Sulcal Polymorphisms of the IFC and ACC Contribute to Inhibitory Control Variability in Children and Adults

Abstract

Inhibitory control (IC) is a core executive function that enables humans to resist habits, temptations, or distractions. IC efficiency in childhood is a strong predictor of academic and professional success later in life. Based on analysis of the sulcal pattern, a qualitative feature of cortex anatomy determined during fetal life and stable during development, we searched for evidence that interindividual differences in IC partly trace back to prenatal processes. Using anatomical magnetic resonance imaging (MRI), we analyzed the sulcal pattern of two key regions of the IC neural network, the dorsal anterior cingulate cortex (ACC) and the inferior frontal cortex (IFC), which limits the inferior frontal gyrus. We found that the sulcal pattern asymmetry of both the ACC and IFC contributes to IC (Stroop score) in children and adults: participants with asymmetrical ACC or IFC sulcal patterns had better IC efficiency than participants with symmetrical ACC or IFC sulcal patterns. Such additive effects of IFC and ACC sulcal patterns on IC efficiency suggest that distinct early neurodevelopmental mechanisms targeting different brain regions likely contribute to IC efficiency. This view shares some analogies with the “common variant–small effect” model in genetics, which states that frequent genetic polymorphisms have small effects but collectively account for a large portion of the variance. Similarly, each sulcal polymorphism has a small but additive effect: IFC and ACC sulcal patterns, respectively, explained 3% and 14% of the variance of the Stroop interference scores.

ACC Sulcal Patterns and Their Modulation on Cognitive Control Efficiency Across Lifespan: A Neuroanatomical Study on Bilinguals and Monolinguals

“…The contribution of ACC morphology to CC skills has been recently investigated by parameterizing variability in ACC sulcation (Huster et al 2011;Borst et al 2014;Cachia et al 2014), which is primarily assessed by quantifying the occurrence and extension of the paracingulate sulcus (PCS), a secondary sulcus that runs dorsal and parallel to the cingulate sulcus (CS) on the medial surface of the ACC (Ono et al 1990;Paus et al 1996;Vogt and Palomero-Gallagher 2012). Differently from quantitative measures of cortex structure (e.g., cortical thickness, surface area, or gyrification index), the ACC sulcal pattern is a neurodevelopmental marker determined in utero (Chi et al 1977;Welker 1990;Mangin et al 2010) and largely unaffected by brain maturation (Cachia et al 2016;Tissier et al 2018) or environmentally induced neuroplastic changes (Sun et al 2012). While primary sulci (e.g., CS) emerge early during fetal development and are present in all individuals with stable characteristic locations and orientations, secondary, and tertiary sulci (e.g., PCS) begin to appear much later during gestation (in the second-third trimester) in approximately half of all neonates, thus, providing a clue to the study of individual differences in brain-behavior relationships (Chi et al 1977;Armstrong et al 1995).…”

“…The double parallel type is present in 30-60% of normal individuals (Paus et al 1996;Yücel et al 2001) with greater prevalence in the left hemisphere (Paus et al 1996;Yücel et al 2001;Leonard et al 2009), thereby yielding a leftward asymmetry population bias. Although the specific factors mediating the development of the PCS and its asymmetry are still unclear, evidence suggests that individuals with asymmetrical ACC sulcal patterns as compared with those with symmetrical patterns exhibit a performance advantage across several higher-order functions that draw on CC, such as reality monitoring (Whittle et al 2009;Buda et al 2011), inhibitory control (Huster et al 2009;Borst et al 2014;Cachia et al 2014;Tissier et al 2018), and verbal and spatial working memory (Fornito et al 2004). The functional significance of individual differences in ACC sulcation has also been reported in clinical studies, where abnormal occurrence and/or morphology of the PCS have been linked to CC impairment in patients with full-blown schizophrenia (Yücel et al 2002;Fornito et al 2006;Garrison et al 2015) as well as in individuals at-risk of developing schizophrenia symptoms (Yücel et al 2003b).…”

Sulcal Pattern Variability and Dorsal Anterior Cingulate Cortex Functional Connectivity Across Adult Age

“…Secondary and tertiary sulci develop as side-branches of primary sulci between the 30th and 36th week of gestation, yielding variable patterns that are likely influenced by in-womb and perinatal environmental factors (Amiez et al, 2018;Lohmann et al, 1999). Different from quantitative measures of cortex structure (e.g., cortical thickness, surface area, gyrification index), the dACC sulcal pattern is a morphologic feature determined prenatally and stable throughout development (Cachia et al, 2016;Tissier et al, 2018). The longitudinal stability of the dACC sulcal pattern and its resilience to neuroplastic changes* provide a clue to the study of individual differences in structure-function mappings, with the possibility to identify early neuroanatomical constraints on subsequent cognitive abilities (Borst et al, 2014;Fornito et al, 2004;Tissier et al, 2018).…”

“…Different from quantitative measures of cortex structure (e.g., cortical thickness, surface area, gyrification index), the dACC sulcal pattern is a morphologic feature determined prenatally and stable throughout development (Cachia et al, 2016;Tissier et al, 2018). The longitudinal stability of the dACC sulcal pattern and its resilience to neuroplastic changes* provide a clue to the study of individual differences in structure-function mappings, with the possibility to identify early neuroanatomical constraints on subsequent cognitive abilities (Borst et al, 2014;Fornito et al, 2004;Tissier et al, 2018). Although variability in dACC sulcation has been shown to affect the spatial distribution of local task-related functional activity (Amiez et al, 2013;Crosson et al, 1999;Jahn et al, 2016), it is largely unknown whether differences in sulcal pattern might alter the functional organization of the dACC in resting state, that is, in absence of overt task performance or stimulation.…”

Volumetric Segmentation and Characterisation of the Paracingulate Sulcus on MRI Scans

“…The sulcus has been proved to be highly related to psychiatric and psychological phenomena such as hallucinations, where 1 cm reduction in sulcal length can increase the chance of hallucination by 20%, semantic fluency, and schizophrenia [1,2,3]. The morphology of the sulcus is highly variable between individuals [4], and the its presence can also affect the size of anterior cingulate and paracingulate cortices, which contributes to the control of emotion, inhibitory, and cognition [5,6]. One of the widely used methods to manually identify the PCS is explained in [1].…”