Emiliano Bruner’s research while affiliated with The National Museum of Natural Sciences and other places

The Evolutionary Roots of Human Brain Diseases takes an innovative approach and assembles recent findings ranging from evolutionary biology and anthropology to clinical neurosciences, all showing the price on health of human brain evolution. Written by experts in their field, the chapters explore the tenet that extensive human brain development during evolution has given rise to exclusively human brain diseases, both priming and impacting their clinical expression. There are presentations on cerebral cellular specificities or human-specific network developments, detailed discussions of neurological or psychiatric diseases with an evolutionary focus, and chapters exploring evolutionarily grounded medication developments as well as cultural and societal repercussions. Evolutionary concepts ranging from genetic pleiotropic antagonism to disease remnants of ancient behaviors crucial for survival are presented. The horizon is extended to include potential repercussions of ongoing human evolution on the human brain when cultural evolution outpaces biological evolution.

Considering the biomechanical and cognitive aspects involved in tool manipulation, hand size emerges as a critical factor. Males, on average, exhibit greater grip strength attributed to larger hand dimensions. Beyond mere physical factors, cognitive components tied to visuospatial abilities also influence stone tool use. However, the intricate relationship between hand size, grip strength, and ergonomic patterns necessitates further exploration. Here, we study the ergonomic pattern of phalanx flexion during the manipulation of Lower Paleolithic stone tools (choppers and handaxes) to understand the nuanced interplay between hand dimensions and grasping behaviors in Lower Paleolithic stone tool use. The static hand posture during the comfortable grasping of each tool is measured using a motion capture hand glove. Flexions are measured at the metacarpophalangeal joint, the proximal interphalangeal joint and the distal interphalangeal joint of each finger. Our investigation into Lower Paleolithic stone tool manipulation reveals gender-based differences in phalanx flexion, with hand dimensions showing correlation only in pooled samples. However, these associations diminish when analyzing males and females separately. This study suggests a minimal link between hand size and grasping behavior within our sample, hinting at the influence of cognitive, behavioral, and motor factors. Exploring lifestyle and psychometric profiles could provide further insights. In the context of early human technology, our results prompt considerations on the evolution of the hand-tool interaction system, linking our tool-dependent culture to our phylogenetic history.

Spatial interactions among anatomical elements help to identify topological factors behind morphological variation and can be investigated through network analysis. Here, a whole‐brain network model of the chimpanzee ( Pan troglodytes , Blumenbach 1776) is presented, based on macroanatomical divisions, and compared with a previous equivalent model of the human brain. The goal was to contrast which regions are essential in the geometric balance of the brains of the two species, to compare underlying phenotypic patterns of spatial variation, and to understand how these patterns might have influenced the evolution of human brain morphology. The human and chimpanzee brains share morphologically complex inferior‐medial regions and a topological organization that matches the spatial constraints exerted by the surrounding braincase. These shared topological features are interesting because they can be traced back to the Chimpanzee‐Human Last Common Ancestor, 7–10 million years ago. Nevertheless, some key differences are found in the human and chimpanzee brains. In humans, the temporal lobe, particularly its deep and medial limbic aspect (the parahippocampal gyrus), is a crucial node for topological complexity. Meanwhile, in chimpanzees, the cerebellum is, in this sense, more embedded in an intricate spatial position. This information helps to interpret brain macroanatomical change in fossil hominids.

The human brain's complex morphology is spatially constrained by numerous intrinsic and extrinsic physical interactions. Spatial constraints help to identify the source of morphological variability and can be investigated by employing anatomical network analysis. Here, a model of human craniocerebral topology is presented, based on the bony elements of the skull at birth and a previously designed model of the brain. The goal was to investigate the topological components fundamental to the craniocerebral geometric balance, to identify underlying phenotypic patterns of spatial arrangement, and to understand how these patterns might have influenced the evolution of human brain morphology. Analysis of the craniocerebral network model revealed that the combined structure of the body and lesser wings of the sphenoid bone, the parahippocampal gyrus, and the parietal and ethmoid bones are susceptible to sustain and apply major spatial constraints that are likely to limit or channel their morphological evolution. The results also showcase a high level of global integration and efficient diffusion of biomechanical forces across the craniocerebral system, a fundamental aspect of morphological variability in terms of plasticity. Finally, community detection in the craniocerebral system highlights the concurrence of a longitudinal and a vertical modular partition. The former reflects the distinct morphogenetic environments of the three endocranial fossae, while the latter corresponds to those of the basicranium and calvaria.

Although both central and peripheral inflammation have been consistently observed in depression, the relationship between the two remains obscure. Extra-axial immune cells may play a role in mediating the connection between central and peripheral immunity. This study investigates the potential roles of calvarial bone marrow and parameningeal spaces in mediating interactions between central and peripheral immunity in depression. Positron emission tomography was employed to measure regional TSPO expression in the skull and parameninges as a marker of inflammatory activity. This measure was correlated with brain TSPO expression and peripheral cytokine concentrations in a cohort enriched for heightened peripheral and central immunity comprising 51 individuals with depression and 25 healthy controls. The findings reveal a complex relationship between regional skull TSPO expression and both peripheral and central immunity. Facial and parietal skull bone TSPO expression showed significant associations with both peripheral and central immunity. TSPO expression in the confluence of sinuses was also linked to both central and peripheral immune markers. Group dependant elevations in TSPO expression within the occipital skull bone marrow were also found to be significantly associated with central inflammation. Significant associations between immune activity within the skull, parameninges, parenchyma, and periphery highlight the role of the skull bone marrow and venous sinuses as pivotal sites for peripheral and central immune interactions.

The term craniovascular traits refers to the imprints left by arteries and veins on the skull bones. These features can be used in biological anthropology and archaeology to investigate the morphology of the vascular network in extinct species and past populations. Generally, the term refers to macrovascular features of the endocranial cavity, like those associated with the middle meningeal artery, venous sinuses, emissary foramina, and diploic channels. However, small vascular passages (here called microforamina or microchannels) have been occasionally described on the endocranial surface. The larger ones (generally with a diameter between 0.5 and 2.0 mm) can be detected through medical scanners on osteological collections. In this study, we describe and quantify the number and distribution of these microforamina in adult humans (N = 45) and, preliminarily, in a small sample of children (N = 7). Adults display more microchannels than juvenile skulls. A higher frequency in females is also observed, although this result is not statistically significant and might be associated with allometric cranial variations. The distribution of the microforamina is particularly concentrated on the top of the vault, in particular along the sagittal, metopic, and coronal sutures, matching the course of major venous sinuses and parasagittal bridging veins. Nonetheless, the density is lower in the region posterior to bregma. Beyond oxygenation, these vessels are likely involved in endocranial thermal regulation, infection, inflammation, and immune responses, and their distribution and prevalence can hence be of interest in human biology, evolutionary anthropology, and medicine.

Evolutionary anthropology relies on both neontological and paleontological information. In the latter case, fields such as paleoneurology, neuroarchaeology, and cognitive archaeology are supplying new perspectives in prehistory and neuroscience. Cognitive archaeology, in particular, investigates the behaviors associated with extinct species or cultures according to specific psychological models. For example, changes in working memory, attention, or visuospatial integration can be postulated when related behavioral changes are described in the archaeological record. However, cognition is a process based on different and partially independent functional elements, and extinct species could hence have evolved distinct combinations of cognitive abilities or features, based on both quantitative and qualitative differences. Accordingly, differences in working memory can lead to more conceptual or more holistic mindsets, with important changes in the perception and management of the mental experience. The parietal cortex is particularly interesting, in this sense, being involved in functions associated with body–tool integration, attention, and visual imaging. In some cases, evolutionary mismatches among these elements can induce drawbacks that, despite their positive effects on natural selection, can introduce important constraints in our own mental skills. Beyond the theoretical background, some hypotheses can be tested following methods in experimental psychology. In any case, theories in cognitive evolution must acknowledge that, beyond the brain and its biology, the human mind is also deeply rooted in body perception, in social networks, and in technological extension.

The term craniovascular traits refers to the imprints left by arteries and veins on the skull bones. These features can be used in anthropology and archaeology to investigate the morphology of the vascular network in extinct species and past populations. Generally, the term refers to macrovascular features of the endocranial cavity, like those associated with the middle meningeal artery, venous sinuses, emissary foramina, and diploic channels. However, small vascular passages (here called microforamina or microchannels) have been occasionally described on the endocranial surface. In this study, we describe and quantify the amount and distribution of these microforamina in adult humans (N = 45) and, preliminarily, in early to late juvenile subjects (N = 7). Adults display more microchannels than juvenile skulls. Females show more channels than males, and it should be evaluated whether this trait can represent a new described sexual features, influenced by sex biology. The distribution of the microforamina is particularly concentrated on the top of the vault, in particular along the sides of the sagittal, metopic, and coronal sutures, matching the course of major venous sinuses. Nonetheless, the density is lower in the region behind the bregma. A preferential pattern of distribution seems to join diagonally the coronal and dorsal parietal regions. Beyond oxygenation, these features are likely involved in endocranial thermal regulation and immune responses, and their distribution and prevalence can hence be of interest in human biology, evolutionary anthropology, and medicine.

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.