Scaling Principles of White Matter Connectivity in the Human and Nonhuman Primate Brain

Abstract

Brains come in many shapes and sizes. Nature has endowed big-brained primate species like humans with a proportionally large cerebral cortex. Comparative studies have suggested, however, that the total volume allocated to white matter connectivity—the brain’s infrastructure for long-range interregional communication—does not keep pace with the cortex. We investigated the consequences of this allometric scaling on brain connectivity and network organization. We collated structural and diffusion magnetic resonance imaging data across 14 primate species, describing a comprehensive 350-fold range in brain size across species. We show volumetric scaling relationships that indeed point toward a restriction of macroscale connectivity in bigger brains. We report cortical surface area to outpace white matter volume, with larger brains showing lower levels of overall connectedness particularly through sparser long-range connectivity. We show that these constraints on white matter connectivity are associated with longer communication paths, higher local network clustering, and higher levels of asymmetry in connectivity patterns between homologous areas across the left and right hemispheres. Our findings reveal conserved scaling relationships of major brain components and show consequences for macroscale brain circuitry, providing insights into the connectome architecture that could be expected in larger brains such as the human brain.

The evolution and biological correlates of hand preferences in anthropoid primates

“…Surprisingly, we also did not recover notable influences of absolute brain size on hand preferences. An effect on lateralization strength was expected both on theoretical considerations ( Ringo et al, 1994 ) and empirical evidence from studies investigating intra- and interspecific covariation of brain size and overall cortical lateralization ( Kong et al, 2018 ; Ardesch et al, 2021 ). Why do anthropoid hand preferences not conform to these predictions?…”

“…By now, this idea has also been extended to non-human primates that habitually use tools ( Cashmore et al, 2008 ; Prieur et al, 2019 ). Moreover, neuroanatomical studies demonstrated that the expression of overall neural lateralization and hemispheric independence positively correlates with absolute brain size in primates ( Rilling and Insel, 1999 ; Karolis et al, 2019 ; Ardesch et al, 2021 ). Such a scaling relation was already hypothesized by Ringo et al, 1994 , and implies that the strength of individual handedness could also be tied to absolute brain size ( Hopkins, 2013a ; the concept does, however, not concern the direction of hand preferences).…”

A connectomics-based taxonomy of mammals

“…For example, species with fewer commissural inter-hemispheric connections exhibit lower hemispheric mean-shortest-path (i.e., stronger intra-hemispheric connectivity), suggesting a similar connectivity conservation principle [3]. Likewise, using diffusion-weighted MRI data across 14 different primate species, another study reported negative allometric scaling of cortical surface area with white matter volume and corpus callosum cross-sectional area [2]. This scaling results in less space for white matter connectivity with increasing brain size, translating into larger brains with a relatively higher proportion of shortrange connections than long-range connections when compared with smaller brains [2].…”

“…Likewise, using diffusion-weighted MRI data across 14 different primate species, another study reported negative allometric scaling of cortical surface area with white matter volume and corpus callosum cross-sectional area [2]. This scaling results in less space for white matter connectivity with increasing brain size, translating into larger brains with a relatively higher proportion of shortrange connections than long-range connections when compared with smaller brains [2]. Collectively these studies highlight that the architecture of neural circuits and their physical embedding are intertwined, and the distribution of connections is such that it retains consistent global architectural features across phylogeny.…”

The evolution and biological correlates of hand preferences in anthropoid primates

“…In addition to these considerations, it has been prominently proposed that foraging-related extractive tool use facilitated the evolution of hand preferences in humans to allow for more efficient object handling (Kimura, 1979;Frost, 1980), but this idea has also been extended to nonhuman primates that habitually use tools (Cashmore et al, 2008;Prieur et al, 2019). Moreover, neuroanatomical studies demonstrated that the expression of overall neural lateralization and hemispheric independence positively correlates with absolute brain size in primates (Rilling & Insel, 1999;Karolis et al, 2019;Ardesch et al, 2021). Such a scaling relation was already hypothesized by Ringo et al (1994) and implies that the strength of individual handedness could also be tied to absolute brain size (Hopkins, 2013b); the concept does, however, not concern the direction of hand preferences.…”