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Patterns of intrinsic brain activity in essential tremor with resting tremor and tremor-dominant Parkinson’s disease

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Abstract

The clinical pictures of essential tremor (ET) with resting tremor (rET) and tremor-dominant Parkinson’s disease (tPD) are often quite mimic at the early stage, current approaches to the diagnosis and treatment therefore remain challenging. The regional homogeneity (ReHo) method under resting-state functional magnetic resonance imaging (rs-fMRI) would help exhibit the patterns in neural activity, which further contribute to differentiate these disorders and explore the relationship between symptoms and regional functional abnormalities. Sixty-eight Chinese participants were recruited, including 19 rET patients, 24 tPD patients and 25 age- and gender-matched healthy controls (HCs). All participants underwent clinical assessment and rs-fMRI with a ReHo method to investigate the alterations of neural activity, and the correlation between them. Differences were compared by two-sample t-test (corrected with AlphaSim, p < 0.05). Compared with HCs, patients’ groups both displayed decreased ReHo in the default mode network (DMN), bilateral putamen and bilateral cerebellum. While tPD patients specifically exihibited decreased ReHo in the bilateral supplementary motor area (SMA) and precentral gyrus (M1). The correlation analysis revealed that ReHo in the bilateral putamen, right SMA and left cerebellum_crus I were negatively correlated with the UPDRS-III score, respectively, in tPD group. Our results indicated the rET patients may share part of the pathophysiological mechanism of tPD patients. In addition, we found disorder-specific involvement of the SMA and M1 in tPD. Such a distinction may lend itself to use as a potential biomarker for differentiating between these two diseases.

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References

  • Agosta, F., Pievani, M., Geroldi, C., Copetti, M., Frisoni, G. B., & Filippi, M. (2012). Resting state fMRI in Alzheimer's disease: beyond the default mode network. Neurobiology of Aging, 33, 1564–1578.

    PubMed  Google Scholar 

  • Alon, G., Yungher, D. A., Shulman, L. M., & Rogers, M. W. (2012). Safety and immediate effect of noninvasive transcranial pulsed current stimulation on gait and balance in Parkinson disease. Neurorehabilitation and Neural Repair, 26, 1089–1095.

    PubMed  Google Scholar 

  • Barbagallo, G., Arabia, G., Morelli, M., Nistico, R., Novellino, F., Salsone, M., et al. (2017). Thalamic neurometabolic alterations in tremulous Parkinson's disease: A preliminary proton MR spectroscopy study. Parkinsonism & Related Disorders, 43, 78–84.

    Google Scholar 

  • Benito-Leon, J., & Louis, E. D. (2006). Essential tremor: emerging views of a common disorder. Nature Clinical Practice. Neurology, 2, 666–678.

    PubMed  Google Scholar 

  • Benito-Leon, J., Louis, E. D., Bermejo-Pareja, F., & Neurological Disorders in Central Spain Study G. (2009). Risk of incident Parkinson's disease and parkinsonism in essential tremor: a population based study. Journal of Neurology, Neurosurgery, and Psychiatry, 80, 423–425.

    CAS  PubMed  Google Scholar 

  • Benito-Leon, J., Louis, E. D., Romero, J. P., Hernandez-Tamames, J. A., Manzanedo, E., Alvarez-Linera, J., et al. (2015). Altered Functional Connectivity in Essential Tremor: A Resting-State fMRI Study. Medicine, 94, e1936.

    PubMed  PubMed Central  Google Scholar 

  • Benninger, D. H., Thees, S., Kollias, S. S., Bassetti, C. L., & Waldvogel, D. (2009). Morphological differences in Parkinson's disease with and without rest tremor. Journal of Neurology, 256, 256–263.

    PubMed  Google Scholar 

  • Bhatia, K. P., & Marsden, C. D. (1994). The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain, 117(Pt 4), 859–876.

    PubMed  Google Scholar 

  • Brooks, D. J., Ibanez, V., Sawle, G. V., Quinn, N., Lees, A. J., Mathias, C. J., et al. (1990). Differing patterns of striatal 18F-dopa uptake in Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Annals of Neurology, 28, 547–555.

    CAS  PubMed  Google Scholar 

  • Caligiuri, M. E., Arabia, G., Barbagallo, G., Lupo, A., Morelli, M., Nistico, R., et al. (2017). Structural connectivity differences in essential tremor with and without resting tremor. Journal of Neurology, 264, 1865–1874.

    CAS  PubMed  Google Scholar 

  • Cherubini, A., Nistico, R., Novellino, F., Salsone, M., Nigro, S., Donzuso, G., et al. (2014). Magnetic resonance support vector machine discriminates essential tremor with rest tremor from tremor-dominant Parkinson disease. Movement Disorders, 29, 1216–1219.

    PubMed  Google Scholar 

  • Cohen, O., Pullman, S., Jurewicz, E., Watner, D., & Louis, E. D. (2003). Rest tremor in patients with essential tremor: prevalence, clinical correlates, and electrophysiologic characteristics. Archives of Neurology, 60, 405–410.

    PubMed  Google Scholar 

  • Deuschl, G., Bain, P., & Brin, M. (1998). Consensus statement of the Movement Disorder Society on Tremor. Ad Hoc Scientific Committee. Mov Disord, 13(Suppl 3), 2–23.

    PubMed  Google Scholar 

  • Drew, T., Prentice, S., & Schepens, B. (2004). Cortical and brainstem control of locomotion. Progress in Brain Research, 143, 251–261.

    PubMed  Google Scholar 

  • Fang, W., Lv, F., Luo, T., Cheng, O., Liao, W., Sheng, K., et al. (2013). Abnormal regional homogeneity in patients with essential tremor revealed by resting-state functional MRI. PLoS One, 8, e69199.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang, W. D., Chen, H. Y., Wang, H. S., Zhang, H., Liu, M. Q., Puneet, M., et al. (2015). Multiple Resting-State Networks Are Associated With Tremors and Cognitive Features in Essential Tremor. Movement Disorders, 30, 1926–1936.

    PubMed  Google Scholar 

  • Gerasimou, G., Costa, D. C., Papanastasiou, E., Bostanjiopoulou, S., Arnaoutoglou, M., Moralidis, E., et al. (2012). SPECT study with I-123-Ioflupane (DaTSCAN) in patients with essential tremor. Is there any correlation with Parkinson's disease? Annals of Nuclear Medicine, 26, 337–344.

    CAS  PubMed  Google Scholar 

  • Goetz, C. G., Tilley, B. C., Shaftman, S. R., Stebbins, G. T., Fahn, S., Martinez-Martin, P., et al. (2008). Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Movement Disorders, 23, 2129–2170.

    PubMed  Google Scholar 

  • Hamada, M., Ugawa, Y., Tsuji, S., & Effectiveness r TMSPD. (2009). High-frequency rTMS over the supplementary motor area improves bradykinesia in Parkinson's disease: Subanalysis of double-blind sham-controlled study. Journal of the Neurological Sciences, 287, 143–146.

    PubMed  Google Scholar 

  • Helmich, R. C., Hallett, M., Deuschl, G., Toni, I., & Bloem, B. R. (2012). Cerebral causes and consequences of parkinsonian resting tremor: a tale of two circuits? Brain, 135, 3206–3226.

    PubMed  PubMed Central  Google Scholar 

  • Hoehn, M. M., & Yahr, M. D. (2001). Parkinsonism: onset, progression, and mortality (Reprinted from Neurology, vol 17, 1967). Neurology, 57, S11–S26.

    CAS  PubMed  Google Scholar 

  • Hughes, A. J., Daniel, S. E., Kilford, L., & Lees, A. J. (1992). ACCURACY OF CLINICAL-DIAGNOSIS OF IDIOPATHIC PARKINSONS-DISEASE - A CLINICOPATHOLOGICAL STUDY OF 100 CASES. Journal of Neurology, Neurosurgery, and Psychiatry, 55, 181–184.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain, S., Lo, S. E., & Louis, E. D. (2006). Common misdiagnosis of a common neurological disorder - How are we misdiagnosing essential tremor? Archives of Neurology, 63, 1100–1104.

    PubMed  Google Scholar 

  • Katzman, R., Zhang, M. Y., Ouangyaqu, W. Z. Y., Liu, W. T., Yu, E., et al. (1988). A chinese version of the mini-mental state examination - impact of illiteracy in a Shanghai Dementia survey. Journal of Clinical Epidemiology, 41, 971–978.

    CAS  PubMed  Google Scholar 

  • Lefaucheur, J. P. (2005). Motor cortex dysfunction revealed by cortical excitability studies in Parkinson's disease: influence of antiparkinsonian treatment and cortical stimulation. Clinical Neurophysiology, 116, 244–253.

    CAS  PubMed  Google Scholar 

  • Louis, E. D. (2005). Essential tremor. The Lancet. Neurology, 4, 100–110.

    PubMed  Google Scholar 

  • Mure, H., Hirano, S., Tang, C. C., Isaias, I. U., Antonini, A., Ma, Y., et al. (2011). Parkinson's disease tremor-related metabolic network: characterization, progression, and treatment effects. Neuroimage, 54, 1244–1253.

    PubMed  Google Scholar 

  • Nicoletti, V., Cecchi, P., Frosini, D., Pesaresi, I., Fabbri, S., Diciotti, S., et al. (2015). Morphometric and functional MRI changes in essential tremor with and without resting tremor. Journal of Neurology, 262, 719–728.

    PubMed  Google Scholar 

  • Nistico, R., Pirritano, D., Salsone, M., Novellino, F., Del Giudice, F., Morelli, M., et al. (2011). Synchronous pattern distinguishes resting tremor associated with essential tremor from rest tremor of Parkinson's disease. Parkinsonism & Related Disorders, 17, 30–33.

    CAS  Google Scholar 

  • Novellino, F., Nicoletti, G., Cherubini, A., Caligiuri, M. E., Nistico, R., Salsone, M., et al. (2016). Cerebellar involvement in essential tremor with and without resting tremor: A Diffusion Tensor Imaging study. Parkinsonism & Related Disorders, 27, 61–66.

    Google Scholar 

  • Oldfield, R. C. (1971). THE ASSESSMENT AND ANALYSIS OF HANDEDNESS: THE EDINBURGH INVENTORY. Neuropsychologia, 9, 97–113.

    CAS  PubMed  Google Scholar 

  • Pollok, B., Gross, J., Dirks, M., Timmermann, L., & Schnitzler, A. (2004). The cerebral oscillatory network of voluntary tremor. Journal of Physiology (London), 554, 871–878.

    CAS  Google Scholar 

  • Puertas-Martin V, Villarejo-Galende A, Fernandez-Guinea S, Romero JP, Louis ED, Benito-Leon J. 2016. A Comparison Study of Cognitive and Neuropsychiatric Features of Essential Tremor and Parkinson's Disease. Tremor and other hyperkinetic movements (New York, N.Y.) 6: 431.

  • Sadigh-Eteghad, S., Majdi, A., Farhoudi, M., Talebi, M., & Mahmoudi, J. (2014). Different patterns of brain activation in normal aging and Alzheimer's disease from cognitional sight: meta analysis using activation likelihood estimation. Journal of the Neurological Sciences, 343, 159–166.

    PubMed  Google Scholar 

  • Sambataro, F., Murty, V. P., Callicott, J. H., Tan, H. Y., Das, S., Wwinberger, D. R., et al. (2010). Age-related alterations in default mode network: impact on working memory performance. Neurobiology of Aging, 31, 839–852.

    PubMed  Google Scholar 

  • Sanchez-Ferro, A., Benito-Leon, J., Louis, E. D., Contador, I., Hernandez-Gallego, J., Puertas-Martin, V., et al. (2017). Cognition in non-demented Parkinson's disease vs essential tremor: A population-based study. Acta Neurologica Scandinavica, 136, 393–400.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schepens, B., Stapley, P., & Drew, T. (2008). Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. Journal of Neurophysiology, 100, 2235–2253.

    PubMed  Google Scholar 

  • Sharifi, S., Nederveen, A. J., Booij, J., & van Rootselaar, A. F. (2014). Neuroimaging essentials in essential tremor: a systematic review. NeuroImage Clinical, 5, 217–231.

    PubMed  PubMed Central  Google Scholar 

  • Stebbins, G. T., Goetz, C. G., Burn, D. J., Jankovic, J., Khoo, T. K., & Tilley, B. C. (2013). How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson's disease rating scale: Comparison with the unified Parkinson's disease rating scale. Movement Disorders, 28, 668–670.

    PubMed  Google Scholar 

  • Su, M. L., Wang, S., Fang, W. D., Zhu, Y. C., Li, R., et al. (2015). Alterations in the limbic/paralimbic cortices of Parkinson's disease patients with hyposmia under resting-state functional MRI by regional homogeneity and functional connectivity analysis. Parkinsonism & Related Disorders, 21, 698–703.

    Google Scholar 

  • Tessitore, A., Esposito, F., Vitale, C., Santangelo, G., Amboni, M., Russo, A., et al. (2012). Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology, 79, 2226–2232.

    PubMed  Google Scholar 

  • Wang, Y., Zhao, X., Xu, S., Yu, L., Wang, L., Song, M., et al. (2015). Using regional homogeneity to reveal altered spontaneous activity in patients with mild cognitive impairment. BioMed Research International, 2015, 807093.

    PubMed  PubMed Central  Google Scholar 

  • Wu, T., Long, X., Zang, Y., Wang, L., Hallett, M., Li, K., et al. (2009). Regional homogeneity changes in patients with Parkinson's disease. Human Brain Mapping, 30, 1502–1510.

    PubMed  Google Scholar 

  • Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016). DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics, 14, 339–351.

    PubMed  Google Scholar 

  • Yang, H., Zhou, X. J., Zhang, M. M., Zheng, X. N., Zhao, Y. L., & Wang, J. (2013). Changes in spontaneous brain activity in early Parkinson's disease. Neuroscience Letters, 549, 24–28.

    CAS  PubMed  Google Scholar 

  • Yoon, J. H., Kim, M. S., Lee, S. M., Kim, H. J., & Hong, J. M. (2016). Heart rate variability to differentiate essential tremor from early-stage tremor-dominant Parkinson's disease. Journal of the Neurological Sciences, 368, 55–58.

    PubMed  Google Scholar 

  • Zang, Y. F., Jiang, T. Z., Lu, Y. L., He, Y., & Tian, L. X. (2004). Regional homogeneity approach to fMRI data analysis. Neuroimage, 22, 394–400.

    PubMed  Google Scholar 

  • Zhang, M. Y., Katzman, R., Salmon, D., Jin, H., Cai, G. J., Wang, Z. Y., et al. (1990). The prevalence of dementia and alzheimers-disease In Shanghai, China - impact of age, gender, and education. Annals of Neurology, 27, 428–437.

    CAS  PubMed  Google Scholar 

  • Zhang, J., Wei, L., Hu, X., Xie, B., Zhang, Y., Wu, G. R., et al. (2015). Akinetic-rigid and tremor-dominant Parkinson's disease patients show different patterns of intrinsic brain activity. Parkinsonism & Related Disorders, 21, 23–30.

    Google Scholar 

  • Zuo, X.-N., Xu, T., Jiang, L., Yang, Z., Cao, X.-Y., He, Y., et al. (2013). Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space. Neuroimage, 65, 374–386.

    PubMed  Google Scholar 

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Acknowledgements

We thank all the patients who participated in this study and are grateful to the Department of Neurology at the West China Hospital for their support of this work. We also gratefully acknowledge Professor Dong Zhou, Li He, Guanggu Yuan and all staffs in the laboratory for their help.

Funding

The study was supported by the National Natural Science Foundation of China (81801272), China Postdoctoral Science Foundation (2017 M610605), Sichuan Science and Technology Program (2018FZ0029 and 2018HH0077), The Fundamental Research Funds for the Central Universities (2018SCU12029), and Post-Doctor Research Project, West China Hospital, Sichuan University (2018HXBH085).

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Correspondence to Rong Peng.

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Li, Jy., Lu, Zj., Suo, Xl. et al. Patterns of intrinsic brain activity in essential tremor with resting tremor and tremor-dominant Parkinson’s disease. Brain Imaging and Behavior 14, 2606–2617 (2020). https://doi.org/10.1007/s11682-019-00214-4

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