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Common and specific altered amplitude of low-frequency fluctuations in Parkinson’s disease patients with and without freezing of gait in different frequency bands

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Abstract

Freezing of gait (FOG), a disabling symptom of Parkinson’s disease (PD), severely affects PD patients’ life quality. Previous studies found neuropathologies in functional connectivity related to FOG, but few studies detected abnormal regional activities related to FOG in PD patients. In the present study, we analyzed the amplitude of low-frequency fluctuations (ALFF) to detect brain regions showing abnormal activity in PD patients with FOG (PD-with-FOG) and without FOG (PD-without-FOG). As different frequencies of neural oscillations in brain may reflect distinct brain functional and physiological properties, we conducted this study in three frequency bands, slow-5 (0.01–0.027 Hz), slow-4 (0.027–0.073 Hz), and classical frequency band (0.01–0.08 Hz). We acquired rs-fMRI data from 18 PD-with-FOG patients, 18 PD-without-FOG patients, and 17 healthy controls, then calculated voxel-wise ALFF across the whole brain and compared ALFF among the three groups in each frequency band. We found: (1) in slow-5, both PD-with-FOG and PD-without-FOG patients showed lower ALFF in the bilateral putamen compared to healthy controls, (2) in slow-4, PD-with-FOG patients showed higher ALFF in left inferior temporal gyrus (ITG) and lower ALFF in right middle frontal gyrus (MFG) compared to either PD-without-FOG patients or healthy controls, (3) in classical frequency band, PD-with-FOG patients also showed higher ALFF in ITG compared to either PD-without-FOG patients or healthy controls. Furthermore, we found that ALFF in MFG and ITG in slow-4 provided the highest classification accuracy (96.7%) in distinguishing PD-with-FOG from PD-without-FOG patients by using a stepwise multivariate pattern analysis. Our findings indicated frequency-specific regional spontaneous neural activity related to FOG, which may help to elucidate the pathogenesis of FOG.

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Acknowledgments

The study was supported by grants from the National Natural Science Foundation of China [Grant numbers: 81871338, 81471654, 81428013, 81671275, and 81371535]; Planned Science and Technology Project of Guangdong Province, China [Grant numbers: 2014B020212022, 1563000653, 20160402007]; Innovation Project of Graduate School of South China Normal University. The funding organizations played no further role in study design, data collection, analysis and interpretation, and paper writing. The authors appreciate the editing assistance of Drs.Rhoda E. and Edmund F. Perozzi.

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Correspondence to Biao Huang or Ruiwang Huang.

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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 participants for being included in the study.

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Hu, H., Chen, J., Huang, H. et al. Common and specific altered amplitude of low-frequency fluctuations in Parkinson’s disease patients with and without freezing of gait in different frequency bands. Brain Imaging and Behavior 14, 857–868 (2020). https://doi.org/10.1007/s11682-018-0031-x

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