Patterns of morphological integration between parietal and temporal areas in the human skull

Modern humans have evolved bulging parietal areas and large, projecting temporal lobes. Both changes, largely due to a longitudinal expansion of these cranial and cerebral elements, were hypothesized to be the result of brain evolution and cognitive variations. Nonetheless, the independence of these two morphological characters has not been evaluated. Because of structural and functional integration among cranial elements, changes in the position of the temporal poles can be a secondary consequence of parietal bulging and reorientation of the head axis. In this study, we use geometric morphometrics to test the correlation between parietal shape and the morphology of the endocranial base in a sample of adult modern humans. Our results suggest that parietal proportions show no correlation with the relative position of the temporal poles within the spatial organization of the endocranial base. The vault and endocranial base are likely to be involved in distinct morphogenetic processes, with scarce or no integration between these two districts. Therefore, the current evidence rejects the hypothesis of reciprocal morphological influences between parietal and temporal morphology, suggesting that evolutionary spatial changes in these two areas may have been independent. However, parietal bulging exerts a visible effect on the rotation of the cranial base, influencing head position and orientation. This change can have had a major relevance in the reorganization of the head functional axis.     

Validation of plaster endocast morphology through 3D CT image analysis

A crucial component of research on brain evolution has been the comparison of fossil endocranial surfaces with modern human and primate endocrania. The latter have generally been obtained by creating endocasts out of rubber latex shells filled with plaster. The extent to which the method of production introduces errors in endocast replicas is unknown. We demonstrate a powerful method of comparing complex shapes in 3-dimensions (3D) that is broadly applicable to a wide range of paleoanthropological questions. Pairs of virtual endocasts (VEs) created from high-resolution CT scans of corresponding latex/plaster endocasts and their associated crania were rigidly registered (aligned) in 3D space for two Homo sapiens and two Pan troglodytes specimens. Distances between each cranial VE and its corresponding latex/plaster VE were then mapped on a voxel-by-voxel basis. The results show that between 79.7% and 91.0% of the voxels in the four latex/plaster VEs are within 2 mm of their corresponding cranial VEs surfaces. The average error is relatively small, and variation in the pattern of error across the surfaces appears to be generally random overall. However, inferior areas around the cranial base and the temporal poles were somewhat overestimated in both human and chimpanzee specimens, and the area overlaying Broca's area in humans was somewhat underestimated. This study gives an idea of the size of possible error inherent in latex/plaster endocasts, indicating the level of confidence we can have with studies relying on comparisons between them and, e.g., hominid fossil endocasts.     

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.     

化石人类脑演化研究概况

脑演化是人类演化的一个重要组成部分,其研究可以为人类起源、演化、人群关系及语言、智力等方面提供重要的信息。脑演化的主要证据是通过研究颅内模（endocast）及颅骨的形态得到的。颅内模是从颅骨内表面得到的脑的外部形态。有时颅骨的内腔充满泥沙,并且为钙质所结固,可以自然形成颅内模。也可以人工制作颅内模。颅内模和颅骨的内表面能够提供人类脑髓及神经进化方面的直接证据。对化石人类脑演化的研究主要包括以下几个方面的内容：测量或估计脑量的大小及其和身体大小之间的关系;研究脑量随时间的变化过程;通过对早期人类颅内模表面沟回形态特征的研究,探索脑功能区在早期人类和猿类的区别及在演化上的变化;左右大脑不对称性与一侧优势关系,探讨语言的起源和惯用手的脑功能基础等;脑膜中动脉系统、静脉窦系统及与血液循环相关的排泄孔的变化,探讨大脑各部分比例的变化和功能的日益复杂对供血需求的影响;通过对人类脑演化的研究,探讨人类进化的原因。本文通过对以上几个方面及其中国化石脑演化研究的介绍,对化石人类脑演化的研究概况作综合论述和简单回顾。     

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 new brain endocast of Homo erectus from Hulu Cave, Nanjing, China

A new brain endocast of Homo erectus from Hulu Cave, Tangshan, Nanjing is described and compared with a broad sample of endocasts of H. erectus, Neanderthals, and recent modern humans. The Nanjing 1 endocast is reconstructed based on two portions of endocranial casts taken from the original fossil fragments. The fossil was discovered in 1993, near Nanjing, South China and is dated to ～ 0.58-0.62 Ma. The cranial capacity is ～ 876 cc, as determined by endocast water displacement. There are some common features of Nanjing 1 and other H. erectus endocasts that differentiate them from the Neanderthals and modern humans in our sample. These include small cranial capacity, low height dimensions, simple middle meningeal vessel patterns, a high degree of cerebral-over-cerebellar lobe overhang, elongated and quite separated cerebellar lobes, and a narrow, low, short and flat frontal region. Some features are found to vary among H. erectus, Neanderthals and modern humans, such as the lateral Sylvian fissure position and the venous sinus and petalial patterns. The Nanjing 1 endocast has unique, large, superior frontal convolutions, and strongly protruding Broca's caps. In contrast to other Chinese H. erectus from Hexian and Zhoukoudian, Nanjing 1 lacks strong posterior projection of the occipital lobes. Bivariate and principal component analyses indicate that the small volume and shape of Nanjing 1 is most similar to KNM-WT 15000, KNM-ER 3883, Sangiran 2 and Hexian, illustrating the combination of narrow, low, and short frontal lobes with wide posterior lobes.     

中国古人类颅内模及脑演化研究进展

颅内模保存有脑表面的形态结构,是脑演化研究的直接证据。中国最早复原和研究的颅内模来自20世纪20年代北京周口店遗址发现的3号猿人头骨;此后虽然中国境内也相继发现了一些古人类的头骨化石,但由于古人类标本非常珍贵,不允许对其进行实体解剖,加上多数头骨破碎或者内部附有地层胶结物,导致颅内模无法成功复原。受技术水平及研究手段的限制,研究者一般只是侧重于化石外表形态结构的研究。高分辨率工业CT和3D软件的应用,可以在不损坏标本的情况下,虚拟复原出化石的内部解剖结构,使得一些重要的古人类化石标本的颅内模被复原出来,促进了脑演化的研究。近年来,本文第一作者采用新技术、新方法复原了南京直立人、柳江人等一些重要的中国古人类头骨的颅内模,通过对其颅容量、脑沟回特征、脑不对称性、脑表面的动、静脉血管压迹、各脑叶的大小、形状及比例的研究,获取了中国古人类脑形态特征变化的数据,为探讨东亚地区古人类的演化提供了参考信息。     

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.     

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.     

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.     

A new approach to mammalian cranial analysis, illustrated by examples of prosimian primates

Latex endocranial casts, which may be made without damaging the skull, reveal much of the information provided by a hemisected skull. Examination of drawings of endocasts superimposed on skulls may provide insight into the biological significance of skull and brain morphology. The high degree of cranial flexion and the globose brain shape of Daubentonia appear to be related to the functional demands of its gnawing mechanism. The broad frontal lobes of indriids are correlated with orbital orientation; differences in frontal lobe sulcal pattern suggest greater elaboration of the motor filed for the hand in indriids than in lemurids. Several features of lorisid cranial anatomy are discussed. It is suggested that, as a first approximation, increased splanchnocranial declination in small prosimians results from the necessity of accommodating relatively large eyes in a skull with a relatively small splanchnocranium.     

A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya

The globular braincase of modern humans is distinct from all fossil human species, including our closest extinct relatives, the Neandertals. Such adult shape differences must ultimately be rooted in different developmental patterns, but it is unclear at which point during ontogeny these group characteristics emerge.Here we compared internal shape changes of the braincase from birth to adulthood in Neandertals (N = 10), modern humans (N = 62), and chimpanzees (N = 62). Incomplete fossil specimens, including the two Neandertal newborns from Le Moustier 2 and Mezmaiskaya, were reconstructed using reference-based estimation methods. We used 3D geometric morphometrics to statistically compare shapes of virtual endocasts extracted from computed-tomographic scans. Throughout the analysis, we kept track of possible uncertainties due to the missing data values and small fossil sample sizes.We find that some aspects of endocranial development are shared by the three species. However, in the first year of life, modern humans depart from this presumably ancestral pattern of development. Newborn Neandertals and newborn modern humans have elongated braincases, and similar endocranial volumes. During a ‘globularization-phase’ modern human endocasts change to the globular shape that is characteristic for Homo sapiens. This phase of early development is unique to modern humans, and absent from chimpanzees and Neandertals.Our results support the notion that Neandertals and modern humans reach comparable adult brain sizes via different developmental pathways. The differences between these two human groups are most prominent directly after birth, a critical phase for cognitive development.     

Comparative endocranial vascular changes due to craniosynostosis and artificial cranial deformation

The processes of craniosynostosis (premature fusion of one or more of the calvarial sutures) and artificial cranial deformation are similar since both can alter the shape of the craniofacial complex. Most research exploring these processes has focused on the ectocranium, although it is obvious that these processes also modify the endocranium. Endocranial changes due to either craniosynostosis or artificial cranial deformation have not been as thoroughly examined. Silicone rubber endocasts were made from 11 craniosynostotic archaeologically derived specimens from North and South America. For comparative purposes, endocasts were made from 22 normal and 17 occipitally deformed crania that were archaeologically derived from North and South America. With all samples, middle meningeal vessel patterns and venous sinus impressions were qualitatively and quantitatively analyzed. Depth, width, and convolution of the middle meningeal vessels were recorded, and the direction of vessel branches was noted. Both artificial cranial deformation and craniosynostosis altered the endocranial vasculature. Middle meningeal vessel and venous sinus impressions of the craniosynostotic group differed when compared to both the undeformed and artificially cranially deformed samples. Sinuses traversing under synostosed sutures became wider and deeper. In contrast, sinuses directly underneath the greatest artificial deformational stress were shallower, while there was compensatory enlargement of sinuses further away from the greatest deformational effects. Such compensatory enlargement also was shown by the high incidence of enlarged occipital/marginal sinuses in artificially deformed skulls. Increased intracranial pressure is hypothesized to be the cause of the venous sinus changes found in craniosynostotic individuals. Middle meningeal vessel patterns from craniosynostotic and artificially deformed specimens were similar in that their direction paralleled the direction of altered cranial growth. These findings demonstrate that the endocranial vasculature is developmentally plastic and responds to deformation in a predictable pattern. © 1996 Wiley-Liss, Inc.     

Comparative Endocranial Anatomy,Encephalization, and Phylogeny of Notoungulata (Placentalia,Mammalia)

Journal of Mammalian Evolution - Cranial endocasts are one of the most direct tools available to obtain information about the endocranial cavity of fossil mammals, but few anatomical comparisons...     

Flightless birds are not neuroanatomical analogs of non-avian dinosaurs

Background

In comparative neurobiology, major transitions in behavior are thought to be associated with proportional size changes in brain regions. Bird-line theropod dinosaurs underwent a drastic locomotory shift from terrestrial to volant forms, accompanied by a suite of well-documented postcranial adaptations. To elucidate the potential impact of this locomotor shift on neuroanatomy, we first tested for a correlation between loss of flight in extant birds and whether the brain morphology of these birds resembles that of their flightless, non-avian dinosaurian ancestors. We constructed virtual endocasts of the braincase for 80 individuals of non-avian and avian theropods, including 25 flying and 19 flightless species of crown group birds. The endocasts were analyzed using a three-dimensional (3-D) geometric morphometric approach to assess changes in brain shape along the dinosaur-bird transition and secondary losses of flight in crown-group birds (Aves).

Results

While non-avian dinosaurs and crown-group birds are clearly distinct in endocranial shape, volant and flightless birds overlap considerably in brain morphology. Phylogenetically informed analyses show that locomotory mode does not significantly account for neuroanatomical variation in crown-group birds. Linear discriminant analysis (LDA) also indicates poor predictive power of neuroanatomical shape for inferring locomotory mode. Given current sampling, Archaeopteryx, typically considered the oldest known bird, is inferred to be terrestrial based on its endocranial morphology.

Conclusion

The results demonstrate that loss of flight does not correlate with an appreciable amount of neuroanatomical changes across Aves, but rather is partially constrained due to phylogenetic inertia, evident from sister taxa having similarly shaped endocasts. Although the present study does not explicitly test whether endocranial changes along the dinosaur-bird transition are due to the acquisition of powered flight, the prominent relative expansion of the cerebrum, in areas associated with flight-related cognitive capacity, suggests that the acquisition of flight may have been an important initial driver of brain shape evolution in theropods.

     

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.     

Parietal lobe variation in cercopithecid endocasts

In extant primates, the posterior parietal cortex is involved in visuospatial integration, attention, and eye‐hand coordination, which are crucial functions for foraging and feeding behaviors. Paleoneurology studies brain evolution through the analysis of endocasts, that is molds of the inner surface of the braincase. These may preserve imprints of cortical structures, such as sulci, which might be of interest for locating the boundaries of major cortical regions. Old World monkeys (Cercopithecidae) represent an interesting zoological group for evolutionary studies, because of their diverse ecologies and locomotor behaviors. In this study, we quantify parietal lobe variation within the cercopithecid family, in a sample of 30 endocasts including 11 genera and 17 species, by combining landmark‐based and landmark‐free geometric morphometric analyses. More specifically, we quantitatively assess variation of the parietal proportions based on landmarks placed on reliable anatomical references and of parietal lobe surface morphology through deformation‐based methods. The main feature associated with the cercopithecid endocranial variation regards the inverse proportions of parietal and occipital lobes, with colobines, Theropithecus, and Papio displaying relatively larger parietal lobes and smaller occipital lobes compared with cercopithecins. The parietal surface is anteroposteriorly longer and mediolaterally flatter in colobines, while longitudinally shorter but laterally bulging in baboons. Large parietal lobes in colobines and baboons are likely to be independent evolutionary traits, and not necessarily associated with analogous functions or morphogenetic mechanisms.     

The endocast from Dana Aoule North (DAN5/P1): A 1.5 million year-old human braincase from Gona,Afar, Ethiopia

The nearly complete cranium DAN5/P1 was found at Gona (Afar, Ethiopia), dated to 1.5–1.6 Ma, and assigned to the species Homo erectus. Its size is, nonetheless, particularly small for the known range of variation of this taxon, and the cranial capacity has been estimated as 598 cc. In this study, we analyzed a reconstruction of its endocranial cast, to investigate its paleoneurological features. The main anatomical traits of the endocast were described, and its morphology was compared with other fossil and modern human samples. The endocast shows most of the traits associated with less encephalized human taxa, like narrow frontal lobes and a simple meningeal vascular network with posterior parietal branches. The parietal region is relatively tall and rounded, although not especially large. Based on our set of measures, the general endocranial proportions are within the range of fossils included in the species Homo habilis or in the genus Australopithecus. Similarities with the genus Homo include a more posterior position of the frontal lobe relative to the cranial bones, and the general endocranial length and width when size is taken into account. This new specimen extends the known brain size variability of Homo ergaster/erectus, while suggesting that differences in gross brain proportions among early human species, or even between early humans and australopiths, were absent or subtle.