Reward-Sensitive Basal Ganglia Stabilize the Maintenance of Goal-Relevant Neural Patterns in Adolescents

Authors

Nicholas A. Hubbard, Massachusetts Institute of Technology; University of Nebraska-LincolnFollow
Rachel R. Romeo, Massachusetts Institute of Technology: Harvard Medical School
Hannah Grotzinger, Massachusetts Institute of Technology
Melissa Giebler, Massachusetts Institute of Technology
Andrea Imhof, Massachusetts Institute of Technology; University of Oregon
Clemens C. C Bauer, Massachusetts Institute of Technology; University of Oregon
John D. E. Gabrieli, Massachusetts Institute of Technology; University of Oregon

Document Type

Article

Date of this Version

2020

Citation

Published in final edited form as: J Cogn Neurosci. 2020 August ; 32(8): 1508–1524. doi:10.1162/jocn_a_01572.

Comments

Author manuscript J Cogn Neurosci. Author manuscript; available in PMC 2021 October 08.

Abstract

Maturation of basal ganglia (BG) and frontoparietal circuitry parallels developmental gains in working memory (WM). Neurobiological models posit that adult WM performance is enhanced by communication between reward-sensitive BG and frontoparietal regions, via increased stability in the maintenance of goal-relevant neural patterns. It is not known whether this reward-driven pattern stability mechanism may have a role in WM development. In 34 young adolescents (12.16–14.72 years old) undergoing fMRI, reward-sensitive BG regions were localized using an incentive processing task. WM-sensitive regions were localized using a delayed-response WM task. Functional connectivity analyses were used to examine the stability of goal-relevant functional connectivity patterns during WM delay periods between and within reward-sensitive BG and WM-sensitive frontoparietal regions. Analyses revealed that more stable goal-relevant connectivity patterns between reward-sensitive BG and WM-sensitive frontoparietal regions were associated with both greater adolescent age and WM ability. Computational lesion models also revealed that functional connections to WM-sensitive frontoparietal regions from reward-sensitive BG uniquely increased the stability of goal-relevant functional connectivity patterns within frontoparietal regions. Findings suggested (1) the extent to which goal-relevant communication patterns within reward-frontoparietal circuitry are maintained increases with adolescent development and WM ability and (2) communication from reward-sensitive BG to frontoparietal regions enhances the maintenance of goal-relevant neural patterns in adolescents’ WM. The maturation of reward-driven stability of goal-relevant neural patterns may provide a putative mechanism for understanding the developmental enhancement of WM.