Sulcal organization in the medial frontal cortex provides insights into primate brain evolution

Abstract

Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of the human uniqueness, if any, and between-species anatomo-functional comparisons of the frontal areas remain controversial. To provide a novel interpretation of the evolution of primate brains, sulcal morphological variability of the medial frontal cortex was assessed in Old World monkeys (macaque/baboon) and Hominoidea (chimpanzee/human). We show that both Hominoidea possess a paracingulate sulcus, which was previously thought to be unique to the human brain and linked to higher cognitive functions, such as mentalizing. Also, we show systematic sulcal morphological organization of the medial frontal cortex that can be traced from Old World monkeys to Hominoidea species, demonstrating an evolutionarily conserved organizational principle. These data provide a new framework to compare sulcal morphology, cytoarchitectonic areal distribution, connectivity, and function across the primate order, leading to clear predictions about how other primate brains might be anatomo-functionally organized.

Fig. 1

Presence of the paracingulate sulcus (PCGS) across primates. The location of the cingulate sulcus (CGS) is shown in red in typical hemispheres displaying no PCGS and in those displaying a PCGS in human (a) and chimpanzee (b), as well as in typical hemispheres of baboon (c) and macaque (d) brains. The location of the PCGS is shown in yellow in typical hemispheres displaying a PCGS in the human (a) and chimpanzee brains (b). A PCGS is observed in both human and chimpanzee brains, but not in baboon and macaque brains (e). The probability of occurrence of a PCGS decreased from Human to chimpanzee. The PCGS is lateralized in the left hemisphere in human, but not in chimpanzee brains. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. Source data are provided as a Source Data file

Fig. 2

Presence of the ILS across primates. The location of the ILS is shown in yellow in typical hemispheres of the human, chimpanzee, baboon, and macaque monkey brains (right panels). a The probability of occurrence of an ILS is higher in human compared with non-human primate brains. A post-hoc Tukey test indicated no significant difference in the presence of the ILS in the three non-human primate species. Only in chimpanzee brains, the probability of observing an ILS is higher in the left than in the right hemisphere. No difference between the probability of occurrence of ILS in the left versus right hemisphere was found in human, baboon, and macaque brains. b In Hominoidea, when a PCGS is present, the ILS is almost always absent. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. Source data are provided as a Source Data file

Fig. 3

Location of vertical sulci in the dorsal MFC across primates. a Schematic representation of the location of the various sulci in the respective standard space of each primate species. The scale represents the antero-posterior level (in mm) in each brain. Fixed anatomical landmarks across primates are displayed: the rostral limit of the pons (landmark 1, in yellow), the anterior commissure (landmark 2, in red), the caudal limit of the genu of the corpus callosum (landmark 3, in light blue), and the rostral limit of the genu of the corpus callosum (landmark 4, in dark blue). b Density of the difference between the Y coordinates of PACS and of the anatomical landmark 1 in human, chimpanzee, baboon, and macaque (from top to bottom panels). This difference was normalized in relation to the brain size (total antero-posterior extent). The 0 value corresponds to the Y level of the anatomical landmark 1 in standard brains. c Density of the normalized difference between the Y coordinates of PRPACS and of the anatomical landmark 2. The 0 value corresponds to the Y level of the anatomical landmark 2 in standard brains. d Density of the normalized difference between the Y coordinates of VPCGS-P and of the anatomical landmark 3. The 0 value corresponds to the Y level of the anatomical landmark 3 in standard brains. e Density of the normalized difference between the Y coordinates of VPCGS-A and of the anatomical landmark 4. The 0 value corresponds to the Y level of the anatomical landmark 4 in standard brains. Source data are provided as a Source Data file

Fig. 4

Presence of vertical sulci in the dorsomedial frontal cortex across primates. Probability of occurrence (±s.e.m.) of the paracentral sulcus (PACS, a), the pre-paracentral sulcus (PRPACS, b), the posterior (VPCGS-P, c) and the anterior (VPCGS-A, d) vertical paracingulate sulci in the four species. a PACS. Left panel: The probability of observing a PACS decreases from human, chimpanzee, baboon, to macaque. Posthoc analysis showed that the presence of PACS was higher in Hominoidea (human and chimpanzee) than in Old-world monkeys (baboon and macaque), but that it was similar between human and chimpanzees and also between baboon and macaque. Right panel: PACS characteristics vary across primates: it is a sulcus (blue) in 100% of hemispheres in Hominoidea, it is a spur (green) or a dimple (pink) in Old-world monkeys. It is more frequently a spur than a dimple in baboon, as opposed to macaque. b PRPACS. Left panel: the probability of observing PACS is higher in Hominoidea than in Old-world monkeys but is similar between human and chimpanzee, on one hand, and between baboon and macaque on the other hand. Right panel: PRPACS characteristics vary across primates: it is a sulcus in 100% of hemispheres in Hominoidea, but it is a spur or a dimple in Old-world monkeys. It is more frequently a spur than a dimple in baboon, as opposed to macaque. c VPCGS-P. Left panel: the probability of observing VPCGS-P decreases from human, chimpanzee, baboon, to macaque. Posthoc analysis demonstrated that the presence of the VPCGS-P was higher in human than in non-human primates. Its probability of occurrence was also higher in chimpanzee than in Old-world monkeys. It was, however, similar between macaque and baboon. Right panel: VPCGS-P characteristics vary across primates: it is a sulcus in 100% of hemispheres in Hominoidea, but it is a spur or a dimple in baboon and only a dimple in Macaque. d VPCGS-A. Left panel: The probability of occurrence of VPCGS-A decreases from human, chimpanzee, baboon, to macaque. Right panel: VPCGS-P characteristics vary across primates: it is a sulcus in 100% of hemispheres in Hominoidea, but it is more frequently a spur than a dimple in baboon, as compared with macaque. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. Source data are provided as a Source Data file

Fig. 5

Morphological characteristics of the junction between the dorsal and ventral MFC. a Rostral end of the CGS/PCGS. In human. The rostral end of CGS is characterized by two sulci forming a fork pointing downward: SU-ROS, pointing downward, and SOS, pointing upward. In chimpanzee. The fork formed by the precursors of SU-ROS and SOS, i.e., CGS-VE and CGS-DE, respectively, is also pointing as in the human brain in the majority of hemispheres. In 17.5% of hemispheres, the fork is forward facing (purple area), and is incomplete (green area) (i.e., SOS is present but SU-ROS is absent) in 1.25% of hemispheres. In baboon. The fork formed by CGS-VE and CGS-DE is also pointing downward in the majority of hemispheres but to a lesser extent than in Hominoidea. In 25% of hemispheres, the fork is forward facing, it is incomplete in 28.75% of hemispheres, and is absent in 6.25% of hemispheres. In macaque. The fork formed by CGS-VE and CGS-DE is displaying the same patterns as in the baboon but in different proportions: the most frequent pattern observed is a fork facing forward, followed by a fork pointing downward. The fork is incomplete in 13.75% of hemispheres and is absent in 17.5% of hemispheres. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. b Location of the SU-ROS/SOS and CGS-DE/CGS-VE intersection. The top diagram shows the location of the intersection between SU-ROS/SOS and CGS-VE/CGS-DE in a typical hemisphere of a chimpanzee. The ΔZ corresponds to the difference between the dorsoventral Z coordinates where the intersection is observed and the dorsoventral Z coordinates where the rostral limit of the genu of the corpus callosum (represented by a purple cross) is located. ΔZ was then normalized for brain size to compare across primate brains. Boxplots displaying the mean (±s.e.m.) normalized ΔZ across individuals are presented in the bottom diagram. Note that black dots represent outliers and horizontal lines the mean of each distribution. c Probability of occurrence (±s.e.m.) of RP-PCGS. The RP-PCGS is human-specific since it is not present in non-human primates. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. Source data are provided as a Source Data file

Fig. 6

Sulci present in the ventral MFC across primates. The location of the ROS-S, ROS-I, and ASOS sulci are displayed in human, chimpanzee, baboon, and macaque brains in the right panels. a The probability of occurrence (±s.e.m.) of ROS-S is similar in human and non-human primates. b The probability of occurrence (±s.e.m.) of ROS-I is comparable in human and chimpanzee and is almost absent in Old-world monkeys. c The probability of occurrence of ASOS is equal in human and chimpanzee. It is decreased in Old-world monkeys but equally present in baboon and macaque. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. Source data are provided as a Source Data file

Fig. 7

Probability of occurrence of DMPS and VMPS across primates. The location of the DMPS and VMPS sulci are displayed in human and chimpanzee brains in the right panels. The probability of occurrence of both DMPS (a) and VMPS (b) is higher in human than in chimpanzee but is very low in Old-world monkeys. Statistics: *p < 0.05, **p < 0.01, ***p < 0.001, ns non-significant. Source data are provided as a Source Data file

Fig. 8

Summary of sulcal changes occurring from macaque to human. Schematic sulcal organization of the MFC in each species is represented in their respective stereotaxic space. Main changes from one species to another are indicated. The ΔZ corresponds to the difference between the dorso-ventral Z coordinates where the intersection is observed and the dorso-ventral Z coordinates where the rostral limit of the genu of the corpus callosum is located. The difference ΔZ is decreased in the human compared to non-human primates, showing that the intersection between the CGS with the SU-ROS/CGS-VE and with the supra-orbital sulcus SOS/CGS-DE is pushed down from non-human to human primates