans (n=62), Upper Paleolithic humans (n=6), early anatomically modern humans (n=3) and Homo erectus (n=3). Univariate and multivariate statistical tests were used to evaluate the differences between contemporary modern humans and Neandertals, while the much sparser data sets from the other fossil samples were included primarily for comparison. Statistically significant differences reflecting overall crown shape and internal placement of the crown apices were found. Neandertals are distinguished from contemporary humans by possessing maxillary first molars that 1) are markedly skewed; 2) possess a narrower distal segment of the occlusal polygon compared to the mesial segment; 3) possess a significantly smaller metacone and a significantly larger hypocone; and 4) possess a significantly smaller relative occlusal polygon area reflecting internally placed cusps. Differences in relative cusp base areas of the hypocone and metacone may contribute to the shape differences observed in Neandertals. However, early anatomically modern humans possessing a pattern of relative cusp base areas similar to Neandertals lack their unusual shape. That the morphology observed in non-Neandertal fossil hominins is more anatomically modern human-like than Neandertal-like, suggests that this distinctive morphology may be derived in Neandertals.     

Do modern humans and Neandertals have different patterns of cranial integration?

Studies of cranial differences between modern humans and Neandertals have identified several characteristics for which the two groups differ in their mean values, the proportional relationships with other traits, or both. However, the limited number of fairly complete Neandertals has hindered investigations into patterns of integration – covariance and correlation among traits – in this fossil group. Here, we use multiple approaches specifically designed to deal with fragmentary fossils to test if metric cranial traits in Neandertals fit modern human patterns of integration. Based on 37 traits collected from a sample of 2524 modern humans from Howells’ data set and 20 Neandertals, we show that overall patterns of cranial integration are significantly different between Neandertals and modern humans. However, at the same time, Neandertals are consistent with a modern human pattern of integration for more than three-quarters of the traits. Additionally, the differences between the predicted and actual values for the deviating traits are rather small, indicating that the differences in integration are subtle. Traits for which Neandertals deviate from modern human integration patterns tend to be found in regions where Neandertals and modern humans are known to also differ in their mean values. We conclude that the evolution of patterns of cranial integration is a cause for caution but also presents an opportunity for understanding cranial differences between modern humans and Neandertals.     

A bivariate approach to the widening of the frontal lobes in the genus Homo

Within the genus Homo, the most encephalized taxa (Neandertals and modern humans) show relatively wider frontal lobes than either Homo erectus or australopithecines. The present analysis considers whether these changes are associated with a single size-based or allometric pattern (positive allometry of the width of the anterior endocranial fossa) or with a more specific and non-allometric pattern. The relationship between hemispheric length, maximum endocranial width, and frontal width at Broca's area was investigated in extant and extinct humans. Our results do not support positive allometry for the frontal lobe's width in relation to the main endocranial diameters within modern humans (Homo sapiens). Also, the correlation between frontal width and hemispheric length is lower than the correlation between frontal width and parieto-temporal width. When compared with the australopithecines, the genus Homo could have experienced a non-allometric widening of the brain at the temporo-parietal areas, which is most evident in Neandertals. Modern humans and Neandertals also display a non-allometric widening of the anterior endocranial fossa at the Broca's cap when compared with early hominids, again more prominent in the latter group. Taking into account the contrast between the intra-specific patterns and the between-species differences, the relative widening of the anterior fossa can be interpreted as a definite evolutionary character instead of a passive consequence of brain size increase. This expansion is most likely associated with correspondent increments of the underlying neural mass, or at least with a geometrical reallocation of the frontal cortical volumes. Although different structural changes of the cranial architecture can be related to such variations, the widening of the frontal areas is nonetheless particularly interesting when some neural functions (like language or working memory, decision processing, etc.) and related fronto-parietal cortico-cortical connections are taken into account.