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Abnormal spontaneous neural activity of brain regions in patients with primary blepharospasm at rest

      Highlights

      • Spontaneous neural activity in patients with BSP was investigated by resting-state fMRI.
      • We found abnormal activity in multiple cortical regions that go beyond the basal ganglia.
      • These findings support the emerging view for involvement of multiple brain regions.

      Abstract

      Background

      Primary blepharospasm (BSP) is characterized by excessive involuntary eyelid spasms without significant morphological brain abnormalities. Its neural bases remain unclear. Resting-state functional magnetic resonance imaging (rs-fMRI) is a powerful tool for exploring cerebral function mechanisms in BSP.

      Methods

      Two subject groups (24 patients with BSP and 24 healthy controls) underwent rs-fMRI scans. The rs-fMRI images were analyzed using the regional homogeneity (ReHo) method to assess the local features of spontaneous brain activity. Correlation analysis was carried out to explore the relationship between the ReHo values of abnormal brain areas and clinical variables including illness duration, symptom severity, and depression/anxiety symptoms.

      Results

      Relative to healthy controls, patients with BSP showed significantly decreased ReHo in the left superior temporal pole/left insula, left calcarine cortex, and bilateral superior medial frontal gyrus (mSFG), and increased ReHo in the bilateral supplementary motor area (SMA). There were no significant correlations between ReHo values in these brain regions and clinical variables in the patients.

      Conclusions

      Our results suggest that abnormal spontaneous brain activity in multiple brain regions not limited to the basal ganglia may be trait alterations in the patients, which provides more insights into the pathogenesis of BSP.

      Keywords

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      References

        • Valls-Sole J.
        • Defazio G.
        Blepharospasm: update on epidemiology, clinical aspects, and pathophysiology.
        Front. Neurol. 2016; 7: 45
        • Defazio G.
        • et al.
        Blepharospasm 40 years later.
        Mov. Disord. 2017; 32: 498-509
        • Stamelou M.
        • et al.
        The non-motor syndrome of primary dystonia: clinical and pathophysiological implications.
        Brain. 2012; (Pt 6): 1668-1681
        • Kuyper D.J.
        • et al.
        Nonmotor manifestations of dystonia: a systematic review.
        Mov. Disord. 2011; 26: 1206-1217
        • Neychev V.K.
        • et al.
        The functional neuroanatomy of dystonia.
        Neurobiol. Dis. 2011; 42: 185-201
        • Jinnah H.A.
        • Neychev V.
        • Hess E.J.
        The anatomical basis for dystonia: the motor network model.
        Tremor Other Hyperkinet Mov. (N Y). 2017; 7: 506
        • Zhou B.
        • et al.
        A resting state functional magnetic resonance imaging study of patients with benign essential blepharospasm.
        J. Neuroophthalmol. 2013; 33: 235-240
        • Horovitz S.G.
        • et al.
        Anatomical correlates of blepharospasm.
        Transl. Neurodegener. 2012; 1: 12
        • Fabbrini G.
        • et al.
        Cranial movement disorders: clinical features, pathophysiology, differential diagnosis and treatment.
        Nat. Clin. Pract. Neurol. 2009; 5: 93-105
        • Martino D.
        • et al.
        Cortical gray matter changes in primary blepharospasm: a voxel-based morphometry study.
        Mov. Disord. 2011; 26: 1907-1912
        • Baker R.S.
        • et al.
        A functional magnetic resonance imaging study in patients with benign essential blepharospasm.
        J. Neuroophthalmol. 2003; 23: 11-15
        • Dresel C.
        • et al.
        Silent event-related fMRI reveals deficient motor and enhanced somatosensory activation in orofacial dystonia.
        Brain. 2006; (Pt 1): 36-46
        • Ni M.F.
        • et al.
        Resting state fMRI observations of baseline brain functional activities and connectivities in primary blepharospasm.
        Neurosci. Lett. 2017; 660: 22-28
        • Schmidt K.E.
        • et al.
        Striatal activation during blepharospasm revealed by fMRI.
        Neurology. 2003; 60: 1738-1743
        • Biswal B.B.
        Resting state fMRI: a personal history.
        Neuroimage. 2012; 62: 938-944
        • Biswal B.
        • et al.
        Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.
        Magn. Reson. Med. 1995; 34: 537-541
        • Zang Y.
        • et al.
        Regional homogeneity approach to fMRI data analysis.
        Neuroimage. 2004; 22: 394-400
        • Guo W.B.
        • et al.
        Abnormal neural activities in first-episode, treatment-naive, short-illness-duration, and treatment-response patients with major depressive disorder: a resting-state fMRI study.
        J. Affect. Disord. 2011; 135: 326-331
        • Guo W.B.
        • et al.
        Disrupted regional homogeneity in treatment-resistant depression: a resting-state fMRI study.
        Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 2011; 35: 1297-1302
        • Song Y.
        • et al.
        Abnormal regional homogeneity and its correlations with personality in first-episode, treatment-naive somatization disorder.
        Int. J. Psychophysiol. 2015; 97: 108-112
        • Wang S.
        • et al.
        Abnormal regional homogeneity as potential imaging biomarker for psychosis risk syndrome: a resting-state fMRI study and support vector machine analysis.
        Sci. Rep. 2016; 627619
        • Wang S.
        • et al.
        Abnormal regional homogeneity as a potential imaging biomarker for adolescent-onset schizophrenia: a resting-state fMRI study and support vector machine analysis.
        Schizophr. Res. 2018; 192: 179-184
        • Yang T.
        • et al.
        Altered spontaneous activity in treatment-naive childhood absence epilepsy revealed by regional homogeneity.
        J. Neurol. Sci. 2014; 340: 58-62
        • Choe I.H.
        • et al.
        Decreased and increased cerebral regional homogeneity in early Parkinson's disease.
        Brain Res. 2013; 1527: 230-237
        • Hallett M.
        • et al.
        Update on blepharospasm: report from the BEBRF international workshop.
        Neurology. 2008; 71: 1275-1282
        • Lindeboom R.
        • et al.
        The blepharospasm disability scale: an instrument for the assessment of functional health in blepharospasm.
        Mov. Disord. 1995; 10: 444-449
        • Chao-Gan Y.
        • Yu-Feng Z.
        DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI.
        Front. Syst. Neurosci. 2010; 4: 13
        • Avanzino L.
        • et al.
        Sensory-motor integration in focal dystonia.
        Neuropsychologia. 2015; 79: 288-300
        • Patel N.
        • et al.
        Alleviating manoeuvres (sensory tricks) in cervical dystonia.
        J. Neurol. Neurosurg. Psychiatry. 2014; 85: 882-884
        • Naumann M.
        • et al.
        Sensory tricks in cervical dystonia: perceptual dysbalance of parietal cortex modulates frontal motor programming.
        Ann. Neurol. 2000; 47: 322-328
        • Tinazzi M.
        • et al.
        Sensory functions in dystonia: insights from behavioral studies.
        Mov. Disord. 2009; 24: 1427-1436
        • Perruchoud D.
        • et al.
        Focal dystonia and the sensory-motor integrative loop for enacting (SMILE).
        Front. Hum. Neurosci. 2014; 8: 458
        • Wolpert D.M.
        • Ghahramani Z.
        • Jordan M.I.
        An internal model for sensorimotor integration.
        Science. 1995; 269: 1880-1882
        • Cuny E.
        • et al.
        Sensory motor mismatch within the supplementary motor area in the dystonic monkey.
        Neurobiol. Dis. 2008; 30: 151-161
        • Blood A.J.
        Imaging studies in focal dystonias: a systems level approach to studying a systems level disorder.
        Curr. Neuropharmacol. 2013; 11: 3-15
        • Gogolla N.
        The insular cortex.
        Curr. Biol. 2017; 27: R580-R586
        • Gasquoine P.G.
        Contributions of the insula to cognition and emotion.
        Neuropsychol. Rev. 2014; 24: 77-87
        • Mutschler I.
        • et al.
        Functional organization of the human anterior insular cortex.
        Neurosci. Lett. 2009; 457: 66-70
        • Ghaziri J.
        • et al.
        The corticocortical structural connectivity of the human insula.
        Cereb. Cortex. 2017; 27: 1216-1228
        • Hanakawa T.
        • Dimyan M.A.
        • Hallett M.
        Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI.
        Cereb. Cortex. 2008; 18: 2775-2788
        • Johnson J.J.
        • et al.
        The role of nonmotor brain regions during human motor control.
        Conf. Proc. IEEE Eng. Med. Biol. Soc. 2017; 2017: 2498-2501
        • Shelley B.P.
        • Trimble M.R.
        The insular lobe of Reil—its anatamico-functional, behavioural and neuropsychiatric attributes in humans—a review.
        World J. Biol. Psychiatr. 2004; 5: 176-200
        • Hall T.A.
        • et al.
        Health-related quality of life and psychosocial characteristics of patients with benign essential blepharospasm.
        Arch. Ophthalmol. 2006; 124: 116-119
        • Moraru E.
        • et al.
        Relation between depression and anxiety in dystonic patients: implications for clinical management.
        Depress. Anxiety. 2002; 16: 100-103
        • Friedrich M.J.
        Depression is the leading cause of disability around the world.
        Jama. 2017; 317: 1517
        • Smith R.
        • Fass H.
        • Lane R.D.
        Role of medial prefrontal cortex in representing one's own subjective emotional responses: a preliminary study.
        Conscious. Cogn. 2014; 29: 117-130
        • Guo W.
        • et al.
        Increased anterior default-mode network homogeneity in first-episode, drug-naive major depressive disorder: a replication study.
        J. Affect. Disord. 2018; 225: 767-772
        • du Boisgueheneuc F.
        • et al.
        Functions of the left superior frontal gyrus in humans: a lesion study.
        Brain. 2006; (Pt 12): 3315-3328
        • Yang J.
        • et al.
        Screening for cognitive impairments in primary blepharospasm.
        PLoS ONE. 2016; 11 (p. e0160867)
        • Smith S.M.
        • et al.
        Correspondence of the brain's functional architecture during activation and rest.
        Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 13040-13045
        • Filip P.
        • et al.
        Disruption in cerebellar and basal ganglia networks during a visuospatial task in cervical dystonia.
        Mov. Disord. 2017; 32: 757-768
        • Molloy A.
        • et al.
        Sun exposure is an environmental factor for the development of blepharospasm.
        J. Neurol. Neurosurg. Psychiatry. 2016; 87: 420-424
        • Defazio G.
        • et al.
        Environmental risk factors and clinical phenotype in familial and sporadic primary blepharospasm.
        Neurology. 2011; 77: 631-637
        • Draganski B.
        • et al.
        "Motor circuit" gray matter changes in idiopathic cervical dystonia.
        Neurology. 2003; 61: 1228-1231
        • Jochim A.
        • et al.
        Altered functional connectivity in blepharospasm/orofacial dystonia.
        Brain Behav. 2018; 8e00894