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Brain Imaging and Behavior

, Volume 9, Issue 3, pp 619–638 | Cite as

Task-rest modulation of basal ganglia connectivity in mild to moderate Parkinson’s disease

  • Eva M. Müller-Oehring
  • Edith V. Sullivan
  • Adolf Pfefferbaum
  • Neng C. Huang
  • Kathleen L. Poston
  • Helen M. Bronte-Stewart
  • Tilman Schulte
Original Research

Abstract

Parkinson’s disease (PD) is associated with abnormal synchronization in basal ganglia-thalamo-cortical loops. We tested whether early PD patients without demonstrable cognitive impairment exhibit abnormal modulation of functional connectivity at rest, while engaged in a task, or both. PD and healthy controls underwent two functional MRI scans: a resting-state scan and a Stroop Match-to-Sample task scan. Rest-task modulation of basal ganglia (BG) connectivity was tested using seed-to-voxel connectivity analysis with task and rest time series as conditions. Despite substantial overlap of BG–cortical connectivity patterns in both groups, connectivity differences between groups had clinical and behavioral correlates. During rest, stronger putamen–medial parietal and pallidum–occipital connectivity in PD than controls was associated with worse task performance and more severe PD symptoms suggesting that abnormalities in resting-state connectivity denote neural network dedifferentiation. During the executive task, PD patients showed weaker BG-cortical connectivity than controls, i.e., between caudate–supramarginal gyrus and pallidum–inferior prefrontal regions, that was related to more severe PD symptoms and worse task performance. Yet, task processing also evoked stronger striatal–cortical connectivity, specifically between caudate–prefrontal, caudate–precuneus, and putamen–motor/premotor regions in PD relative to controls, which was related to less severe PD symptoms and better performance on the Stroop task. Thus, stronger task-evoked striatal connectivity in PD demonstrated compensatory neural network enhancement to meet task demands and improve performance levels. fMRI-based network analysis revealed that despite resting-state BG network compromise in PD, BG connectivity to prefrontal, premotor, and precuneus regions can be adequately invoked during executive control demands enabling near normal task performance.

Keywords

Parkinson’s disease Cognitive control Response switching fMRI Task-related and resting-state functional connectivity Neural compensation 

Notes

Acknowledgments

Support: AA018022, AA012388, AA017168, AA010723, AA017923, NIH/NINDS K23 NS075097, NIH/NINDS P50 NS071675, Michael J. Fox Foundation for Parkinson’s disease

Conflict of Interest

Authors Eva M. Müller-Oehring, Edith V. Sullivan, Adolf Pfefferbaum, Neng C. Huang, Kathleen L. Poston, Helen M. Bronte-Stewart, and Tilman Schulte declare that they have no conflict of interest.

Informed Consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.

Supplementary material

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Supplementary Table 1 (DOCX 65 kb)
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Supplementary Table 2 (DOCX 67 kb)
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Supplementary Table 3 (DOCX 63 kb)
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Supplementary Table 4 (DOCX 64 kb)
11682_2014_9317_MOESM5_ESM.docx (57 kb)
Supplementary Table 5 (DOCX 56 kb)

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Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Eva M. Müller-Oehring
    • 1
    • 4
  • Edith V. Sullivan
    • 1
  • Adolf Pfefferbaum
    • 1
    • 4
  • Neng C. Huang
    • 3
  • Kathleen L. Poston
    • 2
  • Helen M. Bronte-Stewart
    • 2
  • Tilman Schulte
    • 4
  1. 1.Department of Psychiatry & Behavioral SciencesStanford University School of MedicineStanfordUSA
  2. 2.Department of Neurology & Neurological SciencesStanford University School of MedicineStanfordUSA
  3. 3.Valley Parkinson ClinicLos GatosUSA
  4. 4.Neuroscience Program, SRI InternationalMenlo ParkUSA

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