In the light of evolution: Principles of brain organization deduced from cross-species neuroimaging

Brains come in various shapes and sizes. Nature shows many small-brained species as well as endowed big-brained primate species like humans and chimpanzees with a proportionally large cerebral cortex. The field of 'comparative connectomics' studies commonalities in principles of neural wiring that apply across species, combined with how variations in connectivity between species may form the basis of species-specific brain function and behavior. In this talk, I will discuss both the technical challenges and opportunities of cross-species connectomics. I will start by discussing the methodology and technical details of comparing connectome maps across species. I will focus on the 'how to' and provide an overview of the challenges, technical details, and the importance of the availability of homologous brain atlases and their use in network reconstruction. In the second part, I will discuss examples of the application of these methods. I will discuss a comparison of global white matter connectivity across primate species with a 350-fold range of brain volume and the effect of allometric scaling of brains on network modularity, connectivity, and features of integration and communication. I will further link this work to the evolution of (human) cognition. For chimpanzee-human comparisons, I will discuss the notion of cognitive networks consistent across the two species, together with subtle adaptations of connectome architecture to higher-order cognitive networks (such as the default mode network) in humans, compared to a fine-tuning of the connectome network to visual and spatial working memory functions in chimpanzees. 

The complexity of the human brain has been shaped over extended temporal scales, underscoring its profound anchoring within a rich evolutionary lineage. As a result, cross-species mapping of brain organization plays a critical role in advancing translational neuroscience and clinical applications. This presentation will introduce comparative alignment models for humans, nonhuman primates (NHPs), and rodents, elucidating conserved and divergent brain regions and networks across different species. We will also highlight the utility of alignment models in facilitating cross-species comparisons across modalities. Additionally, by leveraging multiple NHP resources, we will characterize brain development in nonhuman primates, unraveling shared and unique features that contribute to human brain development and cognition. 

While the hippocampus is key for uniquely human cognitive abilities, it is also a phylogenetically old cortex and paradoxically considered evolutionarily preserved. Here, we introduce a comparative framework to quantify the preservation and reconfiguration of hippocampal organisation in primate evolution, by analysing the hippocampus as an unfolded cortical surface that is geometrically matched across species. Our findings revealed an overall conservation of hippocampal macro- and micro-structure, showing anterior-posterior and, perpendicularly, subfield-related organisational axes in both humans and macaques. However, while functional organisation in both species also followed an anterior-posterior axis, the latter showed a marked evolutionary reconfiguration, which mirrors a rudimentary integration of the default-mode-network in non-human primates. Our findings suggest that microstructurally preserved regions like the hippocampus may still undergo functional reconfiguration in primate evolution, due to their embedding in heteromodal association networks. 

Brain development is driven by numerous physiological processes, such as cell migration and neuronal differentiation, which ultimately shape the cellular, anatomical, and functional properties of the brain. Classically, spatial variations in these properties are delineated using discrete boundaries to subdivide anatomically and/or functionally homogeneous cortical and subcortical areas. However, there is no consensus to date as to which specific property should be prioritized in defining these regional boundaries, and the reliance on largely descriptive approaches has resulted in a plethora of different brain parcellations. In this talk, I will describe a new unified geometric-based approach that uses brain geometry to define regions in both the cortex and subcortex of human and various non-human mammalian species. I will show that the resulting geometric parcellations produce regions that are more homogeneous than most existing parcellations in terms of capturing diverse anatomical, functional, cellular, and molecular brain properties, and that the approach can easily be generalized to other mammalian species (e.g., primates, rodents, rabbits, treeshrews) for which no parcellations exist. Finally, I will show that the geometric approach underpinning this parcellation is tied to a generative reaction-diffusion mechanism that describes how the concentration of chemicals (e.g., morphogens) diffuses in space to enable the formation of patterns that shape regional organization.