A comprehensive analysis of variability in the sulci that define the inferior frontal gyrus in the chimpanzee (Pan troglodytes) brain

Abstract

Objectives In the human brain, the inferior frontal gyrus (IFG) is comprised of three morphological regions, which include the pars opercularis, pars triangularis, and pars orbitalis. These brains regions are implicated in a number of cognitive and linguistic functions, and the pars opercularis and pars triangularis of the language dominant hemisphere are collectively referred to as Broca's area. Evolution of the morphology of the IFG has been a topic of study in comparative neuroscience. Materials and Methods Using magnetic resonance images (MRI) from 294 chimpanzees with known pedigrees, we quantified the folding patterns, surface area, and depth of three sulci and their subdivisions that define the IFG. Results Chimpanzees show considerable individual variation in IFG sulci. A higher proportion of males and chimpanzees with better orofacial motor control had a bifurcation in the dorsal limb of the fronto‐orbital sulcus. For surface area and depth, chimpanzees with better orofacial motor control had greater leftward asymmetries in surface area and increased gyrification for the fronto‐orbital sulcus and greater rightward biases for the inferior precentral sulcus. Quantitative genetic analyses revealed that the average surface area and depth for three of the five sulci subdivisions were significantly heritable. By contrast, we found no evidence for heritability in asymmetries for any of the sulci. Discussion These findings provide context to understanding evolutionary selection for increasing motor, cognitive and linguistic functions among primates, and contribute an essential comparative framework for interpreting IFG evolution in the human lineage.

Sulcal morphology of posteromedial cortex substantially differs between humans and chimpanzees

“…Recent work shows that sulcal morphology relates to the appearance of complex behaviors in non-human hominoids 19,35,78,79 . For example, asymmetries in the depth of multiple sulci 19,35,78 , as well as the presence of the paracingulate sulcus 35 and dorsal fronto-orbital sulcus pattern 19 , relates to the production and use of attention-getting sounds by . CC-BY-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.…”

“…The present findings also lay the foundation to examine the cognitive and functional role of PMC sulci in species beyond humans. Recent work shows that sulcal morphology relates to the appearance of complex behaviors in non-human hominoids 19,35,78,79 . For example, asymmetries in the depth of multiple sulci 19,35,78 , as well as the presence of the paracingulate sulcus 35 and dorsal fronto-orbital sulcus pattern 19 , relates to the production and use of attention-getting sounds by chimpanzees.…”

“…Recent work shows that sulcal morphology relates to the appearance of complex behaviors in non-human hominoids 19,35,78,79 . For example, asymmetries in the depth of multiple sulci 19,35,78 , as well as the presence of the paracingulate sulcus 35 and dorsal fronto-orbital sulcus pattern 19 , relates to the production and use of attention-getting sounds by chimpanzees. Further, asymmetries in the depth of the inferior arcuate sulcus was related to gestural communication in baboons 79 , as was the presence of the intralimbic sulcus in chimpanzees 35 .…”

“…For example, while mice and marmosets have rather smooth, lissencephalic cerebral cortices, 60-70% of the cerebral cortex in hominoids is buried within sulci 3,22 . Intriguingly, recent studies have identified "evolutionarily new" shallow sulci in association cortices in hominoid brains that have been linked to functional organization across a broad array of cognitive domains (e.g., 14,19,[23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38] ), several of which reflect cognitive abilities that are arguably unique to humans. Building on this previous work, we compared the sulcal patterning of the posteromedial cortex (PMC) -a region on the medial cortical surface that includes the posterior cingulate, retrosplenial, and precuneal cortices 39 between humans and chimpanzees with a particular emphasis on the smaller, shallower, and relatively overlooked "evolutionarily new" cortical indentations.…”

“…A fundamental question in comparative biology and systems neuroscience is: What features of the brain are unique to humans? Key insights regarding what features of the brain are unique to humans have been gleaned from studies comparing anatomical and functional features of the human brain to features from the brains of our close evolutionary relative, the chimpanzee [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20] . Of all the features to study, researchers particularly focus on the folds of the cerebral cortex, or sulci, as they generally track with evolutionary complexity 21 .…”