A revised perspective on the evolution of the lateral frontal cortex in primates

Abstract

Detailed neuroscientific data from macaque monkeys have been essential in advancing understanding of human frontal cortex function, particularly for regions of frontal cortex without homologs in other model species. However, precise transfer of this knowledge for direct use in human applications requires an understanding of monkey to hominid homologies, particularly whether and how sulci and cytoarchitectonic regions in the frontal cortex of macaques relate to those in hominids. We combine sulcal pattern analysis with resting-state functional magnetic resonance imaging and cytoarchitectonic analysis to show that old-world monkey brains have the same principles of organization as hominid brains, with the notable exception of sulci in the frontopolar cortex. This essential comparative framework provides insights into primate brain evolution and a key tool to drive translation from invasive research in monkeys to human applications.

Fig. 1.. Known and revised view of the sulcal organization in the lateral frontal cortex in human, chimpanzee, baboon, and macaque brains.

Known sulcal organization in the lateral frontal cortex of humans (A), chimpanzees (B), and macaques (C). (D) Revised view of the human homologs of the frontal cortical sulcal organization in the chimpanzee and old-world monkey brains. The color coding of the sulci in (D) corresponds to the sulci identified in the human brain. All sulci observed in the lateral frontal lobe of the human brain have clear homologs in chimpanzees, and only the sulci in the most anterior part of the frontopolar cortex do not have their homologs in old-world monkeys. fs and fi, superior and inferior frontal sulcus; prcs and ipcs, superior and inferior precentral sulcus; fm, middle frontal sulcus; fma, frontomarginal sulcus; SFS-P and SFS-A, posterior and anterior superior frontal sulcus; IFS, inferior frontal sulcus; SPR-S, superior precentral sulcus; IPRS-S, IPRS-P, and IPRS-I, superior, posterior, and inferior segments of the inferior precentral sulcus; PMFS-P, PMFS-I, and PMFS-A, posterior, intermediate, and anterior posteromedial frontal sulcus; IMFS-H and IMFS-V, horizontal and vertical rami of the intermediate frontal sulcus; PIMFS-D and PIMFS-V, dorsal and ventral paraintermediate frontal sulcus; cs, central sulcus. The dark gray sulci represent sulci that are located in the ventrolateral prefrontal cortex and are excluded from this analysis. The light gray sulci represent sulci that have not been named yet.

Fig. 2.. Hominid sulcal correspondence to the arcuate sulcus in old-world monkeys.

(A) Identification and location of the sulci forming the arcuate sulcus in old-world monkeys and their homologs in hominids. (B) Frequency of occurrence of IPRS-S and IPRS-P in brain hemispheres in all primates (top panels) and normalized distance between the anteroposterior (i) Y level of the caudal-most part of IPRS-S and Y level of the anterior commissure (AC) (light green) and (ii) Y level of the intersection between the caudal-most part of PMFS-P and Y level of the rostral limit of the optic chiasma (dark green) (bottom panel). (C) Frequency of occurrence of PMFS-P (top panel) and of hemispheres displaying a PMFS-P joining IPRS-S (middle panel) in all primates, as well as normalized distance between (i) the Y level of the caudal-most part of PMFS-P and the Y level of the rostral limit of the optic chiasma (blue) and (ii) Y level of the rostral-most part of PMFS-P and the Y level of the middle part of the genu of the corpus callosum (bottom panel). (D) Frequency of occurrence of IPRS-I and the various IPRS-I/IFS patterns in brain hemispheres in all primates (top panels) and normalized distance between the (i) Y level of the IPRS-I/IFS intersection and the Y level of the caudal part of the genu of the corpus callosum (pink) and (ii) Y level of the intersection between the rostral-most part of IFS and the Y level of the rostral limit of the genu of the corpus callosum (purple) (bottom panel). ns, nonsignificant. GLMM and/or Tukey post hoc tests at P < 0.05 (see Materials and Methods).

Fig. 3.. Hominid correspondence to the precentral dimples in old-world monkeys.

(A) Identification and location of the sulci forming the precentral dimples in old-world monkeys and their homologs in hominids. Frequency of occurrence of SPR-S (B) and SFS-P (C), and (D) of the various orientations of SPR-S (vertically or horizontally oriented to SFS-P or nonoriented dimple) in all primates. Whereas SPR-S is equally present in all species, SFS-P displays a decreased frequency of occurrence in macaques. The hominid-specific SPR-S vertical orientation can be observed in a few hemispheres in old-world monkeys. (E) Percentage of hemispheres in which SPR-S joins SFS-P. Whereas the SPR-S joins SFS-P in most of the hemispheres in hominids, it is rarely the case in old-world monkeys (F = 528.9, NumDF = 3, DenDF = 502.38, P < 2.2 × 10⁻¹⁶, GLMM). (F) Normalized distance between the (i) Y level of the caudal-most part of SPR-S and the Y level of the rostral limit of the mamillary bodies (blue) and (ii) Y level of the rostral-most part of SFS-P and the Y level of the caudal limit of the rostrum (red). GLMM and/or Tukey post hoc tests at P < 0.05 (see Materials and Methods).

Fig. 4.. Hominid correspondence to the principal sulcus in old-world monkeys.

(A) Identification and location of the sulci forming the principal sulcus in old-world monkeys and their homologs in hominids. Frequency of occurrence of PMFS-I (B), PMFS-A (C), and IMFS-H (D). (E) Percentage of hemispheres in which PMFS-I joins PMFS-A. (F) Percentage of hemispheres in which PMFS-A joins IMFS-H. (G) Normalized distance between the (i) Y level of the caudal-most part of PMFS-I and the Y level of the rostral limit of the caudal limit of the genu of the corpus callosum (dark orange), (ii) Y level of the caudal-most part of PMFS-A and the Y level of the rostral limit of the genu of the corpus callosum (light orange), and (iii) Y level of the caudal-most part of IMFS-H and the Y level of the intersection between the CGS, SUROS, and SOS (yellow). (H) Average silhouette score across the two hemispheres of the three macaques performing 12 rs-fMRI runs (see Materials and Methods). The best number of clusters is 3. (I) Probability maps of these three clusters (Post, Mid, and Ant) across 12 runs for each macaque (N, L, and C). The borders of the three functional clusters correspond to anatomical landmarks, strongly suggesting that the posterior (post), middle (mid), and anterior (ant) clusters correspond to, respectively, PMFS-I, PMFS-A, and IMFS-H. GLMM and/or Tukey post hoc tests at P < 0.05 (see Materials and Methods). LH, left hemisphere; RH, right hemisphere.

Fig. 5.. Hominid-specific sulci.

(A) Human correspondence of PIMFS-D, PIMFS-V, and IMFS-V in chimpanzees. (B) Frequency of occurrence of PIMFS-D is decreased in chimpanzees (F = 225.85, NumDF = 1, DenDF = 158, P < 2.2 × 10⁻¹⁶). (C) Frequency of occurrence of PIMFS-V is decreased in chimpanzees (F = 55.9, NumDF = 1, DenDF = 158, P < 4.9 × 10⁻¹², GLMM). (D) Frequency of occurrence of IMFS-V is equal in humans and chimpanzees (ns at P < 0.05, GLMM). (E) PIMFS-D joins more frequently IMFS-H in humans than in chimpanzees (F = 138.46, NumDF = 1, DenDF = 141.72, P < 2.2 × 10⁻¹⁶, GLMM). (F) PIMFS-D joins more frequently IMFS-V in chimpanzees and never in humans (F = 38.75, NumDF = 1, DenDF = 214, P < 2.51 × 10⁻⁹, GLMM). GLMM and/or Tukey post hoc tests at P < 0.05 (see Materials and Methods).