Development of Human Lateral Prefrontal Sulcal Morphology and Its Relation to Reasoning Performance

Abstract

Previous findings show that the morphology of folds (sulci) of the human cerebral cortex flatten during postnatal development. However, previous studies did not consider the relationship between sulcal morphology and cognitive development in individual participants. Here, we fill this gap in knowledge by leveraging cross-sectional morphological neuroimaging data in the lateral prefrontal cortex (LPFC) from individual human participants (6-36 years old, males and females; N = 108; 3672 sulci), as well as longitudinal morphological and behavioral data from a subset of child and adolescent participants scanned at two timepoints (6-18 years old; N = 44; 2992 sulci). Manually defining thousands of sulci revealed that LPFC sulcal morphology (depth, surface area, and gray matter thickness) differed between children (6-11 years old)/adolescents (11-18 years old) and young adults (22-36 years old) cross-sectionally, but only cortical thickness showed differences across childhood and adolescence and presented longitudinal changes during childhood and adolescence. Furthermore, a data-driven approach relating morphology and cognition identified that longitudinal changes in cortical thickness of four left-hemisphere LPFC sulci predicted longitudinal changes in reasoning performance, a higher-level cognitive ability that relies on LPFC. Contrary to previous findings, these results suggest that sulci may flatten either after this time frame or over a longer longitudinal period of time than previously presented. Crucially, these results also suggest that longitudinal changes in the cortex within specific LPFC sulci are behaviorally meaningful, providing targeted structures, and areas of the cortex, for future neuroimaging studies examining the development of cognitive abilities.Significance StatementRecent work has shown that individual differences in neuroanatomical structures (indentations, or sulci) within the lateral prefrontal cortex (LPFC) are behaviorally meaningful during childhood and adolescence. Here, we describe how specific LPFC sulci develop at the level of individual participants for the first time—from both cross-sectional and longitudinal perspectives. Further, we show, also for the first time, that the longitudinal morphological changes in these structures are behaviorally relevant. These findings lay the foundation for a future avenue to precisely study the development of the cortex and highlight the importance of studying the development of sulci in other cortical expanses and charting how these changes relate to the cognitive abilities those areas support at the level of individual participants.

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

“…Indeed, the presence/absence and morphology of sulci are theorized to be anatomically linked to cortical white matter development (Sanides 1962, 1964; Van Essen et al 2014; Reveley et al 2015; Van Essen 2020; Cottaar et al 2021; Miller et al 2021b; Cachia et al 2021), and the presence of sulci relates to changes in the local cytoarchitectonic organization of gray matter (Amiez et al 2021). Neural efficiency is the foundation of our hypothesis regarding relationships between sulcal anatomy and reasoning observed in these and other studies (Voorhies et al 2021; Willbrand et al 2023b). Specifically, we (and others; Garrison et al, 2015) hypothesize that these sulcal-behavioral relationships stem from individual differences in white matter projections and, in turn, the distributed functional brain networks that underlie higher-level cognition.…”

Emotion-related impulsivity is related to orbitofrontal cortical sulcation

“…Continuous Measurements: Building upon our prior work (11,12,13), to analyze continuous morphological sulcal-behavior relationships, we leveraged a pre-existing pipeline that tests for a relationship between sulcal morphology (i.e., sulcal depth) and ERI via the following approach:…”

“…We then implemented a model-based LASSO regression to relate OFC sulcal morphology to ERI, and subsequently tested whether effects were specific to ERI as compared to non-emotion-related impulsivity. We focused on sulcal depth as it is one of the main morphological features differentiating putative primary (deepest), secondary, and tertiary (shallowest) sulci from one another and recent research identifies a link between sulcal depth and cognition (11)(12)(13)(14). To our knowledge, this is the first study to examine the relationship between ERI and sulci identified in each individual hemisphere (including putative tertiary sulci, which have been largely overlooked and are considerably variable across hemispheres (15,(18)(19)), which is consistent with what has been referred to recently as a "precision imaging" approach (20).…”

Individual differences, missing sulci, and nomenclature: A comment on “On presentation of the human cerebral sulci from inside the cerebrum”

“…(a) Left hemisphere FreeSurfer inflated cortical reconstruction (gyri: light gray, sulci: dark gray) from an example Human Connectome Project participant (neuroimaging data from https://db.human conne ctome.org/) focused on the lateral prefrontal cortex (LPFC; inset for the location of the zoomed portion). LPFC sulci have been manually defined (outlined) based on the most recent atlas (Petrides, 2019) and published previously in this individual (Miller et al, 2021;Willbrand et al, 2023). Red sulci are those excluded from the present tool, whereas blue sulci are those included.…”