Arun SP

Timothy Behrens

eLife assessment
This valuable study correlates the size of various prefrontal brain regions in primate species with socioecological variables like foraging distance and population density. The evidence presented is solid but needs to be strengthened with additional analyses that demonstrate the robustness of their results. It is also unclear how this approach would work in other species that show variation in socioecological variables despite lacking clear anatomical markers to define brain areas.

anonymous

Reviewer #1 (Public Review):
The present study provides a phylogenetic analysis of the size prefrontal areas in primates, aiming to investigate whether relative size of the rostral prefrontal cortex (frontal pole) and dorsolateral prefrontal cortex volume vary according to known ecological or social variables.
I am very much in favor of the general approach taken in this study. Neuroimaging now allows us to obtain more detailed anatomical data in a much larger range of species than ever before and this study shows the questions that can be asked using these types of data. In general, the study is conducted with care, focusing on anatomical precision in definition of the cortical areas and using appropriate statistical techniques, such as PGLS.
I have read the revised version of the manuscript with interest. I agree with the authors that a focus on ecological vs laboratory variables is a good one, although it might have been useful to reflect that in the title.
I am happy to see that the authors included additional analyses using different definitions of FP and DLPFC in the supplementary material. As I said in my earlier review, the precise delineation of the areas will always be an issue of debate in studies like this, so showing the effects of different decisions in vital.
I am sorry the authors are so dismissive of the idea of looking the models where brain size and area size are directly compared in the model, rather preferring to run separate models on brain size and area size. This seems to me a sensible suggestion.
Similarly, the debate about whether area volume and number of neurons can be equated across the regions is an important one, of which they are a bit dismissive.
Nevertheless, I think this is an important study. I am happy that we are using imaging data to answer more wider phylogenetic questions. Combining detailed anatomy, big data, and phylogenetic statistical frameworks is a important approach.

Reviewer #2 (Public Review):
In the manuscript entitled "Linking the evolution of two prefrontal brain regions to social and foraging challenges in primates" the authors measure the volume of the frontal pole (FP, related to metacognition) and the dorsolateral prefrontal cortex (DLPFC, related to working memory) in 16 primate species to evaluate the influence of socio-ecological factors on the size of these cortical regions. The authors select 11 socio-ecological variables and use a phylogenetic generalized least squares (PGLS) approach to evaluate the joint influence of these socio-ecological variables on the neuro-anatomical variability of FP and DLPFC across the 16 selected primate species; in this way, the authors take into account the phylogenetic relations across primate species in their attempt to discover the the influence of socio-ecological variables on FP and DLPF evolution.
The authors run their studies on brains collected from 1920 to 1970 and preserved in formalin solution. Also, they obtained data from the Mussée National d´Histoire Naturelle in Paris and from the Allen Brain Institute in California. The main findings consist in showing that the volume of the FP, the DLPFC, and the Rest of the Brain (ROB) across the 16 selected primate species is related to three socio-ecological variables: body mass, daily traveled distance, and population density. The authors conclude that metacognition and working memory are critical for foraging in primates and that FP volume is more sensitive to social constraints than DLPFC volume.
The topic addressed in the present manuscript is relevant for understanding human brain evolution from the point of view of primate research, which, unfortunately, is a shrinking field in neuroscience. But the experimental design has two major weak points: the absence of lissencephalic primates among the selected species and the delimitation of FP and DLPFC. Also, a general theoretical and experimental frame linking evolution (phylogeny) and development (ontogeny) is lacking.

Reviewer #3 (Public Review):
This is an interesting manuscript that addresses a longstanding debate in evolutionary biology - whether social or ecological factors are primarily responsible for the evolution of the large human brain. To address this, the authors examine the relationship between the size of two prefrontal regions involved in metacognition and working memory (DLPFC and FP) and socioecological variables across 16 primate species. I recommend major revisions to this manuscript due to: 1) a lack of clarity surrounding model construction; and 2) an inappropriate treatment of the relative importance of different predictors (due to a lack of scaling/normalization of predictor variables prior to analysis).

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

Figures and data

Boundaries of the dorso-lateral prefrontal cortex

Estimated coefficients of socio-ecological variables for the whole brain volume.

Estimated coefficients of socioecological variables for the Frontal Pole volume.

Estimated coefficients of socio-ecological variables for the DLPFC volume.

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