The brain is a soft-tissue organ surrounded by the bony structure of the skull, where changes in one require changes in the other. From infancy, the bones of the skull are separated by membranous sutures and with rapid brain expansion, these membranous regions of the skull are replaced by bone, fusing the skull into a protective structure around the adult brain. Ontogeny describes changes in the same anatomical structure throughout the life cycle, including the differences between age groups, within a species and across species, while allometry can explain size-related changes to skull shape, particularly between species. The individual bones of the skull join at sutures to form modules which include the facial block, the cranial vault and the cranial base.
A new paper by Scott et al. (2018) examined allometry and ontogeny in the hominid skull. The skulls from three hominid (great ape) species included the Bornean orangutan, the Western lowland gorilla and the common chimpanzee from several age groups were analyzed, and geometric morphometrics was used to capture shape change and allometry in the facial block and endocranium (as an indirect proxy for brain form). Covariation between the facial block and endocranium was tested using 2-block partial least-squares analysis. Results for ontogeny suggested endocranial change was lesser in younger age groups but with increasing age, orangutans separated from gorillas and chimpanzees, showing the greatest difference in face-to-brain shape. Results for allometry indicated that changes in facial shape were mostly related to size differences. However, the endocranium was not entirely influenced by changes in size, suggesting shape change in the endocranium is somewhat independent.
Ultimately, Scott and colleagues have shown the covariation between the facial block and the endocranium was more conserved in all three ape species in younger age groups, but the facial block continued to change shape into adulthood even after the brain growth had stopped. This suggests the endocranium is driven by changes to brain form during earlier stages of life before the cranial vault exerts a greater influence in late adolescence. However, the greatest change to skull morphology occurred during adulthood in facial shape.
A recent work, analyzing the development and evolution of the primate cortical folding, evidences two separate folding processes of the neocortex. Namba and colleagues examine two subtypes of neocortex, the dorsal isocortex, defined as the portion of neocortex limited laterally by the lateral fissure (LF) and medially by the cingulate sulcus (CiS), and the proisocortex within these same boundaries, comprising the insular cortex and the cingulate cortex, respectively. Their sample was composed by three to five specimens from 13 different primate species, including two great apes (humans and chimpanzees), two Old World monkeys, four New World monkeys, one tarsier, one galago, and three lemurs. For each specimen they analyzed five comparable coronal sections. They measured the gyrencephalic index (GI) as the ratio of the length of the inner to outer cortex contours, and calculated the LF score as the ratio of the LF greatest depth to the maximum width of the hemisphere. Then they analyze the relationships between LF score, and the GI values for the dorsal isocortex, the cingulate and insular cortices, and the neocortex, which included the three cortices and the temporal isocortex. To provide an evolutionary perspective, they reconstruct GI and LF score values for the primate ancestors. Furthermore, they examine the timing of folding in a longitudinal sample of humans and long-tailed macaques, and the folding differences in human lissencephalic patients, for a developmental and genetic overview. The proisocortex showed a similar GI across the sample, and the reconstructed ancestor LF scores were in the same magnitude as those of the 13 present-day primates. Conversely, the degree of folding of the dorsal isocortex differs across the species, and between the ancestors and the extant species, increasing with increasing folding of the neocortex. Furthermore, their analyses also revealed that LF and CiS appear earlier in development, while the dorsal isocortex starts to fold later. This portion of the cortex is also the most affected in human lissencephaly, as the LF, and CiS to a lesser degree, are still detectable in all grades of malformation. Hence, the authors conceptualize the folding of the neocortex as two distinct and sequential processes. The conserved folding occurs earlier in development, at the boundaries between the proisocortex and the dorsal isocortex, and involves the formation of the LF and CiS. The evolved folding occurs within the isocortex, after the onset of the conserved folding. Moreover, the authors suggest these two processes might be influenced by different cellular mechanisms, with neuron production contributing more to the conserved folding, and neuron migration to the evolved folding, a matter deserving further investigation.
In evolutionary biology, microevolution and macroevolution impact on the variation and covariation between genotype and phenotype. A related concept is the biological ability of an organism to adapt and evolve, or its evolvability, which is of keen interest to evolutionary biologists. The quantification of genetic change is analysed via the genetic variance-covariance matrix (G-matrix) while phenotypic change is analysed via the phenotypic variance-covariance (P-Matrix). Under the assumption of a neutral evolutionary model with the absence of genetic drift, the G-matrix should be proportional to a P-matrix. Although there is potential for theoretical complications arising from organisms with higher evolvability biasing the rates of evolutionary change, this is not fully investigated and seems to warrant further empirical studies.
The diversity of craniofacial form observed in fossil species of genus Homo and modern humans has been examined in terms of craniofacial adaptation to various biomechanical and environmental stressors. The absence of recovered genomes from species of fossil Homo beyond Homo neanderthalensis and fossil Homo sapiens has required studies of fossil human phylogenetics to rely on high uncertainties in the estimation of fossil hominin phylogeny and further restricted by small sample sizes.
In a recent study, Baab (2018) used the rate of evolutionary change in populations of modern Homo sapiens to estimate evolutionary rates in species of fossil Homo, analyzing craniofacial shape change, diversification and evolvability in the genus Homo. Results were consistent with independent conclusions that a neutral evolutionary model was adequate to generate the diversity in craniofacial form observed in the genus Homo. Once accounting for the small fossil sample size and the degree of evolutionary rate being higher than chance, there was no statistically significant support for higher rates of evolvability generating more rapid rates of evolutionary change across the entire genus Homo.
In contrast, the more recent lineages showed some evidence for selection acting at a greater magnitude in H. neanderthalensis and early H. sapiens, generating a more rapid rate of evolutionary change. Baab (2018) suggests brain expansion may be a likely contributor influencing the more rapid evolutionary rate change in craniofacial shape as observed in early H. sapiens and H. neanderthalensis and why only the more recent lineages of the genus Homo were affected by such rapid changes in craniofacial form.
The gray mouse lemur (Microcebus murinus) is a small Madagascan primate, averaging 12 cm length and weighing between 60-120 grams. Despite the diminutive size, mouse lemurs are increasingly used in medical studies of Alzheimer’s disease and similar neurological disease processes found in humans. Mouse lemurs often live to 12 years or more in the wild, which combined with torpor (a form of short-term hibernation) may be associated with the longer lifespans. Considering mouse lemurs have prolonged lifespans, it is probably not surprising that they also experience age-related brain atrophy. Nadkarni et al. (2019) address the absence of a dedicated mouse lemur brain atlas through in-vivo MRI scanning 34 mouse lemurs, investigating age-related brain atrophy and the neuroanatomy of Microcebus murinus in a comparative context. Results showed that most of the cerebral cortex was affected with age-related brain atrophy including the primary visual cortex and, although the remainder of the primary sensory areas were unaffected by atrophy, an even higher amount of atrophy was found in the sub-cortical brain regions including the thalamus, hippocampus and amygdala. All previous studies of mouse lemur neuroanatomy have been conducted with histological atlases. However, Nadkarni and colleagues compared mouse lemur cerebral to cortical volumes using high-quality MRI, finding that contrary to histology studies, mouse lemurs had similar cortical to cerebral volume indices to other primate species and were not to be considered a “lesser primate” species as has been previously argued. The proportion of cerebral white matter was the highest in humans, before a continual decrease in macaques and smaller monkeys with the lowest white matter volumes observed in mouse lemurs. The trend for increasing white matter volumes in primates, culminating with the highest values in humans, has often been argued as necessary for reinforcing intra-cerebral connectivity, hypothesized as an important process in primate brain evolution.
Included with this study of mouse lemurs, Nadkarni and colleagues also produced an accompanying MRI in-vivo brain atlas which includes 120 labelled brain structures specific to Microcebus murinus which to-date, has been unavailable. The accessibility of a brain atlas specific for mouse lemurs removes the time-consuming process of manual MRI segmentation, allowing quick and direct comparison of brain regions with other primates for a comparative evolutionary context and in medical research for Alzheimer’s disease.
The traces of the middle meningeal artery (MMA) can be observed on dry skulls. For this reasons, it is often investigated in paleoneurology. The vessels run between the two layers of dura mater, along with the endosteal (periosteal) layer which is adherent to the inner surface of the skull. The MMA display connections with other vascular networks, but it is largely independent of the cerebral vascular system. Apparently, in adults there is only scarce or absent blood flow in MMA at rest, and activation may be triggered by thermal stress or other emergency responses (see Bruner et al. 2011). In a recent paper, Niknejad and colleagues (2018) test the possibility of using the MMA as a donor vessel in cerebrovascular bypass procedures, as an alternative to the superficial temporal artery (STA) which is standardly used for this purpose. The authors performed cadaveric dissections on 12 specimens and compared size, diameter and feasibility of both the MMA and the STA for the bypass to the middle cerebral artery. Their results confirmed that the MMA can be a suitable donor vessel. The premise of the donor potential of the MMA is based on its dispensability. Nevertheless, the authors note that the MMA may play an important role in case of the moyamoya disease, in which conditions MMA forms an important collateral network. In addition, this study provides valuable empirical data on the MMA morphology. Authors were able to identify three main branches in all specimens, with the dominant anterior petrosquamosal branch in all the cases. The diameter of the MMA was measured at its ostium and was 2.4 mm in average.
Since the early 2000s, the expansion of digital anatomy tools has been aided by advances in computational power and accessibility of medical imaging such as Computed Tomography (CT). The greater accessibility to digital imaging of fossil material has allowed the reconstructions of inner cranial cavities (endocasts), sinuses cavities, and dental reconstructions of the enamel-dentine junctions (EDJ) of fossilized teeth. Despite great accessibility, the segmentation processes used to generate digital reconstructions of inner cavities remain time-consuming and require specific expertise in computer analysis, anatomy, digital imaging.
Profico et al. (2018) provide two fully-automated digital methods to minimize these time-consuming digital segmentation tasks. Both of these methods rely on point-of-views (POVs) to delineate a region-of-interest (ROI). In the CA-LSE method, POVs were located outside a ROI and all areas beyond are subtracted from the final reconstruction. In contrast, the AST-3D method relies on a ROI defined by POVs placed inside a cavity and all external areas, subtracted from the final reconstruction. While both methods are similar and can be used to generate reconstructions of the inner cavities, each method has slightly different benefits. Profico and colleagues conducted a comparison of both methods to determine strengths and weaknesses of each approach. While both of these methods are available through the Cran R network, two different R packages were tested: Morpho and Arothron.
Results indicated that in the Morpho package, CA-LSE had no restrictions on where POVs could be placed, but using AST-3D method in Morpho, POVs had to be manually placed inside the internal cavity for successful reconstruction. In the Arothron package, CA-LSE method allowed fully-automated placement of POVs outside the ROI surface, however, the AST-3D method a ROI must be defined by manually placed POVs within the inner cavity. In general, accuracy of the AST-3D and CA-LSE methods were determined by each method, with AST-3D more reliable generating reconstructions of inner cavities (such as endocasts), while the CA-LSE was more suited to reconstructions of outer structures (such as skulls).
Although, automatic approaches offer time-efficiency and often allow larger sample sizes to be more quickly processed, many fossilized skulls are highly fragmentary and automated methods remain limited when fossilized remains are partially or entirely matrix-filled with anatomical and digital expertise still requiring manual segmentation. In these complex scenarios, further fine-tuning of automated methods would be invaluable with inclusion of fully-automated, semi-automatic and manual options.
European Society for the study of Human Evolution – Faro, 2018
Duan and colleagues developed a new computational method for automatic detection of patterns of cortical folding in large datasets. This method extracts multiple features that characterize the folding patterns, such as sulcal bottoms and gyral crest curvatures. Then, an overall similarity matrix is calculated that contains information on shared patterns and individual variation. Finally, the subjects are clustered on groups that represent a common folding pattern. The authors show their method is more efficient than previous ones in detecting folding patterns and clustering subjects into affinity groups. They validate its reproducibility and reliability in two main samples. They demonstrate the application of their methodology on a large sample of 595 healthy neonate brains, to characterize folding patterns in newborns. Then, they compare their results to a dataset of adult brains from the Human Connectome Project. They focus on four cortical regions, the superior temporal gyrus (STG), the inferior frontal gyrus (IFG), the cingulate cortex, and the precuneus, considering both sex differences and hemispheric asymmetries. Overall, the typical folding patterns of infants were consistent with those of adults, evidencing that cortical folds are largely established from an early age. On the other hand, some differences were also identified. For instance, four folding patterns were recognized in infant STG, while adults have an extra pattern. In contrast, one of the neonates’ IFG pattern is absent in adults. In both samples, there are sex differences in the proportions of some of the folding patterns of STG, IFG, and cingulate cortex. Hemispheric asymmetries were observed in the cingulate and STG, being more significant in the latter, which the authors suggest might reflect language lateralization. Considering the precuneus, their method revealed three main gyral patterns which were not associated with sex differences or hemispheric asymmetries. These gyral patterns appear to be mainly grouped based on the presence of either a gyral structure (patterns 1 and 2, more frequent) or a deep sulcus (pattern 3) in the middle of the precuneus. According to the authors, these groups are similar to the ones described in a previous study by our lab on a sample of adult healthy brains.
From Fossils to Function
Integrative and Taxonomically-Inclusive Approaches to Vertebrate Evolutionary Neuroscience
Brain, Behavior and Evolution, 91