Using Tertiary Sulci to Map the “Cognitive Globe” of Prefrontal Cortex

Abstract

Stuss considered the human prefrontal cortex (pFC) as a “cognitive globe” [Stuss, D. T., & Benson, D. F. Neuropsychological studies of the frontal lobes. Psychological Bulletin, 95, 3–28, 1984] on which functions of the frontal lobe could be mapped. Here, we discuss classic and recent findings regarding the evolution, development, function, and cognitive role of shallow indentations or tertiary sulci in pFC, with the goal of using tertiary sulci to map the “cognitive globe” of pFC. First, we discuss lateral pFC (LPFC) tertiary sulci in classical anatomy and modern neuroimaging, as well as their development, with a focus on those within the middle frontal gyrus. Second, we discuss tertiary sulci in comparative neuroanatomy, focusing on primates. Third, we summarize recent findings showing the utility of tertiary sulci for understanding structural–functional relationships with functional network insights in ventromedial pFC and LPFC. Fourth, we revisit and update unresolved theoretical perspectives considered by C. Vogt and O. Vogt (Allgemeinere ergebnisse unserer hirnforschung. Journal für Psychologie und Neurologie, 25, 279–462, 1919) and F. Sanides (Structure and function of the human frontal lobe. Neuropsychologia, 2, 209–219, 1964) that tertiary sulci serve as landmarks for cortical gradients. Together, the consideration of these classic and recent findings indicate that tertiary sulci are situated in a unique position within the complexity of the “cognitive globe” of pFC: They are the smallest and shallowest of sulci in pFC, yet can offer insights that bridge spatial scales (microns to networks), modalities (functional connectivity to behavior), and species. As such, the map of tertiary sulci within each individual participant serves as a coordinate system specific to that individual on which functions may be further mapped. We conclude with new theoretical and methodological questions that, if answered in future research, will likely lead to mechanistic insight regarding the structure and function of human LPFC.

Sulcal variability in anterior lateral prefrontal cortex contributes to variability in reasoning performance among young adults

“…There was no hemispheric asymmetry in incidence rates ( p = 0.66; figure 1 ), and when only one pimfs component was present, it was equally likely to be a dorsal or ventral component (χ 2 < 2, p > .15 in both hemispheres; figure 1 ). These incidence rates were similar to those observed in children and adolescents [24], which was anticipated given that sulci are formed during gestation [3,12,55,65,66].…”

Cytoarchitecture, intersubject variability, and 3D mapping of four new areas of the human anterior prefrontal cortex

“…Recent segmentations propose subdivision of the mfs in posterior ( pmfs, posterior middle frontal ) and anterior ( imfs, intermediate frontal ) components (Petrides, 2019 ; Miller et al, 2021b ), whereas the latter ones consist of a horizontal ( imfs-h ) and vertical ( imfs-v ) part, synonymous with the fms , and consistent with the classical definition of mfs (Eberstaller, 1890 ). Moreover, Miller et al ( 2021a , b ) propose that these tertiary sulci may serve as landmarks in the prefrontal cortex, linking microstructure and functional features. This study supports the notion that cytoarchitectonic boundaries cannot be delineated based on anatomical landmarks exclusively (Amunts et al, 2004 ) due to high macroanatomical variance in the DLPFC and varying relationships of cortical areas concerning the sulcal patterns (see Figure 4 ).…”

“…Thus, previous cytoarchitectonic maps show considerable discrepancies in the location and distribution of DLPFC sub-areas and their relationship to sulci and gyri. Reasons may include differing and partly subjective criteria used to define and delineate subregions and the analysis of rather small samples in such time- and labor-intensive studies on microstructure, while differences in the sulcal pattern of the DLPFC are considerable (Ono et al, 1990 ; Miller et al, 2021a ). The DLPFC exhibits a high variability of sulci, i.e., the middle frontal sulcus ( mfs ), which divides the mfg into a dorsal and ventral part, existing only in 86% of human brains (Ono et al, 1990 ).…”

“…The DLPFC exhibits a high variability of sulci, i.e., the middle frontal sulcus ( mfs ), which divides the mfg into a dorsal and ventral part, existing only in 86% of human brains (Ono et al, 1990 ). Furthermore, individuals possessing an mfs to show remarkable variation in its structure, either as a large main furrow parallel to the superior and inferior frontal sulcus or as several irregular smaller (so-called tertiary) sulci (Vogt and Vogt, 1926 ; Huttner, 2004 ; Miller et al, 2021a ).…”

Two common and distinct forms of variation in human functional brain networks

“… 1 Network variant locations are present even after surface-based normalization procedures (Fischl, 2012; Klein et al, 2010; Van Essen, 2005) that align data across people by large-scale sulcal features; with individual differences in fcMRI not well related to variations in anatomical metrics ((Seitzman et al, 2019; Gordon et al, 2016) – although it is possible that they relate to finer-scale anatomical features, e.g., see (Miller et al, 2021)). This, together with correspondence to task responses, suggests that variants may relate more closely to differences in the functional positions of brain areas or systems, which can vary relative to anatomical landmarks (Frost & Goebel, 2012; Van Essen, Glasser, et al, 2012).…”