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Abstract The lateral prefrontal cortex (LPFC) is an evolutionarily expanded region in humans that is critical for numerous complex functions, many of which are largely hominoid specific. Although recent work shows that the presence or absence of specific sulci in anterior LPFC is associated with cognitive performance across age groups, it is unknown whether the presence of these structures relates to individual differences in the functional organization of LPFC. To fill this gap in knowledge, we leveraged multimodal neuroimaging data from two samples encompassing 82 young adult humans (aged 22–36 years) and show that the dorsal and ventral components of the paraintermediate frontal sulcus, or pimfs, present distinct morphological (surface area), architectural (thickness and myelination), and functional (resting-state connectivity networks) properties. We further contextualize the pimfs components within classic and modern cortical parcellations. Taken together, the dorsal and ventral pimfs components mark transitions in LPFC anatomy and function, across metrics and parcellations. These results emphasize that the pimfs is a critical structure to consider when examining individual differences in the anatomical and functional organization of LPFC and suggest that future individual-level parcellations could benefit from incorporating sulcal anatomy when delineating LPFC cortical regions. 

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 morphologic neuroimaging data in the lateral PFC (LPFC) from individual human participants (6-36 years old, males and females;N= 108; 3672 sulci), as well as longitudinal morphologic and behavioral data from a subset of child and adolescent participants scanned at two time points (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 PFC are behaviorally meaningful during childhood and adolescence. Here, we describe how specific lateral PFC 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 morphologic 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. 

Abstract The relationship between structural variability in late-developing association cortices like the lateral prefrontal cortex (LPFC) and the development of higher-order cognitive skills is not well understood. Recent findings show that the morphology of LPFC sulci predicts reasoning performance; this work led to the observation of substantial individual variability in the morphology of one of these sulci, the para-intermediate frontal sulcus (pimfs). Here, we sought to characterize this variability and assess its behavioral significance. To this end, we identified the pimfs in a developmental cohort of 72 participants, ages 6–18. Subsequent analyses revealed that the presence or absence of the ventral component of the pimfs was associated with reasoning, even when controlling for age. This finding shows that the cortex lining the banks of sulci can support the development of complex cognitive abilities and highlights the importance of considering individual differences in local morphology when exploring the neurodevelopmental basis of cognition. 

Abstract The neuroanatomical changes that underpin cognitive development are of major interest in neuroscience. Of the many aspects of neuroanatomy to consider, tertiary sulci are particularly attractive as they emerge last in gestation, show a protracted development after birth, and are either human- or hominoid-specific. Thus, they are ideal targets for exploring morphological-cognitive relationships with cognitive skills that also show protracted development such as working memory (WM). Yet, the relationship between sulcal morphology and WM is unknown—either in development or more generally. To fill this gap, we adopted a data-driven approach with cross-validation to examine the relationship between sulcal depth in lateral prefrontal cortex (LPFC) and verbal WM in 60 children and adolescents between ages 6 and 18. These analyses identified 9 left, and no right, LPFC sulci (of which 7 were tertiary) whose depth predicted verbal WM performance above and beyond the effect of age. Most of these sulci are located within and around contours of previously proposed functional parcellations of LPFC. This sulcal depth model outperformed models with age or cortical thickness. Together, these findings build empirical support for a classic theory that tertiary sulci serve as landmarks in association cortices that contribute to late-maturing human cognitive abilities. 

A previously uncharted brain structure links functional and anatomical organization and differs across the life span and species. 

Prior research points to a positive concurrent relationship between reasoning ability and both frontoparietal structural connectivity (SC) as measured by diffusion tensor imaging (Tamnes et al., 2010) and frontoparietal functional connectivity (FC) as measured by fMRI (Cocchi et al., 2014). Further, recent research demonstrates a link between reasoning ability and FC of two brain regions in particular: rostrolateral prefrontal cortex (RLPFC) and the inferior parietal lobe (IPL) (Wendelken et al., 2016). Here, we sought to investigate the concurrent and dynamic, lead-lag relationships among frontoparietal SC, FC, and reasoning ability in humans. To this end, we combined three longitudinal developmental datasets with behavioral and neuroimaging data from 523 male and female participants between 6 and 22 years of age. Cross-sectionally, reasoning ability was most strongly related to FC between RLPFC and IPL in adolescents and adults, but to frontoparietal SC in children. Longitudinal analysis revealed that RLPFC-IPL SC, but not FC, was a positive predictor of future changes in reasoning ability. Moreover, we found that RLPFC-IPL SC at one time point positively predicted future changes in RLPFC-IPL FC, whereas, in contrast, FC did not predict future changes in SC. Our results demonstrate the importance of strong white matter connectivity between RLPFC and IPL during middle childhood for the subsequent development of both robust FC and good reasoning ability.SIGNIFICANCE STATEMENT The human capacity for reasoning develops substantially during childhood and has a profound impact on achievement in school and in cognitively challenging careers. Reasoning ability depends on communication between lateral prefrontal and parietal cortices. Therefore, to understand how this capacity develops, we examined the dynamic relationships over time among white matter tracts connecting frontoparietal cortices (i.e., structural connectivity, SC), coordinated frontoparietal activation (functional connectivity, FC), and reasoning ability in a large longitudinal sample of subjects 6-22 years of age. We found that greater frontoparietal SC in childhood predicts future increases in both FC and reasoning ability, demonstrating the importance of white matter development during childhood for subsequent brain and cognitive functioning.