Emiliano Bruner

Encephalization and allometric trajectories in the genus Homo: Evidence from the Neandertal and modern lineages

The term “encephalization” is commonly used to describe an enlargement in brain size, considered as either absolute endocranial volumes or relative values in relation to body size. It is widely recognized that a considerable endocranial expansion occurred throughout the evolution of the genus Homo. This article aims to evaluate whether this phenomenon was the outcome of distinct evolutionary lineages, reaching similar brain expansions but through different trajectories. Endocranial morphology was studied in a sample of fossil hominines by multivariate approaches using both traditional metrics and geometric morphometrics. The analysis was focused on the transition from a generalized archaic pattern within the genus Homo to the modern morphology and compared with changes that occurred along the Neandertal lineage. The main result was the identification of two different evolutionary trajectories, in which a similar expansion in endocranial size has been reached by different changes in shape. Along the Neandertal lineage we observed maintenance of an “archaic” endocranial model, in which a large amount of variability is based on a single allometric trend. By contrast, when modern endocasts were compared with nonmodern ones, we found important differences apparently led by a parietal expansion. In this light, the origin of our species may have represented the opportunity to surpass the constraints imposed on encephalization by the ontogenetic pattern shared by nonmodern Homo representatives.

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 Brocas area was investigated in extant and extinct humans. Our results do not support positive allometry for the frontal lobes 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 Brocas 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.

Cranial shape and size variation in human evolution: structural and functional perspectives.

A glimpse into modern paleoanthropologyIn the last decades, paleoanthropology has been deeply modified, changing from a descriptive and historical science to a more quantitative and analytical discipline. The covariation of multiple traits is investigated to study the evolutionary changes of the underlying anatomical models, mostly through the introduction of digital biomedical imaging procedures and of computed geometrical analyses supported by multivariate statistics.Functional craniologyThe evolution of the human cranium is consequently considered in terms of functional and structural relationships between its components, largely influenced by the allometric variations associated with the increase in the relative cranial capacity. In the human genus, the changes in the face, base, and neurocranium are characterised by a mosaic variation, in which adaptations, secondary consequences, and stochastic factors concur to generate a set of anatomical possibilities and constraints.Systemic perspectives to the evolution of the human cranial morphologyConcepts like morphological modularity, anatomical integration, and heterochrony represent key issues in the development of the current human evolutionary studies.

A Quantitative and Descriptive Approach to Morphological Variation of the Endocranial Base in Modern Humans

The cranial base is one of the major foci of interest in functional craniology. The evolution and morphogenesis of this structure are still poorly known and rather controversial because of multifactorial influences and polyphasic stages. Endocranial dynamics are associated anteriorly with the upper facial structures, laterally with the mandibular system and midsagittally with brain development. In the present study, we investigated the endocranial morphology of modern humans using 3D landmark-based approaches, i.e. geometric morphometrics and Euclidean distance matrix analysis. The structure of endocranial variation is poorly integrated, with only weak reciprocal influences among the three fossae. Some major variations are associated with changes in the posterior fossa, with possible consequences on the anterior areas. These main patterns of integration are hypothesized to be influenced by the connective tensors of the dura layers. Static allometry and sex differences are largely related to the ontogenetic sequences, characterized by early maturation of the anterior fossa with respect to the middle and posterior regions (i.e., relatively shorter posterior part of the planum sphenoideum and vertical lengthening of the clivus in males). The relative independence between the endocranial fossae, as well as their structural connection through the meningeal tensors, must be carefully considered in studies on the evolutionary dynamics, since they lead to mosaic changes through phylogeny.

Human midsagittal brain shape variation: patterns, allometry and integration

Midsagittal cerebral morphology provides a homologous geometrical reference for brain shape and cortical vs. subcortical spatial relationships. In this study, midsagittal brain shape variation is investigated in a sample of 102 humans, in order to describe and quantify the major patterns of correlation between morphological features, the effect of size and sex on general anatomy, and the degree of integration between different cortical and subcortical areas. The only evident pattern of covariation was associated with fronto‐parietal cortical bulging. The allometric component was weak for the cortical profile, but more robust for the posterior subcortical areas. Apparent sex differences were evidenced in size but not in brain shape. Cortical and subcortical elements displayed scarcely integrated changes, suggesting a modular separation between these two areas. However, a certain correlation was found between posterior subcortical and parietal cortical variations. These results should be directly integrated with information ranging from functional craniology to wiring organization, and with hypotheses linking brain shape and the mechanical properties of neurons during morphogenesis.

Functional craniology and brain evolution: from paleontology to biomedicine.

Anatomical systems are organized through a network of structural and functional relationships among their elements. This network of relationships is the result of evolution, it represents the actual target of selection, and it generates the set of rules orienting and constraining the morphogenetic processes. Understanding the relationship among cranial and cerebral components is necessary to investigate the factors that have influenced and characterized our neuroanatomy, and possible drawbacks associated with the evolution of large brains. The study of the spatial relationships between skull and brain in the human genus has direct relevance in cranial surgery. Geometrical modeling can provide functional perspectives in evolution and brain physiology, like in simulations to investigate metabolic heat production and dissipation in the endocranial form. Analysis of the evolutionary constraints between facial and neural blocks can provide new information on visual impairment. The study of brain form variation in fossil humans can supply a different perspective for interpreting the processes behind neurodegeneration and Alzheimer’s disease. Following these examples, it is apparent that paleontology and biomedicine can exchange relevant information and contribute at the same time to the development of robust evolutionary hypotheses on brain evolution, while offering more comprehensive biological perspectives with regard to the interpretation of pathological processes.

A Bivariate Approach to the Variation of the Parietal Curvature in the Genus Homo

The parietal bones approximately cover the extension of the underlying parietal lobes. Although the boundaries of these two anatomical elements do not coincide, during morphogenesis the growth of the parietal bones is largely induced by the pressure exerted by the parietal lobes. Modern humans display larger parietal chords and arcs compared with non‐modern human species. However, the variation of these variables have not been analyzed before according to the covariation with the general endocranial diameters. When the curvature of the parietal bones is regressed onto the main neurocranial distances, modern humans show larger relative values, suggesting not only an absolute enlargement but a definite allometric change. Taking into account the morphogenetic relationships with the parietal lobes, these results further support previous hypotheses suggesting a relative enlargement of these cortical areas in Homo sapiens, by using simple and reliable homologous neurocranial arcs. Anat Rec, 2011.

Fractal dimension of the middle meningeal vessels: variation and evolution in Homo erectus, Neanderthals, and modern humans.

The middle meningeal vascular network leaves its traces on the endocranial surface because of the tight relationship between neurocranial development and brain growth. Analysing the endocast of fossil specimens, it is therefore possible to describe the morphology of these structures, leading inferences on the cerebral physiology and metabolism in extinct human groups. In this paper, general features of the meningeal vascular traces are described for specimens included in the Homo erectus, Homo neanderthalensis, and Homo sapiens hypodigms. The complexity of the arterial network is quantified by its fractal dimension, calculated through the box-counting method. Modern humans show significant differences from the other two taxa because of the anterior vascular dominance and the larger fractal dimension. Neither the fractal dimension nor the anterior development are merely associated with cranial size increase. Considering the differences between Neanderthals and modern humans, these results may be interpreted in terms of phylogeny, cerebral functions, or cranial structural network.

Midsagittal brain variation and MRI shape analysis of the precuneus in adult individuals

Recent analyses indicate that the precuneus is one of the main centres of integration in terms of functional and structural processes within the human brain. This neuroanatomical element is formed by different subregions, involved in visuo‐spatial integration, memory and self‐awareness. We analysed the midsagittal brain shape in a sample of adult humans (n = 90) to evidence the patterns of variability and geometrical organization of this area. Interestingly, the major brain covariance pattern within adult humans is strictly associated with the relative proportions of the precuneus. Its morphology displays a marked individual variation, both in terms of geometry (mostly in its longitudinal dimensions) and anatomy (patterns of convolution). No patent differences are evident between males and females, and the allometric effect of size is minimal. However, in terms of morphology, the precuneus does not represent an individual module, being influenced by different neighbouring structures. Taking into consideration the apparent involvement of the precuneus in higher‐order human brain functions and evolution, its wide variation further stresses the important role of these deep parietal areas in modern neuroanatomical organization.

Alzheimer's disease: the downside of a highly evolved parietal lobe?

Clinical grade Alzheimers disease (AD) is only described in humans. Recent imaging studies in early AD patients showed that the parietal areas display the most prominent metabolic impairments. So far, neuroimaging studies have not been able to explain why the medial parietal regions possess this hub characteristic in AD. Paleoneurological and neuroanatomical studies suggest that our species, Homo sapiens, has a unique and derived organization of the parietal areas, which are involved in higher cognitive functions. Combining evidence from neuroimaging, paleontology, and comparative anatomy, we suggest that the vulnerability of the parietal lobe to neurodegenerative processes may be associated with the origin of our species. The species-specific parietal morphology in modern humans largely influenced the brain spatial organization, and it involved changes in vascularization and energy management, which may underlie the sensitivity of these areas to metabolic impairment. Metabolic constraints and anatomical evolutionary changes in the medial parietal regions of modern humans may be important in early AD onset. Taking into account the species-specific adaptations of the modern human parietal areas and their association with AD, we hypothesize that AD can be the evolutionary drawback of the specialized structure of our parietal lobes. The cognitive advantage is associated with increased sensitivity to neurodegenerative processes which, being limited to the post-reproductive period, have a minor effect on the overall genetic fitness. The changes of energy requirements associated with form and size variations at the parietal areas may support the hypothesis of AD as a metabolic syndrome.