Maturational trajectories of white matter microstructure underlying the right presupplementary motor area reflect individual improvements in motor response cancellation in children and adolescents
Authors: Madsen Kathrine Skak , Johansen Louise Baruël , Thompson Wesley K. , Siebner Hartwig R. , Jernigan Terry L. , Baaré William F. C. 
Published: March 2020

The ability to effectively suppress motor response tendencies is essential for focused and goal-directed behavior. Here, we tested the hypothesis that developmental improvement in the ability to cancel a motor response is reflected by maturational changes in the white matter underlying the right presupplementary motor area (preSMA) and posterior inferior frontal gyrus (IFG), two cortical key areas of the fronto-basal ganglia “stopping” network. Eighty-eight typically-developing children and adolescents, aged 7-19 years, were longitudinally assessed with the stop-signal task (SST) and diffusion tensor imaging (DTI) of the brain over a period of six years. Participants were examined from two to nine times with an average of 6.6 times, resulting in 576 SST-DTI datasets. We applied tract-based spatial statistics to extract mean fractional anisotropy (FA) from regions-of-interest in the white matter underlying the right IFG (IFGFA) and right preSMA (preSMAFA) at each time point. Motor response cancelation performance, estimated with the stop-signal reaction time (SSRT), improved with age. Initially well performing children plateaued around the age of 11 years, while initially poor performers caught up at the age of 13-14 years. White matter microstructure continued to mature across the investigated age range. Males generally displayed linear maturational trajectories, while females displayed more curvilinear trajectories that leveled off around 12-14 years of age. Maturational increases in right preSMAFAbut not right IFGFAwere associated with developmental improvements in SSRT. This association differed depending on the mean right preSMAFAacross the individual maturational trajectory. Children with lower mean right preSMAFAexhibited poorer SSRT performance at younger ages but steeper developmental trajectories of SSRT improvement. Children with higher mean right preSMAFAexhibited flatter trajectories of SSRT improvement along with faster SSRT already at the first assessments. The results suggest that no further improvement in motor response cancellation is achieved once a certain level of maturity in the white matter underlying the right preSMA is reached. Similar dynamics may apply to other behavioral read-outs and brain structures and, thus, need to be considered in longitudinal MRI studies designed to map brain structural correlates of behavioral changes during development.

Highlights

Motor response cancellation, i.e. SSRT, improvement plateaued at 13-14 years of age

Fractional anisotropy (FA) captured maturation of white matter (WM) microstructure

FA in the WM underlying right preSMA (preSMAFA) reflected SSRT improvement with age

Individual SSRT improvement depended on mean right preSMAFAacross all DTI sessions

Children with lower mean right preSMAFAhad the steepest improvements in SSRT