What do brain endocasts tell us? A comparative analysis of the accuracy of sulcal identification by experts and perspectives in palaeoanthropology.

Palaeoneurology is a complex field as the object of study, the brain, does not fossilize. Studies rely therefore on the (brain) endocranial cast (often named endocast), the only available and reliable proxy for brain shape, size and details of surface. However, researchers debate whether or not specific marks found on endocasts correspond reliably to particular sulci and/or gyri of the brain that were imprinted in the braincase. The aim of this study is to measure the accuracy of sulcal identification through an experiment that reproduces the conditions that palaeoneurologists face when working with hominin endocasts. We asked 14 experts to manually identify well-known foldings in a proxy endocast that was obtained from an MRI of an actual in vivo Homo sapiens head. We observe clear differences in the results when comparing the non-corrected labels (the original labels proposed by each expert) with the corrected labels. This result illustrates that trying to reconstruct a sulcus following the very general known shape/position in the literature or from a mean specimen may induce a bias when looking at an endocast and trying to follow the marks observed there. We also observe that the identification of sulci appears to be better in the lower part of the endocast compared to the upper part. The results concerning specific anatomical traits have implications for highly debated topics in palaeoanthropology. Endocranial description of fossil specimens should in the future consider the variation in position and shape of sulci in addition to using models of mean brain shape. Moreover, it is clear from this study that researchers can perceive sulcal imprints with reasonably high accuracy, but their correct identification and labelling remains a challenge, particularly when dealing with extinct species for which we lack direct knowledge of the brain.

New high-resolution computed tomography data of the Taung partial cranium and endocast and their bearing on metopism and hominin brain evolution.

Falk and colleagues [Falk D, Zollikofer CP, Morimoto N, Ponce de León MS (2012) Proc Natl Acad Sci U S A 109(22):8467-8470] hypothesized that selective pressures favored late persistence of a metopic suture and open anterior fontanelle early in hominin evolution, and they put an emphasis on the Taung Child (Australopithecus africanus) as evidence for the antiquity of these adaptive features. They suggested three mutually nonexclusive pressures: an "obstetric dilemma," high early postnatal brain growth rates, and neural reorganization in the frontal cortex. To test this hypothesis, we obtained the first high-resolution computed tomography (CT) data from the Taung hominin. These high-resolution image data and an examination of the hominin fossil record do not support the metopic and fontanelle features proposed by Falk and colleagues. Although a possible remnant of the metopic suture is observed in the nasion-glabella region of the Taung partial cranium (but not along the frontal crest), this character state is incongruent with the zipper model of metopic closure described by Falk and colleagues. Nor do chimpanzee and bonobo endocast data support the assertion that delayed metopic closure in Taung is necessary because of widening (reorganization) of the prefrontal or frontal cortex. These results call into question the adaptive value of delaying metopic closure, and particularly its antiquity in hominin evolution. Further data from hominoids and hominins are required to support the proposed adaptive arguments, particularly an obstetric dilemma placing constraints on neural and cranial development in Australopithecus.

Technical note: the midline and endocranial volume of the Taung endocast.

The Taung endocast is one of the best-preserved and most important known in paleoanthropology. Although the endocast is undistorted and preserves distinctive landmarks, Taung has proved a difficult endocast, because it is only about 60% complete. To reconstruct Taung it is necessary to first use the available anatomical landmarks to define the midline of the endocast. It is only with a proper description of the midline that it is possible to reconstruct the endocast and obtain an accurate measurement of Taung's endocranial volume. Holloway (Science 168 (1970) 966-968) determined a conservative estimate for Taung of 404 ml. More recently this estimate has been revised downward by Falk and Clarke (Am J Phys Anthropol 134 (2007) 529-534) to 382 ml, giving Taung the smallest endocast for A. africanus. Certain challenges exist with the reconstruction of any endocast, particularly a hemi-endocast such as Taung. A virtual reconstruction of Taung must assume perfect symmetry, a feature called into question here in Taung's most recent reconstruction by Falk and Clarke (2007). Holloway's (1970) reconstruction of Taung provides a guidepost for a conservative approach to endocast reconstructions, and the most reliable measurement of Taung's true endocranial volume.

A preliminary 3D computed tomography study of the human maxillary sinus and nasal cavity.

Despite centuries of investigation, the function of the maxillary sinus (MS) and underlying patterns governing its form remain elusive. In this study, we articulate a methodology for collecting volumetric data for the MS and nasal cavity (NC) from computed tomography (CT) scans and report details for a small sample of 39 dried human crania of known ecogeographic provenience useful for assessing variation in MS size and shape. We use scaling analyses to preliminarily test the hypothesis that volumes of the nasal cavity (NCV) and maxillary sinus (MSV) are inversely correlated such that the NC covaries with size of the face, whereas the MS "fills in" the leftover space [proposed by Shea: Am J Phys Anthropol 47 (1977):289-300]. Against expectation, MSV is not significantly correlated with NCV or any cranial size variable. NCV, on the other hand, scales isometrically with facial size. The results of this pilot study suggest that NCV covaries with facial size, but that the MS does not simply fill in the leftover space in the face. The role, if any, of the MSs in midfacial function and architecture remains unclear. Larger sample sizes, additional environmental variables, and assessment of MS and NC shape are necessary to resolve this issue.

Quantitative three-dimensional shape analysis of the proximal hallucial metatarsal articular surface in Homo, Pan, Gorilla, and Hylobates.

Multidimensional morphometrics is used to compare the proximal articular surface of the first metatarsal between Homo, Pan, Gorilla, Hylobates, and the hominin fossils A.L. 333-54 (A. afarensis), SKX 5017 (P. robustus), and OH 8 (H. habilis). Statistically significant differences in articular surface morphology exist between H. sapiens and the apes, and between ape groups. Ape groups are characterized by greater surface depth, an obliquely curved articular surface through the dorso-lateral and medio-plantar regions, and a wider medio-lateral surface relative to the dorso-plantar height. The OH 8 articular surface is indistinguishable from H. sapiens, while A.L. 333-54 and SKX 5017 more closely resemble the apes. P. robustus and A. afarensis exhibit ape-like oblique curvature of the articular surface.

Morphology and histology of chimpanzee primary visual striate cortex indicate that brain reorganization predated brain expansion in early hominid evolution.

Human brain evolution is characterized by an overall increase in brain size, cerebral reorganization, and cerebral lateralization. It is generally understood when brain enlargement occurred during human evolution. However, issues concerning cerebral reorganization and hemispheric lateralization are more difficult to determine from brain endocasts, and they are topics of considerable debate. One region of the cerebral cortex that may represent the earliest evidence for brain reorganization is the primary visual cortex (PVC), or area 17 of Brodmann. In nonhuman primates, this region is larger in volume (demarcated anteriorly by the lunate sulcus), and extends further rostrally than it does in modern humans. In early hominid fossil (Australopithecus) endocasts, this region appears to occupy a smaller area compared to that in nonhuman primates. Some have argued that the brain first underwent size expansion prior to reorganization, while others maintain that reorganization predated brain expansion. To help resolve this question, we provide a description of two male, common chimpanzee (Pan troglodytes) brains, YN77-111 and YN92-115, which clearly display a more posterior lunate sulcal morphology than seen in other chimpanzees. These data show that neurogenetic variability exists in chimpanzees, and that significant differences in organization (e.g., a reduced PVC) can predate brain enlargement. While the human brain has experienced numerous expansion and reorganization events throughout evolution, the data from these two chimpanzees offer significant support for the hypothesis that the neurogenetic basis for brain reorganization was present in our early fossil ancestors (i.e., the australopithecines) prior to brain enlargement.

Variability of Broca's area homologue in African great apes: implications for language evolution.

The cortical circuits subserving neural processing of human language are localized to the inferior frontal operculum and the posterior perisylvian region. Functional language dominance has been related to anatomical asymmetry of Broca's area and the planum temporale. The evolutionary history of these asymmetric patterns, however, remains obscure. Although testing of hypotheses about the evolution of language areas requires comparison to homologous regions in the brains of our closest living relatives, the great apes, to date little is known about normal interindividual variation of these regions in this group. Here we focus on Brodmann's area 44 in African great apes (Pan troglodytes and Gorilla gorilla). This area corresponds to the pars opercularis of the inferior frontal gyrus (IFG), and has been shown to exhibit both gross and cytoarchitectural asymmetries in humans. We calculated frequencies of sulcal variations and mapped the distribution of cytoarchitectural area 44 to determine whether its boundaries occurred at consistent macrostructural landmarks. A considerable amount of variation was found in the distribution of the inferior frontal sulci among great ape brains. The inferior precentral sulcus in particular was often bifurcated, which made it impossible to determine the posterior boundary of the pars opercularis. In addition, the distribution of Brodmann's area 44 showed very little correspondence to surface anatomy. We conclude that gross morphologic patterns do not offer substantive landmarks for the measurement of Brodmann's area 44 in great apes. Whether or not Broca's area homologue of great apes exhibits humanlike asymmetry can only be resolved through further analyses of microstructural components.

Missing Omo L338y-6 occipital-marginal sinus drainage pattern: ground sectioning, computer tomography scanning, and the original fossil fail to show it.

The Omo L338y-6 occipital region has been recently studied by White and Falk (1999), who claim that it shows a readily identifiable enlarged left occipital-marginal sinus (O/M). These observations are contrary to the direct observations of previous investigators (Rak and Howell, 1978; Kimbel, 1984; Holloway, 1981; Holloway, 1988). White and Falk (1999) further argue that the presence of this enlarged O/M strongly suggests that the Omo L338y-6 hominid was indeed a "robust" Australopithecus. We used direct sectioning and CT scanning to analyze magnified sections of a high-quality first-generation cast of the newly cleaned original fossil. These methods fail to show any evidence of a morphological landmark that can be interpreted as an enlarged O/M, either as an eminence or a sulcus. In contrast, the same techniques used with both SK 1585 and OH5 ("robust" Australopithecus with an enlarged O/M) show extremely visible and palpable enlarged O/M's. Examination of the original Omo fossil confirms that it lacks an O/M. This evidence clearly shows that an enlarged O/M cannot be identified on either the original fossil or a first-generation cast, although this does not rule out the possibility that the Omo L338y-6 hominid was a "robust" Australopithecus. We believe that the differences between observers regarding this feature are most probably due to displacement caused by a crack and the different source materials employed, i.e., the difference between a first-generation cast of the original fossil and a third- or fourth-generation cast of the endocast made two decades ago.