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Brain functional specialization and cooperation in Parkinson’s disease

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Abstract

Cerebral specialization and inter-hemispheric cooperation are two of the most prominent functional architectures of the human brain. Their dysfunctions may be related to pathophysiological changes in patients with Parkinson’s disease (PD), who are characterized by unbalanced onset and progression of motor symptoms. This study aimed to characterize the two intrinsic architectures of hemispheric functions in PD using resting-state functional magnetic resonance imaging. Seventy idiopathic PD patients and 70 age-, sex-, and education-matched healthy subjects were recruited. All participants underwent magnetic resonance image scanning and clinical evaluations. The cerebral specialization (Autonomy index, AI) and inter-hemispheric cooperation (Connectivity between Functionally Homotopic voxels, CFH) were calculated and compared between groups. Compared with healthy controls, PD patients showed stronger AI in the left angular gyrus. Specifically, this difference in specialization resulted from increased functional connectivity (FC) of the ipsilateral areas (e.g., the left prefrontal area), and decreased FC in the contralateral area (e.g., the right supramarginal gyrus). Imaging-cognitive correlation analysis indicated that these connectivity were positively related to the score of Montreal Cognitive Assessment in PD patients. CFH between the bilateral sensorimotor regions was significantly decreased in PD patients compared with controls. No significant correlation between CFH and cognitive scores was found in PD patients. This study illustrated a strong leftward specialization but weak inter-hemispheric coordination in PD patients. It provided new insights to further clarify the pathological mechanism of PD.

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Data availability

The data and materials that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

The authors thank the participants for taking part in this study and thank Information Science Laboratory Center of USTC for the measurement services.

Funding

This study was funded by the National Natural Science Foundation of China, Grant/Award Numbers: 31970979, 81971689, 91432301, 81671354, 31571149, 91232717, and 81771456; the Doctoral Foundation of Anhui Medical University, Grant/Award Number XJ201532; the National Basic Research Program of China, Grant/Award Number 2015CB856405; the National Key R&D Plan of China, Grant/Award Number: 2016YFC1300604; the Collaborative Innovation Center of Neuropsychiatric Disorders and Mental Health of Anhui Province; and the Youth Top-notch Talent Support Program of Anhui Medical University.

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Author notes

  1. Jinmei Sun and Xiaoran Gao have contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology, The First Affiliated Hospital of Anhui Medical University, Anhui Medical University, Hefei, 230000, China

    Jinmei Sun, Pingping Liu, Tingting Liu, Gong-Jun Ji, Panpan Hu & Kai Wang

  2. School of Mental Health and Psychological Sciences, Anhui Medical University, Hefei, 230000, China

    Xiaoran Gao, Qiang Hua, Rongrong Du & Gong-Jun Ji

  3. Anhui Province Key Laboratory of Cognition and Neuropsychiatric Disorders, Hefei, 230032, China

    Jinmei Sun, Xiaoran Gao, Qiang Hua, Rongrong Du, Pingping Liu, Tingting Liu, Gong-Jun Ji, Panpan Hu & Kai Wang

  4. Collaborative Innovation Centre of Neuropsychiatric Disorder and Mental Health, Hefei, 230000, China

    Jinmei Sun, Xiaoran Gao, Qiang Hua, Rongrong Du, Pingping Liu, Tingting Liu, Gong-Jun Ji, Panpan Hu & Kai Wang

  5. Laboratory Center for Information Science, University of Science and Technology of China, Hefei, China

    Jinying Yang

  6. Hefei National Lab for Physical Sciences at the Microscale and the Centers for Biomedical Engineering, University of Science and Technology of China, Hefei, China

    Bensheng Qiu

  7. Institute of Artificial Intelligence, Hefei Comprehensive National Science Center, Hefei, 230000, China

    Kai Wang

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  1. Jinmei Sun
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Contributions

All the authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Conceptualization, JMS, GJJ, PPH, and KW; Data Acquisition, JMS, XRG, QH, RRD, PPL and TTL; Methodology, JMS, and GJJ; Writing—Original Draft, JMS; Writing—Review & Editing, GJJ, PPH and KW; Formal Analysis, GJJ; Funding Acquisition, GJJ, PPH, and KW; Resources, PPH, and KW; Supervision, JYY and BSQ.

Corresponding authors

Correspondence to Gong-Jun Ji, Panpan Hu or Kai Wang.

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The authors declare that they have no competing interests.

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This study protocol was reviewed and approved by the Medical Ethics Committee of Anhui Medical University.

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The research protocol was performed according to the Helsinki Declaration of 1975 and approved by the Medical Ethics Committee of Anhui Medical University. Written informed consent was obtained from all participants after full explanation of the procedures involved.

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Sun, J., Gao, X., Hua, Q. et al. Brain functional specialization and cooperation in Parkinson’s disease. Brain Imaging and Behavior 16, 565–573 (2022). https://doi.org/10.1007/s11682-021-00526-4

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