Skip to main content
Top
Published in: BMC Neurology 1/2021

Open Access 01-12-2021 | Stroke | Research article

Longitudinal changes in the inferior cerebellar peduncle and lower limb motor recovery following subcortical infarction

Authors: Gang Liu, Yaomin Guo, Chao Dang, Kangqiang Peng, Shuangquan Tan, Chuanmiao Xie, Shihui Xing, Jinsheng Zeng

Published in: BMC Neurology | Issue 1/2021

Login to get access

Abstract

Background

The cerebellum receives afferent signals from spinocerebellar pathways regulating lower limb movements. However, the longitudinal changes in the spinocerebellar pathway in the early stage of unilateral supratentorial stroke and their potential clinical significance have received little attention.

Methods

Diffusion tensor imaging and Fugl-Meyer assessment of lower limb were performed 1, 4, and 12 weeks after onset in 33 patients with acute subcortical infarction involving the supratentorial areas, and in 33 healthy subjects. We evaluated group differences in diffusion metrics in the bilateral inferior cerebellar peduncle (ICP) and analyzed the correlation between ICP diffusion metrics and changes to the Fugl-Meyer scores of the affected lower limb within 12 weeks after stroke.

Results

Significantly decreased fractional anisotropy and increased mean diffusivity were found in the contralesional ICP at week 12 after stroke compared to controls (all P < 0.01) and those at week 1 (all P < 0.05). There were significant fractional anisotropy decreases in the ipsilesional ICP at week 4 (P = 0.008) and week 12 (P = 0.004) compared to controls. Both fractional anisotropy (rs = 0.416, P = 0.025) and mean diffusivity (rs = -0.507, P = 0.005) changes in the contralesional ICP correlated with changes in Fugl-Meyer scores of the affected lower limb in all patients.

Conclusions

Bilateral ICP degeneration occurs in the early phase of supratentorial stroke, and diffusion metric values of the contralesional ICP are useful indicators of affected lower limb function after supratentorial stroke.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kim Y, Im S, Kim SH, Park GY. Laterality of cerebellar afferent and efferent pathways in a healthy right-handed population: a diffusion tensor imaging study. J Neurosci Res. 2019;97:582–96.CrossRef Kim Y, Im S, Kim SH, Park GY. Laterality of cerebellar afferent and efferent pathways in a healthy right-handed population: a diffusion tensor imaging study. J Neurosci Res. 2019;97:582–96.CrossRef
2.
go back to reference Grimaldi G, Manto M. Topography of cerebellar deficits in humans. Cerebellum. 2012;11:336–51.CrossRef Grimaldi G, Manto M. Topography of cerebellar deficits in humans. Cerebellum. 2012;11:336–51.CrossRef
3.
go back to reference Mann MD. Axons of dorsal spinocerebellar tract which respond to activity in cutaneous receptors. J Neurophysiol. 1971;34:1035–50.CrossRef Mann MD. Axons of dorsal spinocerebellar tract which respond to activity in cutaneous receptors. J Neurophysiol. 1971;34:1035–50.CrossRef
4.
go back to reference Pantano P, Baron JC, Samson Y, Bousser MG, Derouesne C, Comar D. Crossed cerebellar diaschisis. Further studies. Brain. 1986;109:677–94.CrossRef Pantano P, Baron JC, Samson Y, Bousser MG, Derouesne C, Comar D. Crossed cerebellar diaschisis. Further studies. Brain. 1986;109:677–94.CrossRef
5.
go back to reference Kim Y, Kim SH, Kim JS, Hong BY. Modification of cerebellar afferent pathway in the subacute phase of stroke. J Stroke Cerebrovasc Dis. 2018;27:2445–52.CrossRef Kim Y, Kim SH, Kim JS, Hong BY. Modification of cerebellar afferent pathway in the subacute phase of stroke. J Stroke Cerebrovasc Dis. 2018;27:2445–52.CrossRef
6.
go back to reference Kim JS, Kim SH, Lim SH, Im S, Hong BY, Oh J, et al. Degeneration of the inferior cerebellar peduncle after middle cerebral artery stroke: another perspective on crossed cerebellar diaschisis. Stroke. 2019;50:2700–7.CrossRef Kim JS, Kim SH, Lim SH, Im S, Hong BY, Oh J, et al. Degeneration of the inferior cerebellar peduncle after middle cerebral artery stroke: another perspective on crossed cerebellar diaschisis. Stroke. 2019;50:2700–7.CrossRef
7.
go back to reference Li J, Zuo Z, Zhang X, Shao X, Lu J, Xue R, et al. Excitatory repetitive transcranial magnetic stimulation induces contralesional cortico-cerebellar pathways after acute ischemic stroke: a preliminary DTI Study. Front Behav Neurosci. 2018;12:160.CrossRef Li J, Zuo Z, Zhang X, Shao X, Lu J, Xue R, et al. Excitatory repetitive transcranial magnetic stimulation induces contralesional cortico-cerebellar pathways after acute ischemic stroke: a preliminary DTI Study. Front Behav Neurosci. 2018;12:160.CrossRef
8.
go back to reference Habas C, Cabanis EA. Anatomical parcellation of the brainstem and cerebellar white matter: a preliminary probabilistic tractography study at 3 T. Neuroradiology. 2007;49:849–63.CrossRef Habas C, Cabanis EA. Anatomical parcellation of the brainstem and cerebellar white matter: a preliminary probabilistic tractography study at 3 T. Neuroradiology. 2007;49:849–63.CrossRef
9.
go back to reference Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;29:83–91.CrossRef Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;29:83–91.CrossRef
10.
go back to reference Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–7.CrossRef Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–7.CrossRef
11.
go back to reference Mohamed MA, Yousem DM, Tekes A, Browner N, Calhoun VD. Correlation between the amplitude of cortical activation and reaction time: a functional MRI study. AJR Am J Roentgenol. 2004;183:759–65.CrossRef Mohamed MA, Yousem DM, Tekes A, Browner N, Calhoun VD. Correlation between the amplitude of cortical activation and reaction time: a functional MRI study. AJR Am J Roentgenol. 2004;183:759–65.CrossRef
12.
go back to reference Yang H, Long XY, Yang Y, Yan H, Zhu CZ, Zhou XP, Zang YF, Gong QY. Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage. 2007;36:144–52.CrossRef Yang H, Long XY, Yang Y, Yan H, Zhu CZ, Zhou XP, Zang YF, Gong QY. Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage. 2007;36:144–52.CrossRef
13.
go back to reference Zhang J, Meng L, Qin W, Liu N, Shi FD, Yu C. Structural damage and functional reorganization in ipsilesional M1 in well-recovered patients with subcortical stroke. Stroke. 2014;45:788–93.CrossRef Zhang J, Meng L, Qin W, Liu N, Shi FD, Yu C. Structural damage and functional reorganization in ipsilesional M1 in well-recovered patients with subcortical stroke. Stroke. 2014;45:788–93.CrossRef
14.
go back to reference Zhang Z, Lu G, Zhong Y, Tan Q, Chen H, Liao W, et al. fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Hum Brain Mapp. 2010;31:1851–61.CrossRef Zhang Z, Lu G, Zhong Y, Tan Q, Chen H, Liao W, et al. fMRI study of mesial temporal lobe epilepsy using amplitude of low-frequency fluctuation analysis. Hum Brain Mapp. 2010;31:1851–61.CrossRef
15.
go back to reference Zhu J, Jin Y, Wang K, Zhou Y, Feng Y, Yu M, et al. Frequency-dependent changes in the regional amplitude and synchronization of resting-state functional MRI in stroke. PLoS One. 2015;10:e0123850.CrossRef Zhu J, Jin Y, Wang K, Zhou Y, Feng Y, Yu M, et al. Frequency-dependent changes in the regional amplitude and synchronization of resting-state functional MRI in stroke. PLoS One. 2015;10:e0123850.CrossRef
16.
go back to reference Liu G, Dang C, Peng K, Xie C, Chen H, Xing S, et al. Increased spontaneous neuronal activity in structurally damaged cortex is correlated with early motor recovery in patients with subcortical infarction. Eur J Neurol. 2015;22:1540–7.CrossRef Liu G, Dang C, Peng K, Xie C, Chen H, Xing S, et al. Increased spontaneous neuronal activity in structurally damaged cortex is correlated with early motor recovery in patients with subcortical infarction. Eur J Neurol. 2015;22:1540–7.CrossRef
17.
go back to reference Liang Z, Zeng J, Zhang C, Liu S, Ling X, Wang F, et al. Progression of pathological changes in the middle cerebellar peduncle by diffusion tensor imaging correlates with lesser motor gains after pontine infarction. Neurorehabil Neural Repair. 2009;23:692–8.CrossRef Liang Z, Zeng J, Zhang C, Liu S, Ling X, Wang F, et al. Progression of pathological changes in the middle cerebellar peduncle by diffusion tensor imaging correlates with lesser motor gains after pontine infarction. Neurorehabil Neural Repair. 2009;23:692–8.CrossRef
18.
go back to reference Liang Z, Zeng J, Zhang C, Liu S, Ling X, Xu A, et al. Longitudinal investigations on the anterograde and retrograde degeneration in the pyramidal tract following pontine infarction with diffusion tensor imaging. Cerebrovasc Dis. 2008;25:209–16.CrossRef Liang Z, Zeng J, Zhang C, Liu S, Ling X, Xu A, et al. Longitudinal investigations on the anterograde and retrograde degeneration in the pyramidal tract following pontine infarction with diffusion tensor imaging. Cerebrovasc Dis. 2008;25:209–16.CrossRef
19.
go back to reference Liang Z, Zeng J, Liu S, Ling X, Xu A, Yu J, et al. A prospective study of secondary degeneration following subcortical infarction using diffusion tensor imaging. J Neurol Neurosurg Psychiatry. 2007;78:581–6.CrossRef Liang Z, Zeng J, Liu S, Ling X, Xu A, Yu J, et al. A prospective study of secondary degeneration following subcortical infarction using diffusion tensor imaging. J Neurol Neurosurg Psychiatry. 2007;78:581–6.CrossRef
20.
go back to reference Liu G, Dang C, Chen X, Xing S, Dani K, Xie C, et al. Structural remodeling of white matter in the contralesional hemisphere is correlated with early motor recovery in patients with subcortical infarction. Restor Neurol Neurosci. 2015;33:309–19.PubMed Liu G, Dang C, Chen X, Xing S, Dani K, Xie C, et al. Structural remodeling of white matter in the contralesional hemisphere is correlated with early motor recovery in patients with subcortical infarction. Restor Neurol Neurosci. 2015;33:309–19.PubMed
21.
go back to reference Liu G, Tan S, Dang C, Peng K, Xie C, Xing S, et al. Motor recovery prediction with clinical assessment and local diffusion homogeneity after acute subcortical infarction. Stroke. 2017;48:2121–8.CrossRef Liu G, Tan S, Dang C, Peng K, Xie C, Xing S, et al. Motor recovery prediction with clinical assessment and local diffusion homogeneity after acute subcortical infarction. Stroke. 2017;48:2121–8.CrossRef
22.
go back to reference Liu G, Peng K, Dang C, Tan S, Chen H, Xie C, et al. Axial diffusivity changes in the motor pathway above stroke foci and functional recovery after subcortical infarction. Restor Neurol Neurosci. 2018;36:173–82.PubMed Liu G, Peng K, Dang C, Tan S, Chen H, Xie C, et al. Axial diffusivity changes in the motor pathway above stroke foci and functional recovery after subcortical infarction. Restor Neurol Neurosci. 2018;36:173–82.PubMed
23.
go back to reference Cui Z, Zhong S, Xu P, He Y, Gong G. PANDA: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci. 2013;7:42.PubMedPubMedCentral Cui Z, Zhong S, Xu P, He Y, Gong G. PANDA: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci. 2013;7:42.PubMedPubMedCentral
24.
go back to reference Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL Neuroimage. 2012;62:782–90.CrossRef Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL Neuroimage. 2012;62:782–90.CrossRef
25.
go back to reference Xing S, Lacey EH, Skipper-Kallal LM, Jiang X, Harris-Love ML, Zeng J, et al. Right hemisphere grey matter structure and language outcomes in chronic left hemisphere stroke. Brain. 2016;139:227–41.CrossRef Xing S, Lacey EH, Skipper-Kallal LM, Jiang X, Harris-Love ML, Zeng J, et al. Right hemisphere grey matter structure and language outcomes in chronic left hemisphere stroke. Brain. 2016;139:227–41.CrossRef
26.
go back to reference Paldino MJ, Hedges K, Zhang W. Independent contribution of individual white matter pathways to language function in pediatric epilepsy patients. Neuroimage Clin. 2014;6:327–32.CrossRef Paldino MJ, Hedges K, Zhang W. Independent contribution of individual white matter pathways to language function in pediatric epilepsy patients. Neuroimage Clin. 2014;6:327–32.CrossRef
27.
go back to reference Zhang M, Lin Q, Lu J, Rong D, Zhao Z, Ma Q, et al. Pontine infarction: diffusion-tensor imaging of motor pathways-a longitudinal study. Radiology. 2015;274:841–50.CrossRef Zhang M, Lin Q, Lu J, Rong D, Zhao Z, Ma Q, et al. Pontine infarction: diffusion-tensor imaging of motor pathways-a longitudinal study. Radiology. 2015;274:841–50.CrossRef
28.
go back to reference Mori S, Wakana S, Van Zijl PCM, Nagae-Poetscher L. MRI Atlas of Human White Matter. London: Elsevier Science; 2005. Mori S, Wakana S, Van Zijl PCM, Nagae-Poetscher L. MRI Atlas of Human White Matter. London: Elsevier Science; 2005.
29.
go back to reference Bosco G, Eian J, Poppele RE. Phase-specific sensory representations in spinocerebellar activity during stepping: evidence for a hybrid kinematic/kinetic framework. Exp Brain Res. 2006;175:83–96.CrossRef Bosco G, Eian J, Poppele RE. Phase-specific sensory representations in spinocerebellar activity during stepping: evidence for a hybrid kinematic/kinetic framework. Exp Brain Res. 2006;175:83–96.CrossRef
30.
go back to reference Yanagihara D. Mechanisms of locomotor control in the cerebellum. Brain Nerve. 2010;62:1149–56.PubMed Yanagihara D. Mechanisms of locomotor control in the cerebellum. Brain Nerve. 2010;62:1149–56.PubMed
31.
go back to reference Jang SH, Kwon HG. Diffusion tensor tractography for the dorsal spinocerebellar tract in the human brain. Somatosens Mot Res. 2014;31:7–10.CrossRef Jang SH, Kwon HG. Diffusion tensor tractography for the dorsal spinocerebellar tract in the human brain. Somatosens Mot Res. 2014;31:7–10.CrossRef
32.
go back to reference Choi JH, Seo JD, Choi YR, Kim MJ, Kim HJ, Kim JS, et al. Inferior cerebellar peduncular lesion causes a distinct vestibular syndrome. Eur J Neurol. 2015;22:1062–7.CrossRef Choi JH, Seo JD, Choi YR, Kim MJ, Kim HJ, Kim JS, et al. Inferior cerebellar peduncular lesion causes a distinct vestibular syndrome. Eur J Neurol. 2015;22:1062–7.CrossRef
33.
go back to reference Thömke F, Marx JJ, Iannetti GD, Cruccu G, Fitzek S, Urban PP, et al. A topodiagnostic investigation on body lateropulsion in medullary infarcts. Neurology. 2005;64:716–8.CrossRef Thömke F, Marx JJ, Iannetti GD, Cruccu G, Fitzek S, Urban PP, et al. A topodiagnostic investigation on body lateropulsion in medullary infarcts. Neurology. 2005;64:716–8.CrossRef
34.
go back to reference Eggers C, Fink GR, Möller-Hartmann W, Nowak DA. Correlation of anatomy and function in medulla oblongata infarction. Eur J Neurol. 2009;16:201–4.CrossRef Eggers C, Fink GR, Möller-Hartmann W, Nowak DA. Correlation of anatomy and function in medulla oblongata infarction. Eur J Neurol. 2009;16:201–4.CrossRef
35.
go back to reference Jayaram G, Stagg CJ, Esser P, Kischka U, Stinear J, Johansen-Berg H. Relationships between functional and structural corticospinal tract integrity and walking post stroke. Clin Neurophysiol. 2012;123:2422–8.CrossRef Jayaram G, Stagg CJ, Esser P, Kischka U, Stinear J, Johansen-Berg H. Relationships between functional and structural corticospinal tract integrity and walking post stroke. Clin Neurophysiol. 2012;123:2422–8.CrossRef
36.
go back to reference Jones PS, Pomeroy VM, Wang J, Schlaug G, Tulasi Marrapu S, Geva S, et al. Does stroke location predict walk speed response to gait rehabilitation? Hum Brain Mapp. 2016;37:689–703.CrossRef Jones PS, Pomeroy VM, Wang J, Schlaug G, Tulasi Marrapu S, Geva S, et al. Does stroke location predict walk speed response to gait rehabilitation? Hum Brain Mapp. 2016;37:689–703.CrossRef
37.
go back to reference Dawes H, Enzinger C, Johansen-Berg H, Bogdanovic M, Guy C, Collett J, et al. Walking performance and its recovery in chronic stroke in relation to extent of lesion overlap with the descending motor tract. Exp Brain Res. 2008;186:325–33.CrossRef Dawes H, Enzinger C, Johansen-Berg H, Bogdanovic M, Guy C, Collett J, et al. Walking performance and its recovery in chronic stroke in relation to extent of lesion overlap with the descending motor tract. Exp Brain Res. 2008;186:325–33.CrossRef
38.
go back to reference Smith MC, Byblow WD, Barber PA, Stinear CM. Proportional recovery from lower limb motor impairment after stroke. Stroke. 2017;48:1400–3.CrossRef Smith MC, Byblow WD, Barber PA, Stinear CM. Proportional recovery from lower limb motor impairment after stroke. Stroke. 2017;48:1400–3.CrossRef
Metadata
Title
Longitudinal changes in the inferior cerebellar peduncle and lower limb motor recovery following subcortical infarction
Authors
Gang Liu
Yaomin Guo
Chao Dang
Kangqiang Peng
Shuangquan Tan
Chuanmiao Xie
Shihui Xing
Jinsheng Zeng
Publication date
01-12-2021
Publisher
BioMed Central
Keyword
Stroke
Published in
BMC Neurology / Issue 1/2021
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-021-02346-x

Other articles of this Issue 1/2021

BMC Neurology 1/2021 Go to the issue