Hyperdirect insula-basal-ganglia pathway and adult-like maturity of global brain responses predict inhibitory control in children

Weidong Cai,Victor Carrion,Aarthi Padmanabhan,Katherine Duberg,Vinod Menon,Rachel Rehert,Travis Bradley

doi:10.1038/s41467-019-12756-8

Weidong Cai, Victor Carrion + Show 5 more

Open Access

https://doi.org/10.1038/s41467-019-12756-8

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Journal: Nature Communications	Publication Date: Oct 22, 2019
Citations: 33	License type: open-access

Affiliation: Stanford University

Abstract

Inhibitory control is fundamental to children’s self-regulation and cognitive development. Here we investigate cortical-basal ganglia pathways underlying inhibitory control in children and their adult-like maturity. We first conduct a comprehensive meta-analysis of extant neurodevelopmental studies of inhibitory control and highlight important gaps in the literature. Second, we examine cortical-basal ganglia activation during inhibitory control in children ages 9–12 and demonstrate the formation of an adult-like inhibitory control network by late childhood. Third, we develop a neural maturation index (NMI), which assesses the similarity of brain activation patterns between children and adults, and demonstrate that higher NMI in children predicts better inhibitory control. Fourth, we show that activity in the subthalamic nucleus and its effective connectivity with the right anterior insula predicts children’s inhibitory control. Fifth, we replicate our findings across multiple cohorts. Our findings provide insights into cortical-basal ganglia circuits and global brain organization underlying the development of inhibitory control.

Highlights

Inhibitory control is fundamental to children’s self-regulation and cognitive development
Adults showed a highly consistent pattern of brain activations associated with inhibitory control[17], encompassing bilateral AI, right IFG, MFG, preSMA, posterior parietal cortex (PPC), and striatum (p < 0.01, FWE corrected, Fig. 2a, see cluster coordinates in Supplementary Table 3)
The use of open-source fMRI datasets allowed us to test the generalizability of our findings, and to advance analytic approaches for facilitating replicability in developmental cognitive neuroscience

Summary

Introduction

Inhibitory control is fundamental to children’s self-regulation and cognitive development. Inhibitory action control engages a widely distributed set of cortical and basal ganglia systems[10,11,12,13,14,15,16] including, most notably, the right anterior insula (rAI) and the right inferior frontal gyrus (rIFG), and to a lesser extent the right middle frontal gyrus (rMFG), right pre-supplementary motor area (rPreSMA), right supramarginal gyrus (rSMG) and right caudate (rCau)[17] Both animal[18,19,20,21] and human[9,22] studies have shown strong evidence for the role of the hyperdirect cortical–basal ganglia pathway during inhibitory action control[23,24]. The SSRT is an optimal measure of stopping as it has a strong association with stopping-related neuronal activity in cortical-STN circuits[30,31]

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