Presence or absence of a prefrontal sulcus is linked to reasoning performance during child development

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. When controlling for age, the presence or absence of the ventral component of the pimfs was associated with reasoning, as was the total surface area of pimfs. These findings show that multiple features of sulci can support the development of complex cognitive abilities and highlight the importance of considering individual differences in local morphology when exploring the neurodevelopmental basis of cognition.

Development of human lateral prefrontal sulcal morphology and its relation to reasoning performance

“…General details: The present study leveraged previously published data from the longitudinal Neurodevelopment of Reasoning Ability (NORA) dataset (Wendelken et al, 2011(Wendelken et al, , 2016(Wendelken et al, , 2017Ferrer et al, 2013;Voorhies et al, 2021;Willbrand et al, 2022b;Yao et al, 2022). All participants were screened for neurological impairments, psychiatric illness, history of learning disability, and developmental delay.…”

“…We then defined eight sulci anterior to the prcs and superior to the ifs: 1) the anterior (sfs-a) and 2) posterior (sfs-p) components of the superior frontal sulcus (sfs), 3) the vertical (imfs-v) and 4) horizontal (imfs-h) components of the intermediate fronto-marginal sulcus (imfs), 5) the anterior (pmfs-a), 6) intermediate (pmfs-i), and 7) posterior (pmfs-p) components of the posterior middle frontal sulcus (pmfs), and 8) the paraintermediate frontal sulcus (pimfs). These 12 sulci have previously been identified in children and adolescents (Voorhies et al, 2021;Willbrand et al, 2022b;Yao et al, 2022), as well as in young adults (Miller et al, 2021b). Finally, we defined the six sulci inferior to the ifs: the diagonal sulcus (ds), the triangular sulcus (ts), the pre-triangular sulcus (prts), the lateral marginal frontal sulcus (lfms), the ascending ramus of the lateral fissure (aalf), and the horizontal ramus of the lateral fissure (half).…”

“…After defining LPFC sulci in FreeSurfer, we extracted the following morphological metrics from each sulcal label file: sulcal depth (mm), surface area (mm 2 ), cortical thickness (mm), and local gyrification index (lGI). We selected sulcal depth and surface area as these metrics are prominent features of sulci (Sanides, 1964;Chi et al, 1977;Welker, 1990;Armstrong et al, 1995;Weiner et al, 2014Weiner et al, , 2018Lopez-Persem et al, 2019;Madan, 2019;Petrides, 2019;Weiner, 2019;Miller et al, 2020Miller et al, , 2021aMiller et al, , 2021bNatu et al, 2021;Voorhies et al, 2021;Li et al, 2022;Willbrand et al, 2022aWillbrand et al, , 2022bYao et al, 2022). We further selected cortical thickness and lGI since the longitudinal development of these features was previously analyzed at the lobular level (Alemán-Gómez et al, 2013).…”

“…Fourth, LPFC contains indentations, or sulci, that are either hominoid-specific or human-specific (Amiez and Petrides, 2007;Petrides, 2019;Miller et al, 2021aMiller et al, , 2021bVoorhies et al, 2021;Hathaway et al, 2022;Willbrand et al, 2022b;Yao et al, 2022). Importantly, the morphology (Voorhies et al, 2021;Yao et al, 2022) and the presence or absence of these variable LPFC sulci (Willbrand et al, 2022b) is related to cognitive abilities. Thus, human LPFC is a heterogeneous entity with sulci that show striking individual differences in morphology that are related to individual differences in cognition-a relationship that necessitates studying LPFC sulcal development at the individual level.…”

“…Given the limitations of "large N," group-level analyses on studying sulcal morphology (Miller et al, 2021a(Miller et al, , 2021b, here, we took a "deep imaging" approach (Gratton et al, 2022) to study age-related changes in sulcal morphology and brain-behavior relationships by focusing on a large sampling of individual sulci within individual participants. To this end, we first leveraged individual LPFC sulcal data (3672 sulcal definitions) from 108 participants (6-36 years old) from previous work in pediatric (Voorhies et al, 2021;Willbrand et al, 2022b;Yao et al, 2022) and young adult samples (Miller et al, 2021b) to address whether the morphology of these sulci differs cross-sectionally during this timeframe. We then defined 2992 sulci (1496 per timepoint) in a subset of the pediatric participants scanned at two timepoints (N = 44) to determine whether LPFC sulcal morphology changes longitudinally, across an average timeframe of 1.6 years.…”