Proprioception deficits in chronic ankle instability associated with structural and functional alternations in cerebellar vermis

Xiao'ao Xue , Yuwen Zhang , LeYu , Qianru Li , Yiran Wang , Zikun Wang , Shanshan Zheng , Yang Sun , He Wang , Yinghui Hua

Sports Medicine and Health Science ›› 2026, Vol. 8 ›› Issue (1) : 96 -101.

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Sports Medicine and Health Science ›› 2026, Vol. 8 ›› Issue (1) :96 -101. DOI: 10.1016/j.smhs.2024.11.006
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Proprioception deficits in chronic ankle instability associated with structural and functional alternations in cerebellar vermis
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Abstract

Purpose: Ankle proprioception deficits have been widely reported in patients with chronic ankle instability (CAI), but their central neuropathological mechanisms have not been fully discussed. So, we aimed to figure out whether the structural and functional features of the cerebellar vermis differed between patients with CAI and healthy controls, and are associated with proprioception deficits in patients.

Methods: Twenty- two patients and 25 control individuals were enrolled in a cross-sectional investigation. All participants underwent structural and resting-state functional magnetic resonance imaging scanning to calculate voxel-based morphometry (VBM) and fractional amplitude of low-frequency fluctuation (fALFF) of the vermis. Between-group comparisons of the ankle instability-related subregions of the vermis were performed. Correlation analyses were performed between the outcomes of the surviving subregions and the proprioceptive scores of the ankle inversion discrimination apparatus for landing test.

Results: The subregion of vermis IV/V survived the multiple comparison correction to reveal a lower VBM value in patients than in healthy controls (Cohen's d ​= ​−0.968). The patients also showed significantly higher fALFF (Cohen's d ​= ​0.666) in this subregion. After controlling the demographic features, the proprioceptive scores were significantly correlated with VBM (r ​= ​0.622) and fALFF values (r ​= ​−0.512) in the group of patients.

Conclusions: Patients with CAI have lower gray matter volume and higher activity intensity in the cerebellar vermis than healthy control. The more severe proprioception deficits were significantly associated with the vermal volume and activity, which might be able to facilitate future diagnoses and treatments for CAI.

Keywords

Ankle injuries / Proprioception / Cerebellar vermis / Magnetic resonance imaging

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Xiao'ao Xue, Yuwen Zhang, LeYu, Qianru Li, Yiran Wang, Zikun Wang, Shanshan Zheng, Yang Sun, He Wang, Yinghui Hua. Proprioception deficits in chronic ankle instability associated with structural and functional alternations in cerebellar vermis. Sports Medicine and Health Science, 2026, 8(1): 96-101 DOI:10.1016/j.smhs.2024.11.006

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CRediT authorship contribution statement

Xiao'ao Xue: Writing - original draft, Formal analysis, Data curation, Conceptualization. Yuwen Zhang: Writing - original draft, Formal analysis, Data curation, Conceptualization. Le Yu: Writing - original draft, Formal analysis, Data curation, Conceptualization. Qianru Li: Writing - review & editing, Software, Methodology. Yiran Wang: Writing - review & editing, Visualization, Software. Zikun Wang: Writing - review & editing, Methodology. Shanshan Zheng: Writing - review & editing, Formal analysis. Yang Sun: Writing - review & editing, Supervision, Resources. He Wang: Writing - review & editing, Supervision, Funding acquisition. Yinghui Hua: Writing - review & editing, Supervision, Project administration, Funding acquisition.

Funding

This work was supported by the National Natural Science Foundation of China [grant numbers 82372492, 82072510], National Key R&D Program of China [grant numbers 2018YFC1312900], Shanghai Natural Science Foundation [grant numbers 20ZR1406400], Science and Technology Commission of Shanghai Municipality [grant numbers 22dz1204700].

Ethical approval statement

All procedures were conducted adequate understanding and written informed consent from the subjects. All research protocols were approved by the institutional research ethics committee of Huashan Hospital (No. 2016-314).

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors sincerely thank the subjects for their participation and support in this study. The authors would also like to gratefully acknowledge EditSprings (https://www.editsprings.com/) for the expert linguistic services provided, and Prof. Jia Han for his series of high-quality studies on ankle proprioception that played as the guideline for the work of the first author.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.smhs.2024.11.006.

References

[1]

Owoeye OBA, Palacios-Derflingher LM, Emery CA. Prevention of ankle sprain injuries in youth soccer and basketball: effectiveness of a neuromuscular training program and examining risk factors. Clin J Sport Med. 2018; 28(4):325-331. https://doi.org/10.1097/JSM.0000000000000462.

[2]

Gribble PA, Delahunt E, Bleakley C, et al. Selection criteria for patients with chronic ankle instability in controlled research: a position statement of the International Ankle Consortium. Br J Sports Med. 2014; 48(13):1014-1018. https://doi.org/10.1136/bjsports-2013-093175.

[3]

Hertel J, Corbett RO. An updated model of chronic ankle instability. J Athl Train. 2019; 54(6):572-588. https://doi.org/10.4085/1062-6050-344-18.

[4]

Xue X, Wang Y, Xu X, et al. Postural control deficits during static single-leg stance in chronic ankle instability: a systematic review and meta-analysis. Sport Health. 2024; 16(1):29-37. https://doi.org/10.1177/19417381231152490.

[5]

Han J, Waddington G, Adams R, Anson J, Liu Y. Assessing proprioception: a critical review of methods. J Sport Heal Sci. 2016; 5(1):80-90. https://doi.org/10.1016/j.jshs.2014.10.004.

[6]

Xue X, Ma T, Li Q, Song Y, Hua Y. Chronic ankle instability is associated with proprioception deficits: a systematic review and meta-analysis. J Sport Heal Sci. 2021; 10(2):182-191. https://doi.org/10.1016/j.jshs.2020.09.014.

[7]

Thompson C, Schabrun S, Romero R, Bialocerkowski A, van Dieen J, Marshall P. Factors contributing to chronic ankle instability: a systematic review and meta-analysis of systematic reviews. Sports Med. 2018; 48(1):189-205. https://doi.org/10.1007/s40279-017-0781-4.

[8]

Han J, Waddington G, Anson J, Adams R. Level of competitive success achieved by elite athletes and multi-joint proprioceptive ability. J Sci Med Sport. 2015; 18(1): 77-81. https://doi.org/10.1016/j.jsams.2013.11.013.

[9]

Kobayashi T, Tanaka M, Shida M. Intrinsic risk factors of lateral ankle sprain: a systematic review and meta-analysis. Sport Health. 2016; 8(2):190-193. https://doi.org/10.1177/1941738115623775.

[10]

Cho BK, Park JK. Correlation between joint-position sense, peroneal strength, postural control, and functional performance ability in patients with chronic lateral ankle instability. Foot Ankle Int. 2019; 40(8):961-968. https://doi.org/10.1177/1071100719846114.

[11]

Needle AR, Lepley AS, Grooms DR. Central nervous system adaptation after ligamentous injury: a summary of theories, evidence, and clinical interpretation. Sports Med. 2017; 47(7):1271-1288. https://doi.org/10.1007/s40279-016-0666-y.

[12]

Röijezon U, Clark NC, Treleaven J. Proprioception in musculoskeletal rehabilitation: Part 1: basic science and principles of assessment and clinical interventions. Man Ther. 2015; 20(3):368-377. https://doi.org/10.1016/j.math.2015.01.008.

[13]

Bosco G, Poppele RE. Proprioception from a spinocerebellar perspective. Physiol Rev. 2001; 81(2):539-568. https://doi.org/10.1152/physrev.2001.81.2.539.

[14]

Xue X, Zhang Y, Li S, Xu H, Chen S, Hua Y. Lateral ankle instability-induced neuroplasticity in brain grey matter: a voxel-based morphometry MRI study. J Sci Med Sport. 2021; 24(12):1240-1244. https://doi.org/10.1016/j.jsams.2021.06.013.

[15]

Wikstrom EA, Hubbard-Turner T, Woods S, Guderian S, Turner MJ. Developing a mouse model of chronic ankle instability. Med Sci Sports Exerc. 2015; 47(4):866-872. https://doi.org/10.1249/MSS.0000000000000466.

[16]

Xue X, Zhang Y, Tao W, et al. Longitudinal neuroplasticity after ankle sprain in mice: a voxel-based morphometry study on 11.7T MRI. J Orthop Res. 2023; 41(6): 1291-1298. https://doi.org/10.1002/jor.25458.

[17]

Logothetis NK. What we can do and what we cannot do with fMRI. Nature. 2008; 453(7197):869-878. https://doi.org/10.1038/nature06976.

[18]

Yang J, Gohel S, Vachha B. Current methods and new directions in resting state fMRI. Clin Imag. 2020; 65(November 2019):47-53. https://doi.org/10.1016/j.clinimag.2020.04.004.

[19]

Xue X, Lu R, Zang D, et al. Low regional homogeneity of intrinsic cerebellar activity in ankle instability: an externally validated rs-fMRI study. Med Sci Sports Exerc. 2022; 54(12):2037-2044. https://doi.org/10.1249/mss.0000000000002998.

[20]

Zou QH, Zhu CZ, Yang Y, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008; 172(1):137-141. https://doi.org/10.1016/j.jneumeth.2008.04.012.

[21]

Han J, Yang Z, Adams R, Ganderton C, Witchalls J, Waddington G. Ankle inversion proprioception measured during landing in individuals with and without chronic ankle instability. J Sci Med Sport. 2021; 24(7):665-669. https://doi.org/10.1016/j.jsams.2021.02.004.

[22]

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. Neuroimage. 2002; 15(1):273-289. https://doi.org/10.1006/nimg.2001.0978.

[23]

Han J, Yang Z, Witchalls J, Ganderton C, Adams R, Waddington G. Ankle inversion proprioception impairment in persons with chronic ankle instability is task-specific. Percept Mot Skills. 2022; 0(0):1-13. https://doi.org/10.1177/00315125221125608.

[24]

Cohen J. Statistical Power Analysis for the Behavioral Sciences. England: Lawrence Erlbaum Associates; 1988.

[25]

Han J, Anson J, Waddington G, Adams R, Liu Y. The role of ankle proprioception for balance control in relation to sports performance and injury. BioMed Res Int. 2015; 2015:842804. https://doi.org/10.1155/2015/842804.

[26]

Witchalls J, Waddington G, Blanch P, Adams R. Ankle instability effects on joint position sense when stepping across the active movement extent discrimination apparatus. J Athl Train. 2012; 47(6):627-634. https://doi.org/10.4085/1062-6050-47.6.12.

[27]

Asan L, Falfán-Melgoza C, Beretta CA, et al. Cellular correlates of gray matter volume changes in magnetic resonance morphometry identified by two-photon microscopy. Sci Rep. 2021; 11(1):1-20. https://doi.org/10.1038/s41598-021-83491-8.

[28]

Doherty C, Bleakley C, Delahunt E, Holden S. Treatment and prevention of acute and recurrent ankle sprain: an overview of systematic reviews with meta-analysis. Br J Sports Med. 2017; 51(2):113-125. https://doi.org/10.1136/bjsports-2016-096178.

[29]

Xue X, Chen Z, Xu X, Tao W, Hua Y. Do external supports influence proprioception in patients with chronic ankle instability?: a systematic review and meta-analyses. Am J Phys Med Rehabil. 2022; 101(7):644-651. https://doi.org/10.1097/PHM.0000000000001876.

[30]

Han J, Luan L, Adams R, et al. Can therapeutic exercises improve proprioception in chronic ankle instability? A systematic review and network meta-analysis. Arch Phys Med Rehabil. 2022; 103(11):2232-2244. https://doi.org/10.1016/j.apmr.2022.04.007.

[31]

Xue X, Tao W, Xu X, et al. Do exercise therapies restore the deficits of joint position sense in patients with chronic ankle instability? A systematic review and meta-analysis. Sport Med Heal Sci. 2023:4-10. https://doi.org/10.1016/j.smhs.2023.01.001.

[32]

Yosephi MH, Ehsani F, Zoghi M, Jaberzadeh S. Multi-session anodal tDCS enhances the effects of postural training on balance and postural stability in older adults with high fall risk: primary motor cortex versus cerebellar stimulation. Brain Stimul. 2018; 11(6):1239-1250. https://doi.org/10.1016/j.brs.2018.07.044.

[33]

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(12):2875-2884. https://doi.org/10.1111/ejn.13731.

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