White Matter Microstructure of the Cerebellar Peduncles Is Associated with Balance Performance during Sensory Re-Weighting in People with Multiple Sclerosis.
Adolescent
Adult
Aged
Aged, 80 and over
Cerebellum
/ diagnostic imaging
Diffusion Magnetic Resonance Imaging
Disability Evaluation
Female
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Multiple Sclerosis
/ diagnostic imaging
Photic Stimulation
Physical Therapy Modalities
Postural Balance
Pressure
Proprioception
Sensation
White Matter
/ diagnostic imaging
Young Adult
Balance
Cerebellum
MRI
Multiple sclerosis
Proprioception
Sensory
Journal
Cerebellum (London, England)
ISSN: 1473-4230
Titre abrégé: Cerebellum
Pays: United States
ID NLM: 101089443
Informations de publication
Date de publication:
Feb 2021
Feb 2021
Historique:
accepted:
07
09
2020
pubmed:
25
9
2020
medline:
26
10
2021
entrez:
24
9
2020
Statut:
ppublish
Résumé
People with multiple sclerosis (PwMS) exhibit impaired balance during different sensory environments and poor cerebellar peduncle microstructure. We aimed to examine associations between microstructures of the superior, middle and inferior cerebellar peduncles (CP) with visual, vestibular, and proprioceptive-based balance in PwMS. Twenty-seven PwMS and twenty-nine healthy controls (HC) underwent MRI and balance assessments. We assessed CP microstructure with radial diffusivity (RD) and fractional anisotropy (FA) and balance with center of pressure-derived measures of path length and root mean square of sway during proprioceptive (C2), visual (C3), and vestibular (C4) balance conditions of the modified clinical test of sensory integration on balance (mCTSIB). PwMS exhibited significantly lower FA (p < 0.001) and greater RD (p < 0.001) across all CP and greater path length (p < 0.05) in the mCTSIB compared with HC. In PwMS, significant associations were detected between inferior CP white matter microstructure and proprioceptive-based balance control (rho = -0.43, p < 0.05) and middle CP white matter microstructure and visual-based balance control (rho = 0.39, p < 0.05). PwMS may rely more on cerebellar-regulated proprioceptive- and visual-based balance control than HC.
Identifiants
pubmed: 32970313
doi: 10.1007/s12311-020-01190-y
pii: 10.1007/s12311-020-01190-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
92-100Subventions
Organisme : National Multiple Sclerosis Society
ID : PP-1708-29077
Références
Trapp BD, Nave K-A. Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci. 2008;31:247–69. https://doi.org/10.1146/annurev.neuro.30.051606.094313 .
doi: 10.1146/annurev.neuro.30.051606.094313
pubmed: 18558855
pmcid: 18558855
Denommé LT, Mandalfino P, Cinelli ME. Understanding balance differences in individuals with multiple sclerosis with mild disability: an investigation of differences in sensory feedback on postural control during a Romberg task. Exp Brain Res. 2014;232:1833–42.
doi: 10.1007/s00221-014-3875-3
Cameron M, Nilsagard Y. Balance, gait and falls in multiple sclerosis. Handb Clin Neurol. 159.
Salmen A, von Wyl V, Puhan MA, et al. The disease burden of multiple sclerosis from the individual and population perspective: which symptoms matter most? Mult Scler Relat Disord. 2018;25:112–21. https://doi.org/10.1016/j.msard.2018.07.013 .
doi: 10.1016/j.msard.2018.07.013
pubmed: 30059895
Cattaneo D, Jonsdottir J. Sensory impairments in quiet standing in subjects with multiple sclerosis. Mult Scler. 2009;15:59–67. https://doi.org/10.1177/1352458508096874 .
doi: 10.1177/1352458508096874
pubmed: 18845654
Horak FB, Diener HC, Nashner LM. Influence of central set on human postural responses. J Neurophysiol. 2017;62:841–53. https://doi.org/10.1152/jn.1989.62.4.841 .
doi: 10.1152/jn.1989.62.4.841
Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol. 2002;88:1097–118. https://doi.org/10.1152/jn.2002.88.3.1097 .
doi: 10.1152/jn.2002.88.3.1097
pubmed: 12205132
Assländer L, Peterka RJ. Sensory reweighting dynamics following removal and addition of visual and proprioceptive cues. J Neurophysiol. 2016;116:272–85. https://doi.org/10.1152/jn.01145.2015 .
doi: 10.1152/jn.01145.2015
pubmed: 27075544
pmcid: 4969387
Huisinga JM, Yentes JM, Filipi ML, Stergiou N. Postural control strategy during standing is altered in patients with multiple sclerosis. Neurosci Lett. 2012;524:124–8.
doi: 10.1016/j.neulet.2012.07.020
Prosperini L, Castelli L. Spotlight on postural control in patients with multiple sclerosis. 2018;8:25–34. https://doi.org/10.2147/DNND.S135755 .
Takakusaki K. Functional neuroanatomy for posture and gait control. J Mov Disord. 2017. https://doi.org/10.14802/jmd.16062 .
Martin CZ, Brooks JX, Green AM. Role of rostral fastigial neurons in encoding a body-centered representation of translation in three dimensions. J Neurosci. 2018;38:3584–602.
doi: 10.1523/JNEUROSCI.2116-17.2018
Angelaki DE, Cullen KE. Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci. 2008;31:125–50.
doi: 10.1146/annurev.neuro.31.060407.125555
Dichgans J. Characteristics of increased postural sway and abnormal long loop responses in patients with cerebellar diseases and Parkinsonism. 1985.
Horak FB, Diener HC. Cerebellar control of postural scaling and central set in stance. J Neurophysiol. 1994;72:479–93. https://doi.org/10.1152/jn.1994.72.2.479 .
doi: 10.1152/jn.1994.72.2.479
pubmed: 7983513
De Santis S, Granberg T, Ouellette R, et al. Evidence of early microstructural white matter abnormalities in multiple sclerosis from multi-shell diffusion MRI. NeuroImage Clin. 2019;22. https://doi.org/10.1016/j.nicl.2019.101699 .
Van Hecke W, Emsell L, Sunaert S. Diffusion tensor imaging 123 a practical handbook. 2016.
doi: 10.1007/978-1-4939-3118-7
Gulani V, Webb AG, Duncan ID, et al. Apparent diffusion tensor measurements in myelin-deficient rat spinal cords. 2001.
doi: 10.1002/1522-2594(200102)45:2<191::AID-MRM1025>3.0.CO;2-9
Gera G, Fling BW, Horak FB. Cerebellar white matter damage is associated with postural sway deficits in people with multiple Sclerosis. Arch Phys Med Rehabil. 2019;101:258–64. https://doi.org/10.1016/j.apmr.2019.07.011 .
doi: 10.1016/j.apmr.2019.07.011
pubmed: 31465761
Fling BW, Dutta GG, Schlueter H, Cameron MH, Horak FB. Associations between proprioceptive neural pathway structural connectivity and balance in people with multiple sclerosis. Front Hum Neurosci. 2014;8. https://doi.org/10.3389/fnhum.2014.00814 .
Ehsani F, Samaei A, Zoghi M, Hedayati R, Jaberzadeh S. The effects of cerebellar transcranial direct current stimulation on static and dynamic postural stability in older individuals: a randomized double-blind sham-controlled study. Eur J Neurosci. 2017;46:2875–84.
doi: 10.1111/ejn.13731
Poortvliet P, Hsieh B, Cresswell A, Au J, Meinzer M. Cerebellar transcranial direct current stimulation improves adaptive postural control. Clin Neurophysiol. 2018;129:33–41.
doi: 10.1016/j.clinph.2017.09.118
Leemans A, Jeurissen B, Sijbers J, Jones D. ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data 2009; 3537.
Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage. 2008;40:570–82.
doi: 10.1016/j.neuroimage.2007.12.035
Cohen HS, Mulavara AP, Peters BT, Sangi-Haghpeykar H, Bloomberg JJ. Standing balance tests for screening people with vestibular impairments. Laryngoscope. 2014;124:545–50.
doi: 10.1002/lary.24314
Richmond SB, Dames KD, Goble DJ, Fling BW. Leveling the playing field: evaluation of a portable instrument for quantifying balance performance. J Biomech. 2018;75:102–7.
doi: 10.1016/j.jbiomech.2018.05.008
Prieto TE, Myklebust JB, Hoffmann RG, et al. Measures of postural steadiness: differences between healthy young and elderly adults. 1996.
Palmieri RM, Ingersoll CD, Stone MB, et al. Center-of-pressure parameters used in the assessment of postural control. J Sport Rehabil. 2016;11:51–66.
doi: 10.1123/jsr.11.1.51
Prosperini L, Sbardella E, Raz E, et al. Multiple sclerosis: white and gray matter damage associated with balance deficit detected at static posturography. Radiology. 2013. https://doi.org/10.1148/radiol.13121695 .
Hannoun S, Kocevar G, Durand-Dubief F, Stamile C, Naji A, Cotton F, et al. Evidence of axonal damage in cerebellar peduncles without T2-lesions in multiple sclerosis. Eur J Radiol. 2018;108:114–9.
doi: 10.1016/j.ejrad.2018.09.016
Anderson VM, Wheeler-Kingshott CAM, Abdel-Aziz K, Miller DH, Toosy A, Thompson AJ, et al. A comprehensive assessment of cerebellar damage in multiple sclerosis using diffusion tractography and volumetric analysis. Mult Scler J. 2011;17:1079–87.
doi: 10.1177/1352458511403528
Polders DL, Leemans A, Hendrikse J, Donahue MJ, Luijten PR, Hoogduin JM. Signal to noise ratio and uncertainty in diffusion tensor imaging at 1.5, 3.0, and 7.0 tesla. J Magn Reson Imaging. 2011;33:1456–63.
doi: 10.1002/jmri.22554
Goble DJ, Coxon JP, van Impe A, Geurts M, Doumas M, Wenderoth N, et al. Brain activity during ankle proprioceptive stimulation predicts balance performance in young and older adults. J Neurosci. 2011;31:16344–52.
doi: 10.1523/JNEUROSCI.4159-11.2011
Leonard G, Lapierre Y, Chen J-K, et al. Noninvasive tongue stimulation combined with intensive cognitive and physical rehabilitation induces neuroplastic changes in patients with multiple sclerosis: a multimodal neuroimaging study. Mult Scler J Exp Transl Clin. 2017;3:205521731769056.
Ouchi Y, Okada H, Yoshikawa E, et al. Brain activation during maintenance of standing postures in humans. Brain. 1999;122:329–38.
doi: 10.1093/brain/122.2.329
Lin IS, Lai DM, Ding JJ, et al. Reweighting of the sensory inputs for postural control in patients with cervical spondylotic myelopathy after surgery. J Neuroeng Rehabil. 2019;16. https://doi.org/10.1186/s12984-019-0564-2 .
Brooks JX, Cullen KE. Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J Neurosci. 2009;29:10499–511.
doi: 10.1523/JNEUROSCI.1937-09.2009
Lam CK, Staines WR, Tokuno CD, et al. The medium latency muscle response to a vestibular perturbation is increased after depression of the cerebellar vermis. Brain Behav. 2017;7. https://doi.org/10.1002/brb3.782 .
Diener HC, Dichgans J, Bacher M, et al. Quantification of postural sway in normals and patients with cerebellar diseases n. 1984.
doi: 10.1016/0013-4694(84)90172-X
Chambers WW, Sprague JM. Functional localization in the cerebellum. J Comp Neurol.
Erickson KI, Kramer AF. Aerobic exercise effects on cognitive and neural plasticity in older adults. Br J Sports Med. 2009;43:22–4.
doi: 10.1136/bjsm.2008.052498
Morton SM, Bastian AJ. Cerebellar control of balance and locomotion. Neuroscientist. 2004;10:247–59.
doi: 10.1177/1073858404263517