Longitudinal stability of the folding pattern of the anterior cingulate cortex during development

Abstract

Prenatal processes are likely critical for the differences in cognitive ability and disease risk that unfold in postnatal life. Prenatally established cortical folding patterns are increasingly studied as an adult proxy for earlier development events - under the as yet untested assumption that an individual's folding pattern is developmentally fixed. Here, we provide the first empirical test of this stability assumption using 263 longitudinally-acquired structural MRI brain scans from 75 typically developing individuals spanning ages 7 to 32 years. We focus on the anterior cingulate cortex (ACC) - an intensely studied cortical region that presents two qualitatively distinct and reliably classifiable sulcal patterns with links to postnatal behavior. We show - without exception-that individual ACC sulcal patterns are fixed from childhood to adulthood, at the same time that quantitative anatomical ACC metrics are undergoing profound developmental change. Our findings buttress use of folding typology as a postnatally-stable marker for linking variations in early brain development to later neurocognitive outcomes in ex utero life.

Keywords: ACC; Executive control; Fetal life; MRI; Neurodevelopment; Sulcal pattern.

Fig. 1

Participant age at scan. Each dot represents a participant scan. Each line represents a participant with repeated scans.

Fig. 2

The different sulcal pattern types of the anterior cingulate cortex (ACC) using Ono's nomenclature (two sulcal pattern types) and Yucel's nomenclature (three sulcal pattern types). Left panel: subject with only a cingulate sulcus (light blue), labeled as ‘single’ type in Ono's nomenclature or ‘absent’ type in Yucel's nomenclature. Middle panel: subject with a cingulate sulcus and a small (<40 mm) additional paracingulate sulcus (in blue), labeled as ‘double parallel’ type in Ono's nomenclature or ‘present’ type in Yucel's nomenclature. Right panel: subjects with a cingulate sulcus and a long (>40 mm) additional paracingulate sulcus (in blue), labeled as ‘double parallel’ type in Ono's nomenclature or ‘prominent’ type in Yucel's nomenclature.

Fig. 3

The sulcal pattern of the anterior cingulate cortex (ACC) remains stable from late childhood to adulthood. Longitudinal stability of the ACC sulcal pattern in a subject with a ‘single type’ ACC, with only the cingulate sulcus (light blue), and in a subject with a ‘double parallel type ACC’, with a cingulate sulcus and an additional paracingulate sulcus (in blue).

Fig. 4

The cortical thickness in the anterior cingulate cortex (ACC) changes with age from late childhood to adulthood. Map of the linear age effect (FDR-corrected T-statistic, q ≤ 0.05) on the cortical thickness. The dorsal part of ACC is indicated with a yellow dashed line.