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.
The lateral prefrontal cortex (LPFC) is disproportionately expanded in humans compared to non-human primates, although the relationship between LPFC brain structures and uniquely human cognitive skills is largely unknown. Here, we test the relationship between variability in LPFC tertiary sulcal morphology and reasoning scores in a cohort of children and adolescents. Using a data-driven approach in independent discovery and replication samples, we show that the depth of specific LPFC tertiary sulci is associated with individual differences in reasoning scores beyond age. To expedite discoveries in future neuroanatomical-behavioral studies, we share tertiary sulcal definitions with the field. These findings support a classic but largely untested theory linking the protracted development of tertiary sulci to late-developing cognitive processes.
more » « less- NSF-PAR ID:
- 10383468
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 12
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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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 STATEMENT Recent 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. -
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Recent work suggests that indentations of the cerebral cortex, or sulci, may be uniquely vulnerable to atrophy in aging and Alzheimer's disease (AD) and that posteromedial cortex (PMC) is particularly vulnerable to atrophy and pathology accumulation. However, these studies did not consider small, shallow, and variable tertiary sulci that are located in association cortices and are often associated with human-specific aspects of cognition. Here, we manually defined 4,362 PMC sulci in 432 hemispheres in 216 human participants (50.5% female) and found that these smaller putative tertiary sulci showed more age- and AD-related thinning than larger, more consistent sulci, with the strongest effects for two newly uncovered sulci. A model-based approach relating sulcal morphology to cognition identified that a subset of these sulci was most associated with memory and executive function scores in older adults. These findings lend support to the retrogenesis hypothesis linking brain development and aging, and provide new neuroanatomical targets for future studies of aging and AD.
Significance Statement Large-scale changes in cortical structure in aging suggest sulci are particularly vulnerable to atrophy. However, tertiary sulci, the smallest and most individually variable cortical folds associated with cognitive development, have not been studied in aging. Here, we investigate tertiary sulci for the first time in aging and Alzheimer's disease (AD). We find that these smaller and shallower sulci show more age- and AD-related thinning than larger sulci in posteromedial cortex (PMC), and that the atrophy of a subset of PMC sulci is most associated with cognition in older adults. These findings support classical theories linking developmental and aging trajectories at a novel anatomical resolution and provide insight into relationships between individual differences in structural brain changes and cognitive decline. -
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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.
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Abstract Recent studies identify a surprising coupling between evolutionarily new sulci and the functional organization of human posteromedial cortex (PMC). Yet, no study has compared this modern PMC sulcal patterning between humans and non-human hominoids. To fill this gap in knowledge, we first manually defined over 2500 PMC sulci in 120 chimpanzee ( Pan Troglodytes ) hemispheres and 144 human hemispheres. We uncovered four new sulci, and quantitatively identified species differences in sulcal incidence, depth, and surface area. Interestingly, some sulci are more common in humans and others, in chimpanzees. Further, we found that the prominent marginal ramus of the cingulate sulcus differs significantly between species. Contrary to classic observations, the present results reveal that the surface anatomy of PMC substantially differs between humans and chimpanzees—findings which lay a foundation for better understanding the evolution of neuroanatomical-functional and neuroanatomical-behavioral relationships in this highly expanded region of the human cerebral cortex.more » « less
