Imaging evolution of the primate brain: the next frontier?

Abstract

Evolution, as we currently understand it, strikes a delicate balance between animals' ancestral history and adaptations to their current niche. Similarities between species are generally considered inherited from a common ancestor whereas observed differences are considered as more recent evolution. Hence comparing species can provide insights into the evolutionary history. Comparative neuroimaging has recently emerged as a novel subdiscipline, which uses magnetic resonance imaging (MRI) to identify similarities and differences in brain structure and function across species. Whereas invasive histological and molecular techniques are superior in spatial resolution, they are laborious, post-mortem, and oftentimes limited to specific species. Neuroimaging, by comparison, has the advantages of being applicable across species and allows for fast, whole-brain, repeatable, and multi-modal measurements of the structure and function in living brains and post-mortem tissue. In this review, we summarise the current state of the art in comparative anatomy and function of the brain and gather together the main scientific questions to be explored in the future of the fascinating new field of brain evolution derived from comparative neuroimaging.

Fig. 1

Comparative anatomy as a glimpse at the evolution of species. a) First evolutionary tree (courtesy of © The Complete Work of Charles Darwin Online) as depicted in the 6th edition of the origin of species (Darwin 1859), b) Comparative anatomy of the skeletal structure whereby obvious similarities can be found between a sea lion and a cheetah, suggesting a close common ancestor (Rybczynski et al., 2009, picture taken at the Museum National D’Histoire Naturelle in Paris) c) Example of comparative genetics (limited to the Preferentially Expressed Antigen In Melanoma – PRAME – gene cluster) whereby the evolutionary tree combine within (i.e. interindividual variability in genetics) and between species (comparative genetics) differences (modified from Gibbs et al., 2007). Hue level differences have been coded so that it represents the level of difference with the original phylogenetic branch (in pink). New non-human variations have been coloured in black.

Fig. 2

Relative brain size cross-species comparison. a) 34 three-dimensional digital brain reconstructions from the brain catalogue (Heuer et al., 2019) b) Body size and weight comparison across apes c) Brain and body weight scatter plot comparison (Jerison 1975). Note that the red circle indicates human primates who deviate from the linear relationship existing between body and brain weight.

Fig. 3

Sulcal anatomy for inter-primate brain comparisons. a) Emergence of the para-cingulate sulcus (PCGS) the primate medial frontal cortex (Amiez et al., 2019 : non-existing in baboons and macaques, but sometimes present for great apes and humans. b) Sulcal landmarks in the primate medial frontal cortex (Amiez et al., 2019). c) Projection of human brain sulci (left) onto a rectangular sulcal model (top right). Correspondences are defined between the human rectangular cortical sulci model and its chimpanzee equivalent (bottom right). d) Application of the model correspondences to map a human surface-based brain atlas onto an individual chimpanzee surface (Coulon et al., 2018).

Fig 4

Brain connectivity cross-species comparison. a) Comparison between post-mortem axonal tracing in monkeys (cases 7&9 modified from Schmahmann and Pandya, 2006) and human in vivo spherical deconvolution tractography. Common anatomical features between human and monkey are reconstructed in red whereas anatomical differences have been coloured in blue (Thiebaut de Schotten et al., 2012) b) Flat maps of the human resting state functional connectivity without correspondence with the monkey (upper row) and its correspondence to cortical expansion maps (Mantini et al., 2013) c) Preliminary comparison of the principal gradient in humans and macaques (see Brain integration section of this paper for a definition of brain gradients ; Xu et al., 2019) d) The rich club organisation of the brain where regions in red are interconnected together and a hub for regions in blue (Bullmore and Sporns 2012).