High-Expanding Regions in Primate Cortical Brain Evolution Support Supramodal Cognitive Flexibility

Abstract

Primate cortical evolution has been characterized by massive and disproportionate expansion of a set of specific regions in the neocortex. The associated increase in neocortical neurons comes with a high metabolic cost, thus the functions served by these regions must have conferred significant evolutionary advantage. In the present series of analyses, we show that evolutionary high-expanding cortex – as estimated from patterns of surface growth from several primate species – shares functional connections with different brain networks in a context-dependent manner. Specifically, we demonstrate that high-expanding cortex is characterized by high internetwork functional connectivity; is recruited flexibly over many different cognitive tasks; and changes its functional coupling pattern between rest and a multimodal task-state. The capacity of high-expanding cortex to connect flexibly with various specialized brain networks depending on particular cognitive requirements suggests that its selective growth and sustainment in evolution may have been linked to an involvement in supramodal cognition. In accordance with an evolutionary-developmental view, we find that this observed ability of high-expanding regions – to flexibly modulate functional connections as a function of cognitive state – emerges gradually through childhood, with a prolonged developmental trajectory plateauing in young adulthood.

Cross-species Functional Alignment Reveals Evolutionary Hierarchy Within the Connectome

“…Within the DMN those regions with low FHI are the same regions that in humans contain the most information about global brain dynamics. Together these results are consistent with a complex view of cross species differentiation which impacts on cortical modules at both a local and global scale 17,66,68,71,72 .…”

The functional foundations of episodic memory remain stable throughout the lifespan

“…These three measures reflect different fundamental aspects of brain organization in which higher values reflect diminished constraints of sensory and structural input and increased capacity to support a wider array of different tasks such as higher-order cognition (4,28,29). Fig.…”

“…Over the last few years, research has demonstrated that the structural foundations of general cognitive abilities are largely constant throughout life (1, 2), being embedded into fundamental aspects of brain organization as captured by evolutionary expansion patterns or connectivity gradients (3,4). However, it is unknown whether the functional foundations supporting specific forms of cognition are equally stable or rather dynamic through life.…”

“…Note that activity (y-axis) values are derived from a PCA (within cluster), and thus demeaned. For clusters[3][4][5], higher values represent stronger positive memory effects (seeFig. 2).…”

Kaleidoscope

“…Sneve et al discuss the beneficiary cognitive gains the 'massive and disproportionate expansion' of parts of the neocortex conferred upon ussupporting selective brain growththrough cross comparison of histological and neuroimaging data from several primate species, including sapiens. 5 High-expanding cortical regionsnotably the lateral temporal, parietal and prefrontal corticesare characterised by significant internetwork connectivity and flexible recruitment across a range of different cognitive tasks. The authors propose that it is the sheer flexibility of these expanding cortical 'hotspots' to connect with and integrate multiple different brain regions depending on cognitive and emotional needssupramodal cognitionthat sustained and supported their evolutionary selection over the ages.…”