From Fossils to Function
Integrative and Taxonomically-Inclusive Approaches to Vertebrate Evolutionary Neuroscience
Category Archives: Neurobiology
From Fossils to Function
Comparative neurobiology has traditionally been used to describe and quantify the macro-and micro-anatomical changes to the brain between human and non-human primates. Research literature commonly refers to the Stephen dataset with brain volumes measured from a small sample of ex-vivo non-human primate brains with species often represented by only one or two individuals. Although this is common limitation inherent to many physical neuroanatomy collections, caution should be used with such limited samples not representative of a species and the actual variation unknown. The consequences for such assumptions on quantifying the neuroanatomical differences between humans and non-human primates have broader implications for human evolution. Despite the increasing accessibility of primate neuroimaging datasets, many comparative studies still rely on the Stephen brain volumes. This is despite the necessary factoring of numerous bias including cerebral tissue damage from the delay between the post-mortem interval and brain preservation, potential introduction of artifacts from tissue preservation processes causing shrinkage, some cellular destruction and occasional damage during brain extraction.
Navarette and colleagues recently compared digital neuroanatomical volumes from ex-vivo brain MRI with the Stephen data using the same primate species but including an extra 20 species. Results showed differences between the Stephen data and those obtained by Navarrete et al. with larger brain volumes measured in the pre-fixed state versus post-fixed, indicating fixation did noticeably affect brain volume measurement. Although Navarrete et al. aimed to quantify primate brain volume variation by increasing the number of primate species to 39, there were still 29 species represented by only one individual, while the maximum of for the entire sample was never greater than three individuals per species. Although Navarrete et al. argued a lack of larger in-vivo primate brain neuroimaging datastes, several are accessible as part of the National Chimpanzee Research Center. More broadly, Navarrete and colleagues have shown quantifiable differences between pre- and post-fixed brain volumes and emphasised the need for caution in the suitability of ex-vivo brain collections to provide reliable volumetric measurements for comparative primate neuroanatomy.
The parietal lobe has a unique central location in the brain, and it is involved in higher cognitive functions. Investigating its functions and connectivity is essential to understand its role in uniquely human abilities. Two recent works have put emphasis on the importance of the parietal lobe for tool use.
Catani and colleagues investigated the intralobar parietal connectivity in human and monkey brains, using diffusion imaging tractography. In general, the patterns of white matter connectivity are similar in both species, although with some differences for areas that are distinct in humans. The larger tract connects the superior parietal lobule (SPL) to the angular and supramarginal gyri of the inferior parietal lobule, within the IPS. The authors suggest it might act to mediate the interaction between the two lobules during object manipulation, and to coordinate both dorsal and ventral visuospatial networks. The second and third larger tracts link the postcentral gyrus to the inferior parietal lobule and to the SPL, respectively. These might transmit tactile and proprioceptive information on the body orientation relatively to an object for guiding motor actions and grasp. The connection between the postcentral and the angular gyri was only observed in humans, leading the authors to highlight its role in specific cognitive functions. Particularly, its connections to SPL are key for tool use, mathematical thinking, and language and communication.
Kastner and coworkers reviewed the organization and function of the dorsal pathway of the visual system of monkey and human brains, focusing on the areas of the posterior parietal cortex within and adjacent to the intraparietal sulcus (IPS). Monkeys and humans have diverged in the functional contributions of the IPS since their last common ancestor, as some functionally-defined areas that are located within the IPS in monkeys have been partially relocated outside this sulcus in humans. The authors suggest this relocation might be due to expansion for accommodation of human-specific abilities, such as tool use. They hypothesize that humans might have developed a derived and advanced tool network from the modification of the macaque circuit for object manipulation. First, the human dorsal vision pathway must provide object shape information regardless of size and viewpoint, facilitating object recognition and mental manipulation. Second, object information is integrated with cognitive information such as working memory, allowing maintaining the information over a period of time. Finally, humans have areas that respond specifically to tool use, some of which also integrate frontal and temporal networks involved in action recognition and semantic knowledge related to tools and actions, respectively.
Both studies point at the parietal lobes and visuospatial integration as key elements for human cognitive capacity, as suggested by evidence in paleoneurology, evolutionary neuroanatomy, and cognitive archaeology.
Space missions can have adverse effects on astronauts, such as the already-mentioned vision deterioration and cognitive impairment. Spending a long time on space can also impact sensorimotor function. Koppelmans et al. have recently investigated the influence of microgravity environment on sensorimotor performance and brain structure. They conducted a longitudinal study with a group of male subjects remaining in a 6-degrees head down tilt bed rest (HDBR) position, an analog environment to study the effects of spaceflight microgravity, during 70 days. MR images were collected before, during, and after HDBR, to explore changes in gray matter (GM) volume, and functional mobility and postural equilibrium tests were conducted pre- and post-HDBR, to check sensorimotor performance. For control, they used data from other subjects who had completed the same measurements at four different times over 90 days for another study, not being exposed to HDBR. Relative to controls, the HDBR subjects showed widespread changes in GM volume, as the percent of brain volume, from pre- to the last assessment during HDBR. More specifically, GM volume increased in the posterior parietal region and decreased in the fronto-temporal regions, and these changes are strongly correlated. The sensorimotor performance was decreased in HDBR subjects from pre- to post-HDBR, as they needed more time to complete the test, while controls showed no difference in performance. Following the HDBR period, both GM volume and sensorimotor changes started to recover, though not totally 12 days later. Regarding the association between brain and behavior, researchers found that larger increases in GM volume in precuneus and pre- and postcentral gyri correlated with better balance performance, though not significantly after Bonferroni correction. They propose these changes in GM volume might reflect cortical plasticity as an adaptive response to alterations in somatosensory input caused by HDBR position. The observed patterns of GM change could also be explained by alterations in intracranial fluids distribution and pressure due to posture, though this hypothesis would need further examination. The authors conclude their findings match the sensorimotor deterioration observed in astronauts, but are also of interest for individuals who are temporarily or permanently confined to a bed and will probably experience the same GM and sensorimotor alterations.
The Internet Brain Volume Database (IBVD) is an online collection of neuroimaging data funded as a part of the international initiative, the Human Brain Project. The IBVD provides access data for both individual and among-group comparisons that allow total volume comparisons with parallelization of the brain into hemispheres, specific lobes or grey matter volumes. While the database contains data on humans, there is also non-human primate (macaque) and rat studies. A summary search provides information on sex, age and handedness as well as age-related pathology, neuro-psychiatric disease, structural disease and twin-studies (monozygotic and dizygotic). These selected individuals can be compared to normal studies or pooled into user-specified group results. For example, it is very easy to generate a plot of left vs. right temporal lobe volume compared to age in normal human in vivo males and females.
The mature primate brain consists of many layers with the outer layer or cerebral cortex forming folds known as sulci and gyri. During embryonic development, the brain is divided into zones with the inner-most ventricular zone where neurons are formed and a series of cytoarchitecturally distinct layers forming plates radiating outward. The subplate is located between the inner ventricular zone and the outer cortical plate hosting the migration of neurons allowing brain expansion. Most embryonic brain research is conducted on non-primate mammals but there are substantial differences in the development of the non-primate and primate brain. A very recent study utilized existing primate tissue databases to examine the embryonic development of the subplate zone in non-human and human primates. Duque et al. found during that development of the macaque brain, once the neurons have migrated to the subplate they then are pushed downward by axons derived from the subcortical layer before further compression occurs from further axonal development originating from the cortical layer. The implications of this force acting on the neurons within the subplate suggests that thickness of the subplate differs unevenly throughout the brain potentially due to an increased axonal density. Duque et al. suggest the density of axonal fibers increases with demand for more connectivity between brain regions with those areas possessing a high-demand for greater complexity causing a thicker subplate.
Changes at the cellular-level of the subplate also have implications for the development of the cerebral convolutions such as sulci and gyri. It was recently posed that the folding patterns in the human brain are the result of mechanical forces related to the subplate and outer expansion of the cerebral cortex. Tallinen et al. showed through numeric and physical simulations with the support of MRI that during fetal development the subplate stabilizes while the outer cortical plate continues to expand. The final stages of growth see the cortical layer undergo extensive gyrification to form the folding patterns we see in the adult human brain. Overall, a better understanding of human neurobiology informed through non-human primate neurobiology offers a glimpse into the evolutionary pathways which led to the evolution of modern humans.
Recently Brazil has declared state of emergency due to an epidemic of newborn microcephaly. Children with microcephaly have significantly smaller head circumference than the mean for their age and body size. It results from abnormal brain development before birth or during infancy that can be caused by genetic (e.g. Down syndrome) or environmental factors affecting development, for instance craniosynostosis, malnutrition, and infection. Children with this condition may be cognitively impaired and need special medical care throughout their lives. During 2015 Brazil has been registering a drastic increase in the cases of microcephaly, mainly in the northeastern states. For instance in Pernambuco there was 141 cases while the mean is around 10 per year. Coincident with this epidemic, Brazil was also affected by a Zika virus outbreak firstly detected in late April and confirmed in 14 states by November. This virus was first identified in the 1940’s in Uganda, and it is now distributed throughout several tropical countries. It is transmitted to humans by bites of infected mosquitoes of the genus Aedes, the same that transmit dengue and yellow fever. Because symptoms of infection by Zika virus are mild it has not been given much attention. However the coincidence between the virus outbreak and increased microcephaly incidence in Brazil led to a suspicion that there was an association, further reinforced by the confirmation of the virus during an autopsy of a microcephalic baby.
The relationship between microcephaly and Zika virus is now being investigated and the government is taking steps to control the mosquitoes’ population and to assist the children with microcephaly. This virus may have spread from the French Polynesia, where there was an outbreak in 2013-2014, and where the Zika virus was associated with neurological complications like Guillain-Barré syndrome. If an association between a mosquito-transmitted virus and neurological conditions is confirmed, further measures of prevention must be taken as the area favorable for mosquitoes spreading seems to be increasing.
There are plenty of reports about anatomical and morphological variation of cranial foramina; however, their developmental mechanisms fundamental for interpretation of such a variation and understanding of vital medical conditions related to their aberrant formation are poorly known. Cranial foramina transmitting the vessels and nerves emerge within the cranial bones which themselves show complex origin and development. Recent embryological study in chicks by Akbareian et al. (2015) presents development of cranial foramina in mesoderm derived occipital bone arising through endochondral ossification. Unexpectedly, the formation mechanism did not show any extensive apoptotic cell activity and target proliferation. Instead as a “clearing” mechanism forming the cavity of foramina was proposed localized restriction of ossification caused by the presence of vessel and nerve elements with minimal mesenchymal cell death. Further importance for morphological studies of foramina can bear a discovery that the shape of vessel dictates the overall shape of the foramen.