Developmental changes in the organization of functional connections between the basal ganglia and cerebral cortex

Deanna J. Greene, Timothy O. Laumann, Joseph W. Dubis, S. Katie Ihnen, Maital Neta, Jonathan D. Power, John R. Pruett, Kevin J. Black, Bradley L. Schlaggar

Research output: Contribution to journalArticle

45 Citations (Scopus)

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 rs-fcMRI 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).

Original languageEnglish (US)
Pages (from-to)5842-5854
Number of pages13
JournalJournal of Neuroscience
Volume34
Issue number17
DOIs
StatePublished - Jan 1 2014

Fingerprint

Basal Ganglia
Cerebral Cortex
Magnetic Resonance Imaging
Basal Ganglia Diseases
Tourette Syndrome
Globus Pallidus
Putamen
Artifacts
Multivariate Analysis
Hand

Keywords

  • Basal ganglia
  • Development
  • Functional connectivity
  • Resting state

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Developmental changes in the organization of functional connections between the basal ganglia and cerebral cortex. / Greene, Deanna J.; Laumann, Timothy O.; Dubis, Joseph W.; Ihnen, S. Katie; Neta, Maital; Power, Jonathan D.; Pruett, John R.; Black, Kevin J.; Schlaggar, Bradley L.

In: Journal of Neuroscience, Vol. 34, No. 17, 01.01.2014, p. 5842-5854.

Research output: Contribution to journalArticle

Greene, DJ, Laumann, TO, Dubis, JW, Ihnen, SK, Neta, M, Power, JD, Pruett, JR, Black, KJ & Schlaggar, BL 2014, 'Developmental changes in the organization of functional connections between the basal ganglia and cerebral cortex', Journal of Neuroscience, vol. 34, no. 17, pp. 5842-5854. https://doi.org/10.1523/JNEUROSCI.3069-13.2014
Greene, Deanna J. ; Laumann, Timothy O. ; Dubis, Joseph W. ; Ihnen, S. Katie ; Neta, Maital ; Power, Jonathan D. ; Pruett, John R. ; Black, Kevin J. ; Schlaggar, Bradley L. / Developmental changes in the organization of functional connections between the basal ganglia and cerebral cortex. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 17. pp. 5842-5854.
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