Functional and diagnostic significance of the fMRI-response type to motor loads in patients after traumatic brain damage

Aim of the study. Clarification of the functional and diagnostic significance of topography, or the type of fMRI-response recorded during active and passive hand movements in patients after traumatic brain injury.

Material and methods. fMRI-responses gained during active and passive hand movements were analyzed in 40 patients with posttraumatic motor function disturbances and compared with results gained from 17 healthy volunteers (control group ).

Results. In analyzed patients the increase of percentage of diffuse fMRI-response has been shown along with the areas of activation not typical for movement activation pattern typical healthy volunteers. The fMRI response type being it local or multifocal does not clearly correlate with the presence of motor function impairment (hemiparesis). However, it was found that with greater severity of hemiparesis there is a larger percentage of multifocal fMRI-response.

The transition from a multifocal form of a motor fMRI-response to a local one observed in a dynamic study is accompanied by an improvement of patient’s general condition, a shift towards normalization of a number of morphofunctional indicators of the central nervous system, the tendency of regression of motor disorders.

Conclusion. The increase of multifocal fMRI-responses in patients after traumatic brain injury is one of the signs of cerebral dysfunction. Dynamically observed transformation from multifocal to local fMRI-responses is associated with current or long-term improvement in motor activity as well, wit the regression of other clinical impairments and can be considered as prognostically positive sign of the course of post-traumatic illness.

1. Bigler E.D.,Wilde E.A. Quantitative neuroimaging and the prediction outcome following traumatic brain injury. Frontiers Human Neurosci. 2010; 4 (3): 228–234. http://doi.org/10.3389/fnhum.2010.00228

2. Potapov A.A., Danilov G.V., Sychev A.A., Zakharova N.E., Pronin I.N., Savin I.A., Oshorov A.V., Polupan A.A., Aleksandrova E.V., Strunina Yu.V., Likhterman L.B., Okhlopkov V.A., Latyshev Ya.A., Chelushkin D.M., Baranich A.I., Kravchuk A.D. Clinical and MRI predictors of coma duration, critical care intensity and outcomes in traumatic brain injury. Burdenko's Journal of Neurosurgery = Zhurnal “Voprosy neirokhirurgii” imeni N.N. Burdenko. 2020; 84 (4): 5–16. https://doi.org/10.17116/neiro2020840415

3. Shtark M.B., Korostishevskaya A.M., Resakova M.V., Savelov A.A. Functional magnetic resonanse imaging and neuroscience. Uspekhi Fiziologicheskikh Nauk. 2012; 43 (1): 3–29. (In Russian)

4. Boldyreva G.N., Sharova E.V., Zhavoronkova L.A., Chelyapina M.V., Dubrovskaia L.P., Simonova O.A., Fadeeva L.M., Pronin I.N., Korniyenko V.N. Structural and Functional Peculiarity of Brain Activity to Performance and Imaginary Motor Tasks in Healthy Persons (EEG and fMRI study). I.P. Pavlov Journal of Higher Nervous Activity = Zh Vyssh Nerv Deiat I P Pavlova. 2013; 63 (3): 316–327. http://doi.org/10.7868/S0044467713030039 (In Russian)

5. Boldyreva G.N., Sharova E.V., Zhavoronkova L.A., Chelyapina M.V., Dubrovskaia L.P., Simonova O.A., Smirnov A.S., Troshina E.M., Korniyenko V.N. EEG and fMRI Reactions of a Healthy Brain at Active and Passive Movements by a Leading Hand. I.P. Pavlov Journal of Higher Nervous Activity = Zh Vyssh Nerv Deiat I P Pavlova. 2014; 64 (5): 388–399. http://doi.org/10.7868/S0044467714050049 (In Russian)

6. Zhavoronkova L.A., Boldyreva G.N., Sharova E.V., Kuptsova S.V., Moraresku S.I., Smirnov A.S., Masherov E.L., Pronin I.N. FMRI reactions in motor tasks performed by patients with traumatic brain injury. Human Physiology. 2018; 44 (5): 2–9. http://doi.org/10.1134/S0131164618050168 (In Russian)

7. Frolov A.A., Fedotova I.R., Husek D., Bobrov P.D. Rhythmic brain activity and brain computer interface based on motor imagery. Uspekhi Fiziologicheskikh Nauk. 2017; 48 (3): 72–91. (In Russian)

8. Van de Winckel A., Klingels K., Bruyninckx F., Wenderoth N., Peeters R., Sunaert S., Van Hecke W.,De Cock P., Eyssen M., De Weerdt W., Feys H. How does brain activation differ in children with unilateral cerebral palsy compared to typically developing children, during active and passive movements, and tactile stimulation? An fMRI study. Res. Dev. Disabil. 2013. 34 (1): 183–197. https://doi.org/10.1016/j.ridd.2012.07.030

9. Weiss C., Nettekoven C., Rehme A., Neuschmelting V., Eisenbeis A., Goldbrunner R., Grefkes C. Mapping the hand, foot and face representations in the primary motor cortex – Retest reliability of neuronavigated TMS versus functional MRI. NeuroImage. 2013. 66: 531–543.

10. Weinstein M., Green D., Rudisch J., Zielinski I.M., Benthem-Muñiz M., Jongsma M.L.A., McClelland V., Steenbergen B., Shiran S., Ben Bashat D., Barker G.J. Understanding the relationship between brain and upper limb function in children with unilateral motor impairments: a multimodal approach. Eur. J. Paediatr. Neurol. 2018; 22 (1): 143–154. https://doi.org/10.1016/j.ejpn.2017.09.012

11. Boldyreva G.N., Zhavoronkova L.A., Sharova E.V., Migalev A.S., Skoriatina I.G., Fadeeva L.M., Podoprigora A.E., Pronin I.N., Kornienko V.N. EEG–fMRI study of human brain functional specialization in healthy persons and patients with cerebral pathology. Medical Visualization. 2012; 1: 16–26. (In Russian)

12. Mukhina T.S., Sharova E.V., Boldyreva G.N., Zhavoronkova L.A., Smirnov A.S., Kulikov M.A., Aleksandrova E.V., Chelyapina M.V., Masherov E.L., Pronin I.N. The neuroanatomy of active hand movement in patients with severe traumatic brain injury: Analysis of functional magnetic resonance imaging data. Neurology, Neuropsychiatry, Psychosomatics. 2017; 9 (1): 27–33. https://doi.org/10.14412/2074-2711-2017-1-27-33 (In Russian)

13. Sharova E., Boldyreva G., Zhavoronkova L., Smirnov A., Azarov A., Mukhina T., Gavron A., Kulikov M., Alexandrova E., Pronin I. FMRI analysis of the human brain’s neuroplasticity as a basis of movement disorders compensation after traumatic brain injury. Accepted abstracts of ECCN. Clin. Neurophysiol. 2017; 128 (9): e278-e279. https://doi.org/10.1016/j.clinph.2017.07.320

14. Dobrynina L.A., Kremneva E.I., Konovalov R.N., Kadykov A.S. Functional reorganization of sensorimotor cortex in chronic hemispheric ischemic stroke patients with different severity of motor deficit. Annals of Clinical and Experimental Neurology. 2012; 6 (3): 4–13. https://doi.org/10.17816/psaic267 (In Russian)

15. Diao Q., Liu J., Wang C., Cao C., Guo J., Han T., Cheng J., Zhang X., Yu C. Gray matter volume changes in chronic subcortical stroke: A cross-sectional study. NeuroImage: Clin. 14 (2017): 679–684. http://dx.doi.org/10.1016/j.nicl.2017.01.031

16. Busheneva S.N., Kadykov A.S., Chernikova L.A. Influence of rehabilitation therapy on functional organization of motor systems after stroke. Annals of Clinical and Experimental Neurology. 2007; 2: 4–8. https://doi.org/10.17816/psaic439 (In Russian)

17. Abela E., Seiler A., Missimer J.H., Federspiel A., Hess C.W., Sturzenegger M., Weder B.J., Wiest R. Grey matter volumetric changes related to recovery from hand paresis after cortical sensorimotor stroke. Brain Struct Funct. 2015; 220: 2533–2550. https://doi.org/10.1007/s00429-014-0804-y

18. Yong Zhang, Kuang-Shi Li, Yan-Zhe Ning, Cai-Hong Fu, Hong-Wei Liu, Xiao Han, Fang-Yuan Cui, Yi Ren, , Yi-Huai Zou . Altered structural and functional connectivity between the bilateral primary motor cortex in unilateral subcortical stroke . A multimodal magnetic resonance imaging study. Medicine. 2016; 95: 31(e4534). http://dx.doi.org/10.1097/MD.0000000000004534

19. Gaberova K, Pacheva I. , Ivanov I. Task-related fMRI in hemiplegic cerebral palsy -A systematic review. J. Eval. Clin. Pract. 2018; 24 (4): 839–850. https://doi.org/10.1111/jep.12929.

20. McPeak L.A. Physiatric history and examination. In: Braddom R., ed. Physical medicine and rehabilitation. W.B. Saunders Company, 1996: 3–42.

21. Dobrynina L.A., Kremneva E.I., Konovalov R.N., Kadykov A.S. Functional MRI study: passive motor paradigm in the assessment of sensorimotor system. Annals of Clinical and Experimental Neurology. 2011; 5 (3): 10–19. https://doi.org/10.17816/psaic302 (In Russian)

22. Saenko I.V., Morozova S.N., Zmeykina E.A., Konovalov R.N., Chervyakov A.V., Poydasheva A.G., Chernikova L.A., Suponeva N.A., Piradov M.A., Kozlovskaya I.B. Changes in the Functional Connectivity of Motor Zones in the Use of Multimodal Exoskeleton Complex “Regent” in the Neurorehabilitation of Post;Stroke Patients. Human Physiology. 2016; 42 (1): 64–72. https://doi.org/10.7868/S013116461601015X (In Russian)

23. Boldyreva G.N., Yarets M.Y., Sharova E.V., Zhavoronkova L.A., Kuptsova S.V., Сhelyapina-Postnikova M.V., Masherov E.L., Kulikov M.A., Smirnov A.S., Pronin I.N. Features Of FMRI brain reaction in motor load by patients with mild post-traumatic hemiparesis. Журнал высшей нервной деятельности. 2020; 70 (5): 579–589. https://doi.org/10.31857/S0044467720050044 (In Russian)

24. Kharauzov A.K., Vasil'ev P.P., Shelepin Y.E., Sokolov A.V., Fokin V.A. Functional magnetic resonance imaging analysis of the human brain in texture recognition tasks. Journal of Optical Technology. 2018; 85 (8): 22–28. https://doi.org/10.17586/1023-5086-2018-85-08-22-28 (In Russian)

25. Kou Z., Iraji A. Imaging brain plasticity after trauma. Neural. Regen. Res. 2014; 9 (7): 693–700. https://doi.org/10.4103/1673-5374.131568

26. Sharova E.V., Boldyreva G.N., Kulikov M.A., Zhavoronkova L.A., Chelyapina-Postnikova M.V., Popov V.A., Troshina E.M., Aleksandrova E.V., Smirnov A.S., Skoryatina I.G., Lysachev D.A. EEG correlates of passive hand movement in patients after traumatic brain injury with preserved fmri motor response. Human Physiology. 2019; 45 (5): 30–40. https://doi.org/10.1134/S0131164619050175

27. Zang K., Johnson B., Ray W., Sebastianelli W., Slobounov S. Are functional deficits is concussed individuals consistent with white matter structural alterations: combined FMRI and DTI study. Exp Brain Res. 2010; 204 (1): 57–70. https://doi.org/10.1007/s00221-010-2294-3

28. Kadykov A.S., Barkhatov Y.D. The value of various brain pathways impairment in the post-stroke rehabilitation of walking function. Annals of Clinical and Experimental Neurology. 2014; 8 (3): 45–48. https://doi.org/10.17816/psaic172 (In Russian)

29. Prosperini L., Di Filippo M. Beyond clinical changes: Rehabilitation induced neuroplasticity in MS. Multiple Sclerosis J. 2019; 25 (10): 1348–1362. https://doi.org/10.1177/1352458519846096