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Structure and function of corticospinal projection originating from supplementary motor area

  • Functional Neuroradiology
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Abstract

Purpose

The importance of supplementary motor area (SMA) for motor function and compensation for primary motor area (M1) has received increased attention.

Methods

We used diffusion tensor imaging (DTI) and transcranial magnetic stimulation (TMS) to evaluate structure and function of corticospinal projection originating from SMA. Fibers of corticospinal projection originating from M1 (CST) and SMA (ACST) were analyzed. ACST originating from mesial SMA area formed separate white matter bundles leaving the anterior part of M1 area, which then entered the posterior limb of the internal capsule. Projection and overlap of both CST and ACST were detected on medulla.

Results

Fibers of contralesional ACST were more than that of ipsilesional ACST in patients with SMA tumors (p<0.05). In patients with SMA tumor, all patients experienced temporary akinesia postoperatively. Seven hundred forty-one fibers of ipsilateral ACST and no fibers of ipsilateral CST were detected in the patient with M1 glioma, while most of contralateral limb movement was preserved. MEP could be evoked by stimulating SMA area as well as M1 area. ACST originated from SMA area and projected to the medial medulla.

Conclusion

SMA area and ACST integrity contributed to contralateral motor function and were a compensation for M1 lesion and damaged CST.

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References

  1. Baker CM, Burks JD, Briggs RG, Smitherman AD, Glenn CA, Conner AK, Wu DH, Sughrue ME (2018) The crossed frontal aslant tract: a possible pathway involved in the recovery of supplementary motor area syndrome. Brain Behav 8(3):e00926. https://doi.org/10.1002/brb3.926

    Article  PubMed  PubMed Central  Google Scholar 

  2. Vassal M, Charroud C, Deverdun J, Le Bars E, Molino F, Bonnetblanc F, Boyer A, Dutta A, Herbet G, Moritz-Gasser S, Bonafe A, Duffau H, de Champfleur NM (2017) Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area. J Neurosurg 126(4):1181–1190. https://doi.org/10.3171/2016.4.JNS152484

    Article  PubMed  Google Scholar 

  3. Rosenberg K, Liebling R, Avidan G, Perry D, Siman-Tov T, Andelman F, Ram Z, Fried I, Hendler T (2008) Language related reorganization in adult brain with slow growing glioma: fMRI prospective case-study. Neurocase 14(6):465–473. https://doi.org/10.1080/13554790802459486

    Article  PubMed  Google Scholar 

  4. Tate MC, Kim CY, Chang EF, Polley MY, Berger MS (2011) Assessment of morbidity following resection of cingulate gyrus gliomas. Clinical article. J Neurosurg 114(3):640–647. https://doi.org/10.3171/2010.9.JNS10709

    Article  PubMed  Google Scholar 

  5. Schulz R, Park CH, Boudrias MH, Gerloff C, Hummel FC, Ward NS (2012) Assessing the integrity of corticospinal pathways from primary and secondary cortical motor areas after stroke. Stroke 43(8):2248–2251. https://doi.org/10.1161/STROKEAHA.112.662619

    Article  PubMed  PubMed Central  Google Scholar 

  6. Newton JM, Ward NS, Parker GJ, Deichmann R, Alexander DC, Friston KJ, Frackowiak RS (2006) Non-invasive mapping of corticofugal fibres from multiple motor areas--relevance to stroke recovery. Brain 129(Pt 7):1844–1858. https://doi.org/10.1093/brain/awl106

    Article  PubMed  Google Scholar 

  7. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG (1997) Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. Brain J Neurol 120(Pt 9):1587–1602. https://doi.org/10.1093/brain/120.9.1587

    Article  Google Scholar 

  8. Cona G, Semenza C (2017) Supplementary motor area as key structure for domain-general sequence processing: a unified account. Neurosci Biobehav Rev 72:28–42. https://doi.org/10.1016/j.neubiorev.2016.10.033

    Article  PubMed  Google Scholar 

  9. Galea MP, Darian-Smith I (1994) Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cereb Cortex 4(2):166–194. https://doi.org/10.1093/cercor/4.2.166

    Article  CAS  PubMed  Google Scholar 

  10. Demeurisse G, Demol O, Robaye E (1980) Motor evaluation in vascular hemiplegia. Eur Neurol 19(6):382–389. https://doi.org/10.1159/000115178

    Article  CAS  PubMed  Google Scholar 

  11. Cona G, Marino G, Semenza C (2017) TMS of supplementary motor area (SMA) facilitates mental rotation performance: evidence for sequence processing in SMA. NeuroImage 146:770–777. https://doi.org/10.1016/j.neuroimage.2016.10.032

    Article  CAS  PubMed  Google Scholar 

  12. Kobayashi M, Pascual-Leone A (2003) Transcranial magnetic stimulation in neurology. Lancet Neurol 2(3):145–156. https://doi.org/10.1016/s1474-4422(03)00321-1

    Article  PubMed  Google Scholar 

  13. Dromerick AW, Edwards DF, Diringer MN (2003) Sensitivity to changes in disability after stroke: a comparison of four scales useful in clinical trials. J Rehabil Res Dev 40(1):1–8. https://doi.org/10.1682/jrrd.2003.01.0001

    Article  PubMed  Google Scholar 

  14. Chang MC, Chun MH (2015) Right lower limb apraxia in a patient with left supplementary motor area infarction: intactness of the corticospinal tract confirmed by transcranial magnetic stimulation. Neural Regen Res 10(2):325–327. https://doi.org/10.4103/1673-5374.152389

    Article  PubMed  PubMed Central  Google Scholar 

  15. Mathew P, Batchala PP, Eluvathingal Muttikkal TJ (2018) Supplementary motor area stroke mimicking functional disorder. Stroke 49(2):e28–e30. https://doi.org/10.1161/STROKEAHA.117.019106

    Article  PubMed  Google Scholar 

  16. Kim YH, Kim CH, Kim JS, Lee SK, Han JH, Kim CY, Chung CK (2013) Risk factor analysis of the development of new neurological deficits following supplementary motor area resection. J Neurosurg 119(1):7–14. https://doi.org/10.3171/2013.3.JNS121492

    Article  PubMed  Google Scholar 

  17. Rosenberg K, Nossek E, Liebling R, Fried I, Shapira-Lichter I, Hendler T, Ram Z (2010) Prediction of neurological deficits and recovery after surgery in the supplementary motor area: a prospective study in 26 patients. J Neurosurg 113(6):1152–1163. https://doi.org/10.3171/2010.6.JNS1090

    Article  PubMed  Google Scholar 

  18. Darling WG, Ge J, Stilwell-Morecraft KS, Rotella DL, Pizzimenti MA, Morecraft RJ (2018) Hand motor recovery following extensive frontoparietal cortical injury is accompanied by upregulated corticoreticular projections in monkey. J Neurosci 38(28):6323–6339. https://doi.org/10.1523/JNEUROSCI.0403-18.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Seo JP, Jang SH (2013) Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. AJNR Am J Neuroradiol 34(7):1359–1363. https://doi.org/10.3174/ajnr.A3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. McNeal DW, Darling WG, Ge J, Stilwell-Morecraft KS, Solon KM, Hynes SM, Pizzimenti MA, Rotella DL, Vanadurongvan T, Morecraft RJ (2010) Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury. J Comp Neurol 518(5):586–621. https://doi.org/10.1002/cne.22218

    Article  PubMed  PubMed Central  Google Scholar 

  21. Green PE, Ridding MC, Hill KD, Semmler JG, Drummond PD, Vallence AM (2018) Supplementary motor area-primary motor cortex facilitation in younger but not older adults. Neurobiol Aging 64:85–91. https://doi.org/10.1016/j.neurobiolaging.2017.12.016

    Article  PubMed  Google Scholar 

  22. Bulubas L, Sabih J, Wohlschlaeger A, Sollmann N, Hauck T, Ille S, Ringel F, Meyer B, Krieg SM (2016) Motor areas of the frontal cortex in patients with motor eloquent brain lesions. J Neurosurg 125(6):1431–1442. https://doi.org/10.3171/2015.11.JNS152103

    Article  PubMed  Google Scholar 

  23. Riley JD, Le V, Der-Yeghiaian L, See J, Newton JM, Ward NS, Cramer SC (2011) Anatomy of stroke injury predicts gains from therapy. Stroke 42(2):421–426. https://doi.org/10.1161/STROKEAHA.110.599340

    Article  PubMed  Google Scholar 

  24. Amengual JL, Munte TF, Marco-Pallares J, Rojo N, Grau-Sanchez J, Rubio F, Duarte E, Grau C, Rodriguez-Fornells A (2014) Overactivation of the supplementary motor area in chronic stroke patients. J Neurophysiol 112(9):2251–2263. https://doi.org/10.1152/jn.00735.2013

    Article  PubMed  Google Scholar 

  25. Yeo SS, Jang SH (2012) A change in injured corticospinal tract originating from the premotor cortex to the primary motor cortex in a patient with intracerebral hemorrhage. Neural Regen Res 7(12):939–942. https://doi.org/10.3969/j.issn.1673-5374.2012.12.010

    Article  PubMed  PubMed Central  Google Scholar 

  26. Magill ST, Han SJ, Li J, Berger MS (2018) Resection of primary motor cortex tumors: feasibility and surgical outcomes. J Neurosurg 129(4):961–972. https://doi.org/10.3171/2017.5.JNS163045

    Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful to our team and clinicians who made the study possible (Ming-xia Xu, especially).

Funding

This work was supported by National Natural Science Foundation of China (No. 81802492 to Pei-Sen Yao), Young and Middle-aged Backbone Key Research Project of National Health and Family Planning Commission of Fujian Province (No. 2017-ZQN-46 to Pei-Sen Yao), and Natural Science Funding of Fujian Province (No. 2018J01175 to Pei-Sen Yao and No. 2018J01176 to Shu-Fa Zheng) and Startup Fund for scientific research, Fujian Medical University(No.2019QH1087 to Ming-xia Xu).

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Author notes

  1. Ya-Wen Xu, Peng Lin and Pei-Sen Yao contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Neurosurgical Institute, The First Affiliated Hospital of Fujian Medical University, NO. 20 Chazhong Road, Taijiang District, Fuzhou, 350004, China

    Ya-Wen Xu, Pei-Sen Yao, Shu-Fa Zheng & De-Zhi Kang

  2. Department of Pain Treatment, The First Affiliated Hospital, Fujian Medical University, Fuzhou, China

    Peng Lin

  3. Fujian Key Laboratory of Precision Medicine for Cancer, The First Affiliated Hospital, Fujian Medical University, Fuzhou, China

    De-Zhi Kang

Authors
  1. Ya-Wen Xu
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  2. Peng Lin
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  3. Pei-Sen Yao
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  4. Shu-Fa Zheng
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  5. De-Zhi Kang
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Ya-Wen Xu, Peng Lin, and Pei-Sen Yao. The first draft of the manuscript was written by Ya-Wen Xu, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to De-Zhi Kang.

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Conflicts of interest

The authors have no financial or proprietary interests in any material discussed in this article

Ethics approval

This retrospective chart review study involving human participants was in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The Human Investigation Committee (IRB) of First Affiliated Hospital of Fujian Medical University approved this study.

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Our study was approved by the institutional review board, which waived informed consent because it was retrospective

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Xu, YW., Lin, P., Yao, PS. et al. Structure and function of corticospinal projection originating from supplementary motor area. Neuroradiology 63, 1283–1292 (2021). https://doi.org/10.1007/s00234-021-02669-z

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  • DOI: https://doi.org/10.1007/s00234-021-02669-z

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