Linking the evolution of two prefrontal brain regions to social and foraging challenges in primates.

The diversity of cognitive skills across primates remains both a fascinating and a controversial issue. Recent comparative studies provided conflicting results regarding the contribution of social vs ecological constraints to the evolution of cognition. Here, we used an interdisciplinary approach combining comparative cognitive neurosciences and behavioral ecology. Using brain imaging data from 16 primate species, we measured the size of two prefrontal brain regions, the frontal pole (FP) and the dorso-lateral prefrontal cortex (DLPFC), respectively, involved in metacognition and working memory, and examined their relation to a combination of socio-ecological variables. The size of these prefrontal regions, as well as the whole brain, was best explained by three variables: body mass, daily traveled distance (an index of ecological constraints), and population density (an index of social constraints). The strong influence of ecological constraints on FP and DLPFC volumes suggests that both metacognition and working memory are critical for foraging in primates. Interestingly, FP volume was much more sensitive to social constraints than DLPFC volume, in line with laboratory studies showing an implication of FP in complex social interactions. Thus, our data highlights the relative weight of social vs ecological constraints on the evolution of specific prefrontal brain regions and their associated cognitive operations in primates. Primates – such as lemurs, monkeys and humans – can perform a diverse range of cognitive skills, from memory to processing speech. But how did this diversity of cognitive skills evolve? To answer this question, scientists often compare the brain sizes of different species and measure how this relates to their social behaviors or ecology in the wild. But using the whole brain as a measure of global cognitive capacities seems crude in the light of modern cognitive neuroscience studies, which have shown that specific parts of the brain are responsible for certain cognitive skills. It is unclear how relevant the findings of cognitive neuroscience studies, which test animals in a laboratory, are to real life situations and evolution. To address this gap, Bouret et al. integrated methods from both behavioral ecology and cognitive neuroscience to examine the size of primate brain regions. The team studied brain images from 16 primate species, focusing on two regions that have been linked to specific cognitive functions in laboratory experiments. They examined the frontal pole, which is involved in metacognition (the ability to be aware of and assess one’s own thoughts), and the dorsolateral prefrontal cortex, which is involved in working memory (the ability to temporarily store information to solve a problem). Bouret et al. then compared the size of these regions to socio-ecological factors: how much each species performs complex social interactions and how hard it is to find food in the wild, by measuring their population density and daily travel distance, respectively. This revealed that the volume of the frontal pole is larger in species that experience more complex social interactions and in species that struggle to find food – two tasks thought to require metacognition. The dorsolateral prefrontal cortex, however, is only larger in species that have difficulty foraging, which might require a strong working memory to plan travel routes. These findings suggest that laboratory experiments linking cognitive skills to specific parts of the brain are reliable enough to predict the size of these regions across wild primates. The work of Bouret et al. also helps bridge the gap between cognitive neuroscience and behavioral ecology, and demonstrates how these two disciplines can be combined to investigate the evolution of cognition.

Informations de copyright

© 2023, Bouret et al.

Déclaration de conflit d'intérêts

SB, EP, SP, LC, PP, EG, CG No competing interests declared