Share this content in WeChat
Original Article
Brain complexity in the patients of Parkinson's disease with depression: a resting-state functional magnetic resonance imaging study
LI Haidong  WANG Jun  NIU Jinliang 

Cite this article as: Li HD, Wang J, Niu JL. Brain complexity in the patients of Parkinson's disease with depression: a resting-state functional magnetic resonance imaging study[J]. Chin J Magn Reson Imaging, 2022, 13(7): 90-95. DOI:10.12015/issn.1674-8034.2022.07.016.

[Abstract] Objective To investigate the change of brain regions complexity by permutation entropy (PE), and to explore the imaging markers of characteristics in the patients of Parkinson's disease (PD) with depression.Materials and Methods Forty-five PD patients [twenty-two Parkinson's disease with depression (PD-Dep) patients, twenty-three Parkinson's disease patients without depression (PD-NDep) patients] and twenty-three healthy controls (HCs) were enrolled prospectively from 2020 to 2021 in the Second Hospital of Shanxi Medical University. All participants underwent resting state functional magnetic resonance imaging (rs-fMRI) scan. The progression of disease of patients was measured by 24-item Hamilton Depression Scale (HAMD-24) and Mini-Mental State Examination (MMSE) following each MRI scan. Permutation entropy (PE) was used to explore the complexity of various brain regions in the three groups. At the same time, the correlation between PE value and scale's score in PD-Dep group were analyzed.Results Age, gender, education and MMSE score showed no significant differences among the three groups (P>0.05). HAMD score in the PD-Dep group was significantly higher than that in the other two groups (P<0.01). PE value showed significant differences in the right inferior temporal gyrus, left anterior cingulate and right median cingulate gyrus among the three groups. PE values of PD-Dep group were increased in the right median cingulate gyrus than those of PD-NDep group (P=0.007). PE values of PD-Dep group were increased in the right inferior temporal gyrus than those of HCs group (P=0.022). PE values of PD-Dep group were decreased in the left anterior cingulate gyrus than those of HCs group (P=0.007). PE values of PD-NDep group were increased in the right inferior temporal gyrus than those of HCs group (P=0.004). The PE values of PD-NDep group were decreased in the left anterior cingulate and right median cingulate gyrus than those of HCs group (P<0.01, P=0.019). In addition, the HAMD score was significantly correlated with the PE value of the right median cingulate gyrus (P<0.01, r=0.790).Conclusions Permutation entropy can reflect the pathophysiological process of brain complexity changes in patients with PD-Dep. PE value in the right median cingulate gyrus may be an important indicator for evaluating disease progression. Permutation entropy may help provide reference information for early diagnosis, treatment and curative effect evaluation.
[Keywords] Parkinson's disease;depression;functional magnetic resonance imaging;permutation entropy;complexity;functional brain imaging;blood oxygen level dependent;pathological mechanism

LI Haidong   WANG Jun   NIU Jinliang*  

Department of Magnetic Resonance Imaging, the Second Hospital of Shanxi Medical University, Taiyuan 030001, China

Niu JL, E-mail:

Conflicts of interest   None.

Received  2022-03-01
Accepted  2022-07-06
DOI: 10.12015/issn.1674-8034.2022.07.016
Cite this article as: Li HD, Wang J, Niu JL. Brain complexity in the patients of Parkinson's disease with depression: a resting-state functional magnetic resonance imaging study[J]. Chin J Magn Reson Imaging, 2022, 13(7): 90-95.DOI:10.12015/issn.1674-8034.2022.07.016

Mason AR, Ziemann A, Finkbeiner S. Targeting the low-hanging fruit of neurodegeneration[J]. Neurology, 2014, 83(16): 1470-1473. DOI: 10.1212/WNL.0000000000000894.
Even C, Weintraub D. Is depression in Parkinson's disease (PD) a specific entity?[J]. J Affect Disord, 2012, 139(2): 103-112. DOI: 10.1016/j.jad.2011.07.002.
van der Hoek TC, Bus BA, Matui P, et al. Prevalence of depression in Parkinson's disease: effects of disease stage, motor subtype and gender[J]. J Neurol Sci, 2011, 310(1/2): 220-224. DOI: 10.1016/j.jns.2011.07.007.
Ni HJ, Song ZJ, Liang L, et al. Decreased resting-state functional complexity in elderly with subjective cognitive decline[J]. Entropy (Basel), 2021, 23(12): 1591. DOI: 10.3390/e23121591.
Aftanas LI, Lotova NV, Koshkarov VI, et al. Non-linear analysis of emotion EEG: calculation of Kolmogorov entropy and the principal Lyapunov exponent[J]. Neurosci Lett, 1997, 226(1): 13-16. DOI: 10.1016/s0304-3940(97)00232-2.
Shannon CE. The mathematical theory of communication. 1963[J]. MD Comput, 1997, 14(4): 306-317.
Ouyang GX, Li J, Liu XZ, et al. Dynamic characteristics of absence EEG recordings with multiscale permutation entropy analysis[J]. Epilepsy Res, 2013, 104(3): 246-252. DOI: 10.1016/j.eplepsyres.2012.11.003.
Ferlazzo E, Mammone N, Cianci V, et al. Permutation entropy of scalp EEG: a tool to investigate epilepsies: suggestions from absence epilepsies[J]. Clin Neurophysiol, 2014, 125(1): 13-20. DOI: 10.1016/j.clinph.2013.06.023.
Shi L, Beaty RE, Chen QL, et al. Brain entropy is associated with divergent thinking[J]. Cereb Cortex, 2020, 30(2): 708-717. DOI: 10.1093/cercor/bhz120.
Li K, Zhao H, Li CM, et al. The relationship between side of onset and cerebral regional homogeneity in Parkinson's disease: a resting-state fMRI study[J/OL]. Parkinsons Dis, 2020 [2022-03-01]. DOI: 10.1155/2020/5146253.
Liao HY, Yi JY, Cai SN, et al. Changes in degree centrality of network nodes in different frequency bands in Parkinson's disease with depression and without depression[J/OL]. Front Neurosci, 2021 [2022-03-01]. DOI: 10.3389/fnins.2021.638554.
Parkinson's Disease and Movement Disorders Study Group, Neurology Branch of Chinese Medical Association, Parkinson's disease and Movement Disorders Professional Committee of neurophysicians branch of Chinese Medical Association. Diagnostic criteria of Parkinson's disease in China[J]. Chin J Urol, 2016, 49(4): 268‐271. DOI: 10.3760/cma.j.issn.1006‐7876.2016.04.002.
Starkstein S, Dragovic M, Jorge R, et al. Diagnostic criteria for depression in Parkinson's disease: a study of symptom patterns using latent class analysis[J]. Mov Disord, 2011, 26(12): 2239-2245. DOI: 10.1002/mds.23836.
Bandt C, Pompe B. Permutation entropy: a natural complexity measure for time series[J/OL]. Phys Rev Lett, 2002 [2022-03-01]. DOI: 10.1103/PhysRevLett.88.174102.
Lo Giudice M, Varone G, Ieracitano C, et al. Permutation entropy-based interpretability of convolutional neural network models for interictal EEG discrimination of subjects with epileptic seizures vs. psychogenic non-epileptic seizures[J]. Entropy (Basel), 2022, 24(1): 102. DOI: 10.3390/e24010102.
Yan CG, Zang YF. DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI[J]. Front Syst Neurosci, 2010, 4: 13. DOI: 10.3389/fnsys.2010.00013.
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain[J]. Neuroimage, 2002, 15(1): 273-289. DOI: 10.1006/nimg.2001.0978.
Zhou MH, Jiang WY, Zhong D, et al. Resting-state brain entropy in right temporal lobe epilepsy and its relationship with alertness[J]. Brain Behav, 2019, 9(11): e01446. DOI: 10.1002/brb3.1446.
Zanin M, Zunino L, Rosso OA, et al. Permutation entropy and its main biomedical and econophysics applications: a review[J]. Entropy, 2012, 14(8): 1553-1577. DOI: 10.3390/e14081553.
Pincus SM. Approximate entropy as a measure of system complexity[J]. Proc Natl Acad Sci USA, 1991, 88(6): 2297-2301. DOI: 10.1073/pnas.88.6.2297.
Richman JS, Moorman JR. Physiological time-series analysis using approximate entropy and sample entropy[J]. Am J Physiol Heart Circ Physiol, 2000, 278(6): H2039-H2049. DOI: 10.1152/ajpheart.2000.278.6.H2039.
Li J, Yan JQ, Liu XZ, et al. Using permutation entropy to measure the changes in EEG signals during absence seizures[J]. Entropy, 2014, 16(6): 3049-3061. DOI: 10.3390/e16063049.
Xiang J, Tan Y, Niu Y, et al. Analysis of functional MRI signal complexity based on permutation fuzzy entropy in bipolar disorder[J]. Neuroreport, 2021, 32(6): 465-471. DOI: 10.1097/WNR.0000000000001617.
Wohlschläger A, Karne H, Jordan D, et al. Spectral dynamics of resting state fMRI within the ventral tegmental area and dorsal raphe nuclei in medication-free major depressive disorder in young adults[J]. Front Psychiatry, 2018, 9: 163. DOI: 10.3389/fpsyt.2018.00163.
Wang B, Niu Y, Miao LW, et al. Decreased complexity in Alzheimer's disease: resting-state fMRI evidence of brain entropy mapping[J]. Front Aging Neurosci, 2017, 9: 378. DOI: 10.3389/fnagi.2017.00378.
Lee H, Huang ZR, Liu XL, et al. Topographic reconfiguration of local and shared information in anesthetic-induced unconsciousness[J]. Entropy (Basel), 2018, 20(7): 518. DOI: 10.3390/e20070518.
Chang D, Song DH, Zhang J, et al. Caffeine caused a widespread increase of resting brain entropy[J]. Sci Rep, 2018, 8(1): 2700. DOI: 10.1038/s41598-018-21008-6.
Xue SW, Yu QB, Guo YH, et al. Resting-state brain entropy in schizophrenia[J]. Compr Psychiatry, 2019, 89: 16-21. DOI: 10.1016/j.comppsych.2018.11.015.
Grotheer M, Jeska B, Grill-Spector K. A preference for mathematical processing outweighs the selectivity for Arabic numbers in the inferior temporal gyrus[J]. NeuroImage, 2018, 175: 188-200. DOI: 10.1016/j.neuroimage.2018.03.064.
Teo R, Dhanasekaran P, Tay SH, et al. Mathematical processing is affected by daily but not cumulative glucocorticoid dose in patients with systemic lupus erythematosus[J]. Rheumatology (Oxford), 2020, 59(9): 2534-2543. DOI: 10.1093/rheumatology/keaa002.
Olson IR, Plotzker A, Ezzyat Y. The Enigmatic temporal pole: a review of findings on social and emotional processing[J]. Brain, 2007, 130(Pt 7): 1718-1731. DOI: 10.1093/brain/awm052.
Li W, Cui HR, Zhu ZP, et al. Aberrant functional connectivity between the amygdala and the temporal pole in drug-free generalized anxiety disorder[J]. Front Hum Neurosci, 2016, 10: 549. DOI: 10.3389/fnhum.2016.00549.
Liao HY, Cai SN, Shen Q, et al. Networks are associated with depression in patients with Parkinson's disease: a resting-state imaging study[J]. Front Neurosci, 2021, 14: 573538. DOI: 10.3389/fnins.2020.573538.
Qiu YH, Huang ZH, Gao YY, et al. Alterations in intrinsic functional networks in Parkinson's disease patients with depression: a resting-state functional magnetic resonance imaging study[J]. CNS Neurosci Ther, 2021, 27(3): 289-298. DOI: 10.1111/cns.13467.
Braak H, del Tredici K, Rüb U, et al. Staging of brain pathology related to sporadic Parkinson's disease[J]. Neurobiol Aging, 2003, 24(2): 197-211. DOI: 10.1016/s0197-4580(02)00065-9.
Shao XJ, Zhu G. Associations among monoamine neurotransmitter pathways, personality traits, and major depressive disorder[J]. Front Psychiatry, 2020, 11: 381. DOI: 10.3389/fpsyt.2020.00381.
Zhang YY, Cui XL, Ou YP, et al. Differentiating melancholic and non-melancholic major depressive disorder using fractional amplitude of low-frequency fluctuations[J]. Front Psychiatry, 2021, 12: 763770. DOI: 10.3389/fpsyt.2021.763770.
Qiu J, Wang BX, Wang L, et al. Research on regional homogeneity of resting state functional magnetic resonance imaging in first-episode depressive disorder patients[J]. Chin J Magn Reson Imaging, 2020, 11(9): 721-725. DOI: 10.12015/issn.1674-8034.2020.09.001.
Uhr L, Tsolaki E, Pouratian N. Diffusion tensor imaging correlates of depressive symptoms in Parkinson disease[J]. J Comp Neurol, 2022, 530(10): 1729-1738. DOI: 10.1002/cne.25310.
Nakano T, Kajiyama Y, Revankar GS, et al. Neural networks associated with quality of life in patients with Parkinson's disease[J]. Parkinsonism Relat Disord, 2021, 89: 6-12. DOI: 10.1016/j.parkreldis.2021.06.007.
Sun JF, Chen LM, He JK, et al. Altered brain function in first-episode and recurrent depression: a resting-state functional magnetic resonance imaging study[J]. Front Neurosci, 2022, 16: 876121. DOI: 10.3389/fnins.2022.876121.
Zhang XL, Cao X, Xue C, et al. Aberrant functional connectivity and activity in Parkinson's disease and comorbidity with depression based on radiomic analysis[J]. Brain Behav, 2021, 11(5): e02103. DOI: 10.1002/brb3.2103.

PREV Abnormal degree centrality values in the frontotemporal lobe, cerebellum and sensorimotor regions are associated with gait freezing in Parkinson,s patients
NEXT Application value of T2WI-Dixon water fat separation sequence in the evaluation of muscle fat infiltration and edema in patient with Duchenne muscular dystrophy

Tel & Fax: +8610-67113815    E-mail: