Effects of cranial integration on hominid endocranial shape

Because brains do not fossilize, the internal surface of the braincase (endocast) serves as an important source of information about brain growth, development, and evolution. Recent studies of endocranial morphology and development in great apes, fossil hominins, and modern humans have revealed taxon‐specific differences. However, it remains to be investigated to which extent differences in endocranial morphology reflect differences in actual brain morphology and development, and to which extent they reflect different interactions of the brain and its case with the cranial base and face. Here we address this question by analyzing the effects of cranial integration on endocranial morphology. We test the ‘spatial packing’ and ‘facial orientation’ hypotheses, which propose that size and orientation of the neurocranium relative to the viscerocranium influence endocranial shape. Results show that a substantial proportion of endocranial shape variation along and across ontogenetic trajectories is due to cranial integration. Specifically, the uniquely globular shape of the human endocast mainly results from the combination of an exceptionally large brain with a comparatively small face. Overall, thus, cranial integration has pervasive effects on endocranial morphology, and only a comparatively small proportion of inter‐ and intra‐taxon variation can directly be associated with variation in brain morphology.     

Re-creating ancient hominid virtual endocasts by CT-scanning

Probably the first radiographic study of human fossils, that by D. Gorganovic-Kramberger on Neandertal remains from Krapina, Croatia, was published in 1906, only 11 years after R?ntgen announced the discovery of X-rays. Many subsequent studies on fossil hominids used regular clinical diagnostic radiological apparatus, as depicted in Atlas of Radiographs of Early Man by M.F. Skinner and G.H. Sperber (1982). Some specimens such as crania filled with heavily calcified matrix proved intractable. Ordinary radiographs of such specimens usually failed to reveal endocranial structure, as fossilized bone and calcified endocast were approximately equally radio-opaque. Thus, neither endocranial volume nor structural details were detectable. The only invasive method that could have been employed involved mechanical removal of the solid matrix, but this entailed hazards to the cranial vault and the destruction of the natural endocranial cast. In 1983--1984, G.C. Conroy and M. Vannier utilized recent advances in high-resolution computed tomography to produce non-invasive, intracranial capacity measurements of matrix-filled fossil skulls. They tried the method on two fossil mammal skulls filled with hard sandstone matrix (1984, Science 26:456-458), and then successfully applied it to a South African, matrix-filled cranium of the ancient hominid (hominin) species, Australopithecus africanus from Makapansgat (Conroy et al. 1990, Science 247:838-841). Details of the morphology of the endocranial surface of the braincase were revealed, including the pattern of venous sinus drainage in the posterior cranial fossa. A group based in St. Louis, Vienna, Paris, Rome, and Johannesburg has taken such studies further. Beautiful "virtual endocasts" have been produced on a large male specimen of A. africanus from Sterkfontein, South Africa, and the endocranial capacity has been determined (1998). The methods make it possible to re-create "virtual endocasts" of ancient hominids.     

Endocranial Occipito‐Temporal Anatomy of SD‐1219 from the Neandertal El Sidrón Site (Asturias,Spain)

We addressed the brain drainage system as inferred by the endocranial morphology of the occipito‐temporal region of the El Sidrón Neandertal specimen SD‐1219. Morphological details of the endocranial surface and its anatomical implications were analyzed for the reconstruction of the dural sinus drainage pattern and its comparison with Neandertals and other hominids. The specimen SD‐1219 shows a pattern in which the superior sagittal sinus goes into the right transverse sinus. Comparative analyses with a large sample of fossil hominids reveal a pattern of the SD‐1219 fossil that is typical for Neandertals. The analysis of the proportions of the occipital lobes prints within the occipital fossae reveals that the left occipital pole projects toward the right. This possibly indicates brain asymmetry (petalia) in this Neandertal individual, similar to that observed in some modern human brains. Conversely, no such asymmetry was observed in the cerebellar fossae. A particular feature of this fossil is the presence of two crests, located at the middle of the left cerebellar fossa that can be related to either an imprinting of a cerebellar fissure or some bone response to mechanical influence on internal bone surface morphology during cerebellar development. Specific aspects of the paleoneurology of Neandertals are discussed. Further quantitative studies on the endocranial morphology of the occipito‐temporal and ‐mastoid region will shed light on the paleoneurological significance of this important anatomical region for the understanding of human evolution. Anat Rec, 291:502–512, 2008. © 2008 Wiley‐Liss, Inc.     

The endocranial shape of Australopithecus africanus: surface analysis of the endocasts of Sts 5 and Sts 60

Assessment of global endocranial morphology and regional neuroanatomical changes in early hominins is critical for the reconstruction of evolutionary trajectories of cerebral regions in the human lineage. Early evidence of cortical reorganization in specific local areas (e.g. visual cortex, inferior frontal gyrus) is perceptible in the non‐human South African hominin fossil record. However, to date, little information is available regarding potential global changes in the early hominin brain. The introduction of non‐invasive imaging techniques opens up new perspectives for the study of hominin brain evolution. In this context, our primary aim in this study is to explore the organization of the Australopithecus africanus endocasts, and highlight the nature and extent of the differences distinguishing A. africanus from the extant hominids at both local and global scales. By means of X‐ray‐based imaging techniques, we investigate two A. africanus specimens from Sterkfontein Member 4, catalogued as Sts 5 and Sts 60, respectively a complete cranium and a partial cranial endocast. Endocrania were virtually reconstructed and compared by using a landmark‐free registration method based on smooth and invertible surface deformation. Both local and global information provided by our deformation‐based approach are used to perform statistical analyses and topological mapping of inter‐specific variation. Statistical analyses indicate that the endocranial shape of Sts 5 and Sts 60 approximates the Pan condition. Furthermore, our study reveals substantial differences with respect to the extant human condition, particularly in the parietal regions. Compared with Pan, the endocranial shape of the fossil specimens differs in the anterior part of the frontal gyri.     

Allosaurus, crocodiles, and birds: evolutionary clues from spiral computed tomography of an endocast

Because the brain does not usually leave direct evidence of its existence in the fossil record, our view of this structure in extinct species has relied upon inferences drawn from comparisons between parts of the skeleton that do fossilize or with modern-day relatives that survived extinction. However, soft-tissue structure preservation may indeed occasionally occur, particularly in the endocranial space. By applying modern imaging and analysis methods to such natural cranial "endocasts," we can now learn more than ever thought possible about the brains of extinct species. I will discuss one such example in which spiral computed tomography (CT) scanning analysis has been successfully applied to reveal preserved internal structures of a naturally occurring endocranial cast of Allosaurus fragilis, the dominant carnivorous dinosaur of the late Jurassic period. The ability to directly examine the neuroanatomy of an extinct dinosaur, whose modern-day relatives are birds and crocodiles, has exciting implications about Allosaurus' behavior, its adaptive responses to its environment, and its eventual extinction.     

Cetacean Skull Telescoping Brings Evolution of Cranial Sutures into Focus

Many modifications to the mammalian bauplan associated with the obligate aquatic lives of cetaceans—fusiform bodies, flukes, flippers, and blowholes—are evident at a glance. But among the most strikingly unusual and divergent features of modern cetacean anatomy are the arrangements of their cranial bones: (1) bones that are situated at opposite ends of the skull in other mammals are positioned close together, their proximity resulting from (2) these bones extensively overlapping the bones that ordinarily would separate them. The term “telescoping” is commonly used to describe the odd anatomy of modern cetacean skulls, yet its usage and the particular skull features to which it refers vary widely. Placing the term in historical and biological context, this review offers an explicit definition of telescoping that includes the two criteria enumerated above. Defining telescoping in this way draws attention to many specific biological questions that are raised by the unusual anatomy of cetacean skulls; highlights the central role of sutures as the locus for changes in the sizes, shapes, mechanical properties, and connectivity of cranial bones; and emphasizes the importance of sutures in skull development and evolution. The unusual arrangements of cranial bones and sutures referred to as telescoping are not easily explained by what is known about cranial development in more conventional mammals. Discovering the evolutionary-developmental processes that produce the extensive overlap characteristic of cetacean telescoping will give insights into both cetacean evolution and the “rules” that more generally govern mammalian skull function, development, and evolution. Anat Rec, 302:1055–1073, 2019. © 2019 Wiley Periodicals, Inc.     

Novel insights into early neuroanatomical evolution in penguins from the oldest described penguin brain endocast

Digital methodologies for rendering the gross morphology of the brain from X‐ray computed tomography data have expanded our current understanding of the origin and evolution of avian neuroanatomy and provided new perspectives on the cognition and behavior of birds in deep time. However, fossil skulls germane to extracting digital endocasts from early stem members of extant avian lineages remain exceptionally rare. Data from early‐diverging species of major avian subclades provide key information on ancestral morphologies in Aves and shifts in gross neuroanatomical structure that have occurred within those groups. Here we describe data on the gross morphology of the brain from a mid‐to‐late Paleocene penguin fossil from New Zealand. This most basal and geochronologically earliest‐described endocast from the penguin clade indicates that described neuroanatomical features of early stem penguins, such as lower telencephalic lateral expansion, a relatively wider cerebellum, and lack of cerebellar folding, were present far earlier in penguin history than previously inferred. Limited dorsal expansion of the wulst in the new fossil is a feature seen in outgroup waterbird taxa such as Gaviidae (Loons) and diving Procellariiformes (Shearwaters, Diving Petrels, and allies), indicating that loss of flight may not drastically affect neuroanatomy in diving taxa. Wulst enlargement in the penguin lineage is first seen in the late Eocene, at least 25 million years after loss of flight and cooption of the flight stroke for aquatic diving. Similar to the origin of avian flight, major shifts in gross brain morphology follow, but do not appear to evolve quickly after, acquisition of a novel locomotor mode. Enlargement of the wulst shows a complex pattern across waterbirds, and may be linked to sensory modifications related to prey choice and foraging strategy.     

Are endocasts good proxies for brain size and shape in archosaurs throughout ontogeny?

Cranial endocasts, or the internal molds of the braincase, are a crucial correlate for investigating the neuroanatomy of extinct vertebrates and tracking brain evolution through deep time. Nevertheless, the validity of such studies pivots on the reliability of endocasts as a proxy for brain morphology. Here, we employ micro‐computed tomography imaging, including diffusible iodine‐based contrast‐enhanced CT, and a three‐dimensional geometric morphometric framework to examine both size and shape differences between brains and endocasts of two exemplar archosaur taxa – the American alligator (Alligator mississippiensis) and the domestic chicken (Gallus gallus). With ontogenetic sampling, we quantitatively evaluate how endocasts differ from brains and whether this deviation changes during development. We find strong size and shape correlations between brains and endocasts, divergent ontogenetic trends in the brain‐to‐endocast correspondence between alligators and chickens, and a comparable magnitude between brain–endocast shape differences and intraspecific neuroanatomical variation. The results have important implications for paleoneurological studies in archosaurs. Notably, we demonstrate that the pattern of endocranial shape variation closely reflects brain shape variation. Therefore, analyses of endocranial morphology are unlikely to generate spurious conclusions about large‐scale trends in brain size and shape. To mitigate any artifacts, however, paleoneurological studies should consider the lower brain–endocast correspondence in the hindbrain relative to the forebrain; higher size and shape correspondences in chickens than alligators throughout postnatal ontogeny; artificially ‘pedomorphic’ shape of endocasts relative to their corresponding brains; and potential biases in both size and shape data due to the lack of control for ontogenetic stages in endocranial sampling.     

Development of the Skull of the Pantropical Spotted Dolphin (Stenella attenuata)

We describe the bony and cartilaginous structures of five fetal skulls of Stenella attenuata (pantropical spotted dolphin) specimens. The specimens represent early fetal life as suggested by the presence of rostral tactile hairs and the beginnings of skin pigmentation. These specimens exhibit the developmental order of ossification of the intramembranous and endochondral elements of the cranium as well as the functional and morphological development of specific cetacean anatomical adaptations. Detailed observations are presented on telescoping, nasal anatomy, and middle ear anatomy. The development of the middle ear ossicles, ectotympanic bone, and median nasal cartilage is of interest because in the adult these structures are morphologically different from those in land mammals. We follow specific cetacean morphological characteristics through fetal development to provide insight into the form and function of the cetacean body plan. Combining these data with fossil evidence, it is possible to overlie ontogenetic patterns and discern evolutionary patterns of the cetacean skull. Anat Rec, 2011. © 2011 Wiley‐Liss, Inc.     

CT-based description and phyletic evaluation of the archaic human calvarium from Ceprano, Italy

The discovery in 1994, of a fossilized human calvarium near Ceprano, Italy, dated about 800-900 thousand years before present, opened a new page for the study of human evolution in Europe. It extended the continental fossil record over the boundary between Early and Middle Pleistocene for the first time and revealed the cranial morphology of humans that where probably ancestral to both Neanderthals and modern Homo sapiens. A tomographic analysis of the Italian specimen is reported here in order to describe size and shape, vascular traces, and other features of the endocranium, as well as some relevant ectocranial traits (particularly of the frontal region). Our results show that the Ceprano calvarium displays plesiomorphies shared by early Homo taxa, involving a general archaic phenotype. At the same time, the presence of some derived features suggests a phylogenetic relationship with the populations referred to the subsequent polymorphic species H. heidelbergensis. The morphology of the supraorbital structures is different from the double-arched browridge of the African H. ergaster, while its superior shape shows similarities with African Middle Pleistocene specimens (Bodo, Kabwe). In contrast, the relationship between supraorbital torus and frontal squama points to an archaic pattern of the relationship between face and vault, associated to moderately narrow frontal lobes and limited development of the upper parietal areas. Despite a nonderived endocranial shape, the increase of cranial capacity (related to a general endocranial widening) and the probable absence of a clear occipital projection also suggest an evolutionary independence from the Asian H. erectus lineage. This analysis therefore supports the conclusion that the Ceprano calvarium represents the best available candidate for the ancestral phenotype of the cranial variation observed among Middle Pleistocene fossil samples in Africa and Europe. Nevertheless, a proper taxonomic interpretation of this crucial specimen remains puzzling.     

Brain morphology in nonsyndromic unicoronal craniosynostosis

Studies of isolated craniosynostosis have shown biomechanical and biochemical influences on the craniofacial phenotype, resulting from both genetic and epigenetic factors. Much less attention has been directed toward the morphology of the brain, despite the interactive nature of the developing skull and developing brain. The aim of this study is to define the morphology of the brain in nonsyndromic unilateral coronal synostosis (UCS) in order to form more complete hypotheses about the cause of craniosynostosis. Landmark coordinate data were collected from 3D magnetic resonance image reconstructions of the brain in a sample of UCS patients and an age-matched morphologically normal cohort. These data were analyzed using Euclidean distance matrix analysis. The results of our study demonstrate that despite the basic similarity of overall shape of the brain and skull in UCS, the effects of craniosynostosis on the brain are not localized to structures immediately adjacent to the fused suture or to the endocranial surface of the skull. Rather, alterations are observed throughout the volume of the brain, with subcortical structures altered in conjunction with cortical changes. These results indicate that the morphological correlates are different for brain and skull and suggest that there is a large degree of independence in the developmental trajectories of the brain and skull.     

Endocranial capacity in Sts 71 (Australopithecus africanus) by three-dimensional computed tomography

In a recent report on early hominid endocranial capacity, it was predicted that future studies would show that: (1) "several key early hominid endocranial estimates may be inflated"; (2) "current views on the tempo and mode of early hominid brain evolution may need reevaluation"; and (3) endocranial capacity in one of these, Sts 71, was "probably closer to 370 cm(3), very near the mean value for female chimpanzees, and not the currently accepted 428 cm(3)" (Conroy et al., Science, 1998; 280: 1730-1731; Falk, Science 1998; 20:1714). Subsequent studies tend to support the first two predictions, but not the third (Culotta, Science, 1999; 284: 1109; Falk, Am. J. Phys. Anthropol. Suppl., 1999; 28: 126; Falk et al., J. Hum. Evol. [in press]). Here we detail the reasons for thinking the currently accepted endocranial value for Sts 71 is probably correct by providing the first quantitative details of endocranial reconstruction in Sts 71 using three-dimensional computed tomography. Relative brain expansion in the hominid lineage started some half-million years before the earliest appearance of the genus Homo, possibly coincident with enhanced tool-making skills and carnivory.     

On the Olfactory Anatomy in an Archaic Whale (Protocetidae,Cetacea) and the Minke Whale Balaenoptera acutorostrata (Balaenopteridae,Cetacea)

The structure of the olfactory apparatus is not well known in both archaic and extant whales; the result of poor preservation in most fossils and locational isolation deep within the skulls in both fossil and Recent taxa. Several specimens now shed additional light on the subject. A partial skull of an archaic cetacean is reported from the Pamunkey River, Virginia, USA. The specimen probably derives from the upper middle Eocene (Piney Point Formation) and is tentatively assigned to the Protocetidae. Uncrushed cranial cavities associated with the olfactory apparatus were devoid of sediment. CT scans clearly reveal the dorsal nasal meatus, ethmoturbinates within the olfactory recess, the cribriform plate, the area occupied by the olfactory bulbs, and the olfactory nerve tract. Several sectioned skulls of the minke whale (Balaenoptera acutorostrata) were also examined, and olfactory structures are remarkably similar to those observed in the fossil skull from the Pamunkey River. One important difference between the two is that the fossil specimen has an elongate olfactory nerve tract. The more forward position of the external nares in extant balaenopterids when compared with those of extant odontocetes is interpreted to be the result of the need to retain a functional olfactory apparatus and the forward position of the supraoccipital/cranial vertex. An increase in the distance between the occipital condyles and the vertex in balaenopterids enhances the mechanical advantage of the epaxial musculature that inserts on the occiput, a specialization that likely stabilizes the head of these enormous mammals during lunge feeding. Anat Rec, 2013. © 2012 Wiley Periodicals, Inc.     

Avian palaeoneurology: Reflections on the eve of its 200th anniversary

In birds, the brain (especially the telencephalon) is remarkably developed, both in relative volume and complexity. Unlike in most early-branching sauropsids, the adults of birds and other archosaurs have a well-ossified neurocranium. In contrast to the situation in most of their reptilian relatives but similar to what can be seen in mammals, the brains of birds fit closely to the endocranial cavity so that their major external features are reflected in the endocasts. This makes birds a highly suitable group for palaeoneurological investigations. The first observation about the brain in a long-extinct bird was made in the first quarter of the 19th century. However, it was not until the 2000s and the application of modern imaging technologies that avian palaeoneurology really took off. Understanding how the mode of life is reflected in the external morphology of the brains of birds is but one of several future directions in which avian palaeoneurological research may extend. Although the number of fossil specimens suitable for palaeoneurological explorations is considerably smaller in birds than in mammals and will very likely remain so, the coming years will certainly witness a momentous strengthening of this rapidly growing field of research at the overlap between ornithology, palaeontology, evolutionary biology and neurosciences.