Developmental Changes in the Organization of Functional Connections between the Basal Ganglia and Cerebral Cortex

Authors

Deanna J. Greene, Washington University School of MedicineFollow
Timothy O. Laumann, Washington University School of Medicine
Joseph W. Dubis, Washington University School of Medicine
S. Katie Ihnen, Washington University School of Medicine
Maital Neta, Washington University School of MedicineFollow
Jonathan D. Power, Washington University School of Medicine
John R. Pruett Jr., Washington University School of Medicine
Kevin J. Black, Washington University School of Medicine
Bradley L. Schlaggar, Washington University School of Medicine

Date of this Version

2014

Citation

J. Neurosci., April 23, 2014 • 34(17):5842–5854

Comments

Copyright © 2014 the authors

DOI:10.1523/JNEUROSCI.3069-13.2014

Abstract

The basal ganglia (BG) comprise a set of subcortical nuclei with sensorimotor, cognitive, and limbic subdivisions, indicative of functional organization. BG dysfunction in several developmental disorders suggests the importance of the healthy maturation of these structures. However, few studies have investigated the development of BG functional organization. Using resting-state functional connectivity MRI (rs-fcMRI), we compared human child and adult functional connectivity of the BG with rs-fcMRI-defined cortical systems. Because children move more than adults, customized preprocessing, including volume censoring, was used to minimize motion-induced rsfcMRI artifact. Our results demonstrated functional organization in the adult BG consistent with subdivisions previously identified in anatomical tracing studies. Group comparisons revealed a developmental shift in bilateral posterior putamen/pallidum clusters from preferential connectivity with the somatomotor “face” system in childhood to preferential connectivity with control/attention systems (frontoparietal, ventral attention) in adulthood. This shift was due to a decline in the functional connectivity of these clusters with the somatomotor face system over development, and no change with control/attention systems. Applying multivariate pattern analysis, we were able to reliably classify individuals as children or adults based on BG–cortical system functional connectivity. Interrogation of the features driving this classification revealed, in addition to the somatomotor face system, contributions by the orbitofrontal, auditory, and somatomotor hand systems. These results demonstrate that BG–cortical functional connectivity evolves over development, and may lend insight into developmental disorders that involve BG dysfunction, particularly those involving motor systems (e.g., Tourette syndrome).