Scaling principles of white matter brain connectivity

Abstract

Brains come in many shapes and sizes. Nature has endowed big-brained primate species like humans with a proportionally large cerebral cortex. White matter connectivity - the brain's infrastructure for long-range communication - might not always scale at the same pace as the cortex. We investigated the consequences of this allometric scaling for white matter brain network connectivity. Structural T1 and diffusion MRI data were collated across fourteen primate species, describing a comprehensive 350-fold range in brain volume. We report volumetric scaling relationships that point towards a restriction in macroscale connectivity in larger brains. Building on previous findings, we show cortical surface to outpace white matter volume and the corpus callosum, suggesting the emergence of a white matter 'bottleneck' of lower levels of connectedness through the corpus callosum in larger brains. At the network level, we find a potential consequence of this bottleneck in shaping connectivity patterns, with homologous regions in the left and right hemisphere showing more divergent connectivity in larger brains. Our findings show conserved scaling relationships of major brain components and their consequence for macroscale brain circuitry, providing a comparative framework for expected connectivity architecture in larger brains such as the human brain.

Neuroplasticity and crossmodal connectivity in the normal, healthy brain.

“…The same study further demonstrated a more pronounced modular topology of the human connectome as compared to the chimpanzee connectome. Based on these findings the researchers suggested an evolutionary shift in the human brain toward investment of neural resources in multimodal connectivity facilitating neural integration, combined with an increase in language-related connectivity supporting functional specialization (Ardesch et al, 2019).…”

“…Further support for the above view comes from a very recent study by Ardesch et al (2019) who investigated adaptations of human brain connectivity by means of comparative connectomicsthe study of differences in the topological organization of connectomes (van den Heuvel et al, 2016). This study compared and contrasted humans and chimpanzees on shared connectivity in the primary, unimodal association, and multimodal association areas (Ardesch et al, 2019).…”

“…Further support for the above view comes from a very recent study by Ardesch et al (2019) who investigated adaptations of human brain connectivity by means of comparative connectomicsthe study of differences in the topological organization of connectomes (van den Heuvel et al, 2016). This study compared and contrasted humans and chimpanzees on shared connectivity in the primary, unimodal association, and multimodal association areas (Ardesch et al, 2019). The study demonstrated that the network centrality of shared connections linking bilateral primary areas was lower in humans than chimpanzees, whereas the shared connections linking bilateral multimodal association areas were more central in humans as compared to chimpanzees.…”

“…In comparative neuroscience, evolution-driven functional reorganization has been studied using both cortical surface expansion model and interspecies activity correlation model as well (Ardesch et al, 2019;Mantini et al, 2012;Orban et al, 2004). Research using a cortical surface expansion model interprets comparative fMRI data for monkey and human relying on spatial assumptions related to cortical expansion during evolution (Orban et al, 2004;Schira et al, 2012).…”

“…Of particular concern here is to clarify the controversy of the role of cortical expansion in driving adaptation or reorganization in the human connectome, a map of neural network in the brain (Ardesch et al, 2019;van den Heuvel et al, 2016). A recent review has suggested that cortical expansion plays an important role in the evolvement of temporoparietal junction and posterior STS in humans (Patel et al, 2019).…”