Concurrent mapping of brain ontogeny and phylogeny within a common space: Standardized tractography and applications

Abstract

Developmental and evolutionary effects on brain organization are complex, yet linked, as evidenced by the correspondence in cortical area expansion across these vastly different time scales. However, it is still not possible to study concurrently the ontogeny and phylogeny of cortical areal connections, which is arguably more relevant to brain function than allometric measurements. Here, we propose a novel framework that allows the integration of structural connectivity maps from humans (adults and neonates) and nonhuman primates (macaques) onto a common space. We use white matter bundles to anchor the common space and use the uniqueness of cortical connection patterns to these bundles to probe area specialization. This enabled us to quantitatively study divergences and similarities in connectivity over evolutionary and developmental scales, to reveal brain maturation trajectories, including the effect of premature birth, and to translate cortical atlases between diverse brains. Our findings open new avenues for an integrative approach to imaging neuroanatomy.

The spatial extent of anatomical connections within the thalamus varies across the cortical hierarchy in humans and macaques

“…These data are publicly available through the PRIMatE Data Exchange (PRIME-DE) repository (http://fcon_1000.projects.nitrc.org/indi/PRIME/oxford2.html) (123). Nonlinear surface transformation to macaque F99 standard space was performed, as described elsewhere (124, 125). Subcortical structures were registered to F99 standard space using FNIRT and templates from the HCP Non-Human Primate Minimal Preprocessing Pipelines (47, 70).…”

Comparing the limbic-frontal connectome across the primate order: conservation of connections and implications for translational neuroscience

“…This has been shown to be a particularly reliable way of comparing aspects of white matter architecture across species, as it allows identification of anatomically similar structures across species 28 and, unlike inferences regarding the connectivity of specific grey matter areas, is not susceptible to false positives 86 . This approach is therefore the basis of tools for comparing white matter architecture across species, development, and individuals 87,88 . However, this does mean we do make claims on the precise grey matter areas innervated by these bundles.…”

Connectome topology of mammalian brains and its relationship to taxonomy and phylogeny

“…Although a brain network modeling approach is seemingly preferable for these comparisons, there remain notable limitations. Establishing regional neural correspondence across species and evolutionary branching is a longstanding research question ( Krubitzer, 2009 ; Kaas, 2011 ; Faunes et al, 2015 ), with new methods emerging to identify homologies by computationally matching anatomical patterns or fingerprints ( Mars et al, 2018 ; Balsters et al, 2020 ; Schaeffer et al, 2020 ; Warrington et al, 2022 ). In the future, major progress will come from the creation of a universal (pan-mammalian) parcellation or atlas covering the entire cerebral cortex, and ideally extending to subcortical regions as well, a challenge that was first anticipated and initiated by Swanson and Bota (2010) .…”