Preview

Medical Visualization

Advanced search

fMRI resting state networks visualization in patients with severe traumatic brain injury

https://doi.org/10.24835/1607-0763-2020-1-68-84

Abstract

According to the literature, fMRI analysis at resting state (RS) is an informative methodological approach to the study of the basic level of a healthy and diseased brain’s functional activity. Averaging data over observation groups for various forms of cerebral pathology is often unacceptable. Previously, we mastered and applied the Independent Component Algorithm (ICA) in FSL software to visualize and analyze individual fMRI resting networks of healthy people.

Objective: to analyze individual fMRI resting networks associated with the state of motor activity and consciousness in patients with severe traumatic brain injury (STBI).

Materials and methods. Observation groups: 23 patients with SТBI (main) and 17 healthy volunteers (control). 3T fMRI recorded at rest. Individual (norm and STBI) and group (norm) analysis of RS networks was carried out by FSL software (ICA algorithm) and SPM8 in MATLAB.
For the DMN and Sensorimotor networks, topography and total volume and intensity of their activation of their activation were determined.

Results. The topography features reproduced in the group and individual analysis of fMRI of healthy people, as well as the averaged quantitative indicators of the rest networks were used as reference for pathology.
In the context of motor activity, the RS Sensorimotor network was considered. Its topography is close to normal in most patients without or with mild hemiparesis. The growth of this defect is accompanied by a decrease in the integral quantitative indicators of the network, combined with asymmetric reduction (lack of activation in the contralateral motor cortex) in rough hemiparesis.
In the context of consciousness, the expression and characteristics of the DMN network were compared in healthy people and in patients with STBI at its various levels: from clear to chronic vegetative state. It was revealed that a decrease in the level of consciousness is accompanied by a reduction in the cortical components of DMN, primarily the frontal (anterior DMN), not pronounced in the vegetative state. Activation of the caudal component of DMN (in particular, the posterior cingular cortex) persists in patients with depressed consciousness: distinct and even somewhat enhanced compared to the norm with its reversible form, less pronounced with chronic

Conclusion. The data obtained indicate the informative value of fMRI analysis of individual resting networks in the context of studying cerebral structural and functional foundations of consciousness and motor activity, as well as diagnosing the state of these functions in STBI.

About the Authors

E. V. Sharova
Institute of Higher Nervous Activity and Neurophysiology of RAS
Russian Federation

Doct. of Sci. (Biol.), Head of the Laboratory of common and clinical neurophysiology

Phone: +7-499-972-85-59 (rings at least 7)

5A Butlerova Str., Moscow 117485, Russian Federation



Ju. V. Kotovich
Institute of Higher Nervous Activity and Neurophysiology of RAS; National Research Nuclear University MEPhI (Moscow Engineering Physics Institute)
Russian Federation
Master's Degree Student

5A Butlerova Str., Moscow 117485, Russian Federation  31 Kashirskoe hwy, Moscow, 115409, Russian Federation


Yacila Isabela Deza-Araujo
Department of Psychiatry and Neuroimaging Center, Technische Universitat Dresden
Germany
M.Sc. Neuropsych. PhD candidate/Doktorandin

 Dezernat 8, Dresden, 01062, Germany


A. S. Smirnov
Federal State Autonomous Institution “N.N. Burdenko National Medical Research Center of Neurosurgery”of the Ministry of Health of the Russian Federation
Russian Federation
med. doctor of Neuroradiology department

16, 4 Tverskaya-Yamskaya str., Moscow, 125047, Russian Federation



A. A. Gavron
Institute of Higher Nervous Activity and Neurophysiology of RAS; National Research Nuclear University MEPhI (Moscow Engineering Physics Institute)
Russian Federation
Master's Degree Student

5A Butlerova Str., Moscow 117485, Russian Federation  31 Kashirskoe hwy, Moscow, 115409, Russian Federation


L. M. Fadeeva
Federal State Autonomous Institution “N.N. Burdenko National Medical Research Center of Neurosurgery”of the Ministry of Health of the Russian Federation
Russian Federation
lead. engineer of Neuroradiology department

16, 4 Tverskaya-Yamskaya str., Moscow, 125047, Russian Federation



M. V. Chelyapina-Postnikova
Institute of Higher Nervous Activity and Neurophysiology of RAS
Russian Federation
Cand. of Sci. (Med.), Jr. Researcher

5A Butlerova Str., Moscow 117485, Russian Federation





E. V. Alexandrova
Federal State Autonomous Institution “N.N. Burdenko National Medical Research Center of Neurosurgery”of the Ministry of Health of the Russian Federation
Russian Federation
Cand. of Sci. (Med.), neurologist

16, 4 Tverskaya-Yamskaya str., Moscow, 125047, Russian Federation



L. A. Zhavoronkova
Institute of Higher Nervous Activity and Neurophysiology of RAS
Russian Federation
Doct. of Sci. (Biol.), leading researcher of the Institute of Higher Nervous Activity and Neurophysiology of RAS

5A Butlerova Str., Moscow 117485, Russian Federation



G. N. Boldyreva
Institute of Higher Nervous Activity and Neurophysiology of RAS
Russian Federation
Doct. of Sci. (Biol.), prof., Chief researcher

5A Butlerova Str., Moscow 117485, Russian Federation



V. M. Verkhlyutov
Institute of Higher Nervous Activity and Neurophysiology of RAS
Russian Federation
Cand. of Sci. (Med.), senior researcher

5A Butlerova Str., Moscow 117485, Russian Federation


V. N. Kornienko
Federal State Autonomous Institution “N.N. Burdenko National Medical Research Center of Neurosurgery”of the Ministry of Health of the Russian Federation
Russian Federation
Full Мember of the Russian Academy of Sciences, Doct. of Sci. (Med.), Professor, Сonsultant, Neuroradiology department

16, 4 Tverskaya-Yamskaya str., Moscow, 125047, Russian Federation



I. N. Pronin
Federal State Autonomous Institution “N.N. Burdenko National Medical Research Center of Neurosurgery”of the Ministry of Health of the Russian Federation
Russian Federation

Full Мember of the Russian Academy of Sciences, Doct. of Sci. (Med.), Professor, Head of Neuroradiology department, Deputy Director

16, 4 Tverskaya-Yamskaya str., Moscow, 125047, Russian Federation





References

1. Potapov A.A., Likhterman L.B., Kravchuk A.D., Roshal' L.M. Traumatic brain injury: problems and prospects. Burdenko's Journal of Neurosurgery = Zhurnal “Voprosy neirokhirurgii” imeni N.N. Burdenko. 2009; 2: 3–8. (In Russian)

2. Dobrokhotova T.A., Potapov A.A., Zaitsev O.S., Likhterman L.B. Postcoma reversible unconscious state. Sotsial'naya i linicheskaya psikhiatriya. 1996; 2: 26–36. (In Russian)

3. Zaitsev O.S. Psychopathology of severe traumatic brain injury (2nd ed.). Moscow: MEDpress-inform, 2014. 335 p. (In Russian)

4. Laureus S., Tononi G. The Neurology of Consciousness. London: Elssevier. 2009. 423 p.

5. Lutkenhoff E.S., Chiang J., Tshibanda L., Kamau E., Kirsch M., Pickard J.D., Laureys S., Owen A.M., Monti M.M. Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann Neurol. 2015; 78: 68. http://doi.org/10.1002/ana.24423

6. Sharova E.V., Zaitsev O.S., Kulikov M.А., Schepetkov A.N., Korobkova E.V., Chelyapina M.V. Functional and structural preconditions of oppression consciousnesses at the heavycraniocereberal trauma. Neironauhi: Theoretiheskie I klinicheskie Aspecti (Ukraine, Donetsk). 2011; 1–2: 68–75. (In Russian)

7. Kondratieva E.A., Yakovenko I.V. Vegetative state (etiology, pathogenesis, diagnosis). Moscow:Publishing House Medicine, 2014. 361 p. (In Russian)

8. Aleksandrova E.V., Tenedieva V.D., Potapov A.A. Posttraumatic unconscious states. Moscow: GEOTAR-Media; 2015. 392 p. (In Russian)

9. Piradov M.A., Suponeva N.A., Sergeev D.V., Chervyakov A.V., Ryabinkina Yu.V., Sinitsyn D.O., Poydasheva A.G., Kremneva E.I., Morozova S.N., Iazeva E.G., Legostaeva L.A. Structural and functional basis of chronic disorders of consciousness. Ann. Clin. Experimental Neurol. 2018; 12 (Special issue): 6–15. http://doi.org/10.25692/ACEN.2018.5.1 (In Russian)

10. Aleksandrova E.V., Zaytsev O.S., Potapov A.A. Neurotransmitter Basis of Consciousness and Unconsciousness. Burdenko's Journal of Neurosurgery = Zhurnal “Voprosy neirokhirurgii” imeni N.N. Burdenko. 2014: 78 (1): 26–32. (In Russian)

11. Chelyapina-Postnikova M.V., Sharova E.V., Zaitsev О.S. A comparative clinical and encephalographic study on manifestation of the choline and dopamine deficiency syndromes in consciousness recovery after severe traumatic brain injury. Int. J. Med. Sci. Clin. Invent. 2019;

12. 6 (5): 4468–4471. http://doi.org/10.18535/ijmsci/v6i5.07

13. Dobrokhotova T.A., Grindel' O.M., Bragina N.N., Potapov A.A., Sharova E.V., Kniazeva N.A. Recovery of consciousness after prolonged coma in patients with severe traumatic brain injury. S.S. Korsakov Journal of Neurology and Psychiatry = Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 1985; 85 (5): 720–726. (In Russian)

14. Grindel' O.M., Romanova N.V., Zaytsev O.S, Voronov V.G., Skoryatina I.G. Mathematical analysis of EEG in conscious ness recovery after traumatic traumatic brain injuries. S.S. Korsakov Journal of Neurology and Psychiatry = Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 2006; 106 (12): 47–51. (In Russian)

15. Sharova E.V., Chelyapina M.V., Korobkova E.V., Kulikov M.A., Zaitsev O.S. EEG correlates of consciousness recovery after traumatic brain injury. N.N. Burdenko Journal of Neurosurgery. 2014; 1: 13–23.

16. Zhavoronkova L.A., Zharikova A.V., Maksakova O.A. The integrative role of restoration of voluntary postural control in the rehabilitation of patients with craniocerebral trauma. Neuroscience and Behavioral Physiology. 2012; 42 (5): 486–494.

17. Zakharova N., Kornienko V., Potapov A., Pronin I. Neuroiaging of traumatic brain injury. London: Springer, 2014. 159 p.

18. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995; 34: 537–541.

19. Van Dijk K.R., Hedden T., Venkataraman A. et al. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 2010; 103: 297–321. http://doi.org/10.1152/jn.00783.2009.

20. Shtark M.B., Korostyshevskaja A.M., Rezakova M.V., Savelov A.A. Functional magnetic resonance imaging and neuroscience. Uspekhi fiziologicheskikh nauk. 2012; 43 (1): 3–29. (In Russian)

21. Raichle M.E., Mintun M.A. Brain work and brain imaging. Ann. Rev. Neurosci. 2006; 29: 449–476. http://doi.org/10.1146/annurev.neuro.29.051605.112819

22. Cordes D., Haughton V.M., Arfanakis K., Wendt G.J., Turski P.A., Moritz C.H., Quigley M.A., Meyerand M.E. Mapping functionally related regions of brain with functional connectivity MR imaging. Am. J. Neuroradiol. 2000; 21: 1636–1644.

23. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2005; 360: 1001–1013. https://doi.org/10.1098/rstb.2005.1634

24. Rosazza C., Minati L. Resting-state brain networks: literature review and clinical applications. Neurol Sci. 2011; 32 (5): 773–785. http://doi.org/10.1007/s10072-011-0636-y

25. Verkhlyutov V.M., Sokolov P.A., Ushakov V.L., Velichkovsky B.M. Macroscopic Functional Networks of the Human Brain when Viewing and Recalling Short Videos. I.P. Pavlov Journal of Higher Nervous Activity = Zh Vyssh Nerv Deiat I.P. Pavlova. 2015; 65 (3):333–343. PMID: 26281231. (In Russian)

26. Martynova O.V., Sushinskaya-Tetereva A.O., Balaev V.V., Ivanitsky A.M. Correlation of functional connectivity of brain regions active at rest with behavioral and psychological indicators. I.P. Pavlov Journal of Higher Nervous Activity = Zh Vyssh Nerv Deiat I.P. Pavlova. 2016; 66 (5): 541–555.

27. http://doi.org/10.7868/S0044467716050063 (In Russian)

28. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysisof the default mode hypothesis. Proc. Natl. Acad. Sci. USA. 2003; 100: 253–258. http://doi.org/10.1073/pnas.0135058100

29. Allen E.A., Erhardt E.B., Damaraju E., Gruner W., Segall J.M., Silva R.F., Havlicek M., Rachakonda S., Fries J., Kalyanam R., Michael A.M., Caprihan A., Turner J.A., Eichele T., Adelsheim S., Bryan A.D., Bustillo J., Clark V.P., Feldstein Ewing S.W., Filbey F., Ford C.C., Hutchison K., Jung R.E., Kiehl K.A., Kodituwakku P., Komesu Y.M., Mayer A.R., Pearlson G.D., Phillips J.P., Sadek J.R., Stevens M., Teuscher U., Thoma R.J., Calhoun V.D. A baseline for the multivariate comparison of resting-state networks. Frontiers in Systems Neuroscience. 2011; 5: 1–19. http://doi.org/10.3389/fnsys.2011.00002

30. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain’s functional architecture during activation and rest. Proc. Natl. Acad. Sci. USA. 2009; 106: 13040–13045. http://doi.org/10.1073/pnas.0905267106

31. Rocca M.A., Valsasina P., Absinta M., Riccitelli G., Rodegher M.E., Misci P., Rossi P., Falini A., Comi G., Filippi M. Default-mode network dysfunction and cognitive impairment in progressive MS. Neurol. 2010; 74: 1252–1259. http://doi.org/10.1212/WNL.0b013e3181d9ed91

32. Bonavita S., Gallo A., Sacco R., Corte M.D., Bisecco A., Docimo R., Lavorgna L., Corbo D., Costanzo A.D., Tortora F., Cirillo M., Esposito F., Tedeschi G. Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Mult. Scler. 2011; 17: 411–422. http://doi.org/10.1177/1352458510394609

33. Beltrachini L., De Marco M., Taylor Z.A., Lotjonen J., Frangi A.F., Venneri A. Integration of cognitive tests and resting state fMRI for the individual identification of mild cognitive impairment. Curr. Alzheimer Res. 2015; 12: 592–603. http://doi.org/10.2174/156720501206150716120332

34. Selivjorstova E.V., Selivjorstov Ju.A., Konovalov R.N., Illarioshkin S.N. The role of functional rest MRI in the analysis of structural and functional changes in the brain in patients with Parkinson's disease. Russian Electronic Journal of Radiology (REJR). 2013; 3 (2): 418–419. (In Russian)

35. Di Perri C., Stender J., Laureys S., Gosseries O. Functional neuroanatomy of disorders of consciousness. Epilepsy & Behavior. 2014; 30: 28–32. http://dx.doi.org/10.1016/j.yebeh.2013.09.014

36. Vanhaudenhuyse A., Noirhomme Q., Tshibanda L.J., Bruno M.A., Boveroux P., Schnakers C., Soddu A., Perlbarg V., Ledoux D., Brichant J.F., Moonen G., Maquet P., Greicius M.D., Laureys S., Boly M. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain (A Journal of Neurology). 2010: 133 (1); 161–171. http://doi.org/10.1093/brain/awp313

37. Demertzi A., Antonopoulos G., Heine L., Voss H.U., Crone J.S., de Los Angeles C., Bahri M.A., Di Perri C., Vanhaudenhuyse A., Charland-Verville V., Kronbichler M., Trinka E., Phillips C., Gomez F., Tshibanda L., Soddu A., Schiff N.D., Whitfield-Gabrieli S., Laureys S. Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients. Brain. 2015; 138: 2619–2631. https://doi.org/10.1093/brain/awv169

38. Chen P., Xie Q., Wu X., Huang H., Lv W., Chen L., Guo Y., Zhang Sh., Hu H., Wang Y., Nie Y., Yu R., Huang R. Abnormal Effective Connectivity of the Anterior Forebrain Regions in Disorders of Consciousness. Neurosci. Bull. 2018; 34 (4): 647–658. https://doi.org/10.1007/s12264-018-0250-6

39. Pruim R.H.R., Mennes M., van Rooij D., Llera A., Buitelaar J.K., Beckmann C.F. ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data. NeuroImage. 2015; 112: 267–277. http://dx.doi.org/10.1016/j.neuroimage.2015.02.064

40. Salimi-Khorshidi G., Douaud G., Beckmann C.F., Glasser M.F., Griffanti L., Smith S.M. Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers. NeuroImage. 2014; 90: 449–468. http://dx.doi.org/10.1016/j.neuroimage.2013.11.046

41. Gavron A.A., Deza Araujo Y.I., Sharova E.V., Smirnov A.S., Knyazev G.G., Chelyapina M.V., Fadeeva L.M., Abdulaev A.A., Kulikov M.A., Zhavoronkova L.A., Boldyreva G.N., Verkhlyutov V.M., Pronin I.N. Healthy subjects group and individual resting state networks fMRI analysis. I.P. Pavlov Journal of Higher Nervous Activity = Zh Vyssh Nerv Deiat I.P. Pavlova. 2019; 69 (2):150–163. http://doi.org/10.1134/S0044467719020072 (In Russian)

42. Teasdale G., Jennet B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974; 2 (7872): 81–84.

43. Veis M., Zembatyi A.M. (eds). Fizioterapiya[Physiotherapy]. Moscow: Meditsina, 1986. 496 p. (In Russian)

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

45. Hyvärinen A., Oja E. Independent component analysis: algorithms and applications. Neural Netw. 2000; 13 (4–5): 411–430.

46. Dumas E.M., van den Bogaard S.J.A., Hart E.P., Soeter R.P., van Buchem M.A., van der Grond J., Rombouts S.A.R.B., Roos R.A.C. Reduced functional brain connectivity prior to and after disease onset in Huntington's disease. Neuroimage: Clinical. 2013; 2: 377–384. http://dx.doi.org/10.1016/j.nicl.2013.03.001

47. Widjaja E., Zamyadi M., Raybaud C., Snead O.C., Smith M.L. Impaired Default Mode Network on RestingState fMRI in Children with Medically Refractory Epilepsy. Am. J. Neuroradiol. 2013; 34 (3): 552–557. https://doi.org/10.3174/ajnr.A3265

48. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002; 3: 201–215. http://doi.org/10.1038/nrn755

49. Sharova E.V. Electrographic Correlates of Brain Reactions to Afferent Stimuli in Postcomatose Unconscious States after Severe Brain Injury. Hum. Physiol. 2005; 31 (3): 245–254.

50. Vainshenker Yu.I., Ivchenko I.M., Korotkov A.D., Melyucheva L.A., Kataeva G.V., Medvedev S.V. Vegetative State (Prolonged Coma) as Manifestation of Stable Pathological State. Fiziologiya cheloveka. 2010; 36 (1): 138–141. (In Russian)

51. Casarotto S., Comanducci A., Rosanova M., Sarasso S., Fecchio M., Napolitani M., Pigorini A., Casali A.G., Trimarchi P.D., Boly M., Gosseries O., Bodart O., Curto F., Landi C., Mariotti M., Devalle G., Laureys S., Tononi G., Massimini M. Stratification of Unresponsive Patients by an Independently Validated Index of Brain Complexity. Аnn. Neurol. 2016; 80: 718–729. http://doi.org/10.1002/ana.24779

52. Zhavoronkova L.A., Moraresku S.I., Boldyreva G.N., Sharova E.V., Kuptsova S.V., Smirnov A.S., Masherov E.L., Pronin I.N. Human Physiology = Fiziologiya Cheloveka. 2018; 44 (5): 2–9. http://doi.org/10.1134/S0131164618050168 (In Russian)

53. Boldyreva G.N., Yarets M.Y., Zhavoronkova L.A., Sharova E.V., Kuptsova S.V., Troshina E.M., Masherov E.L., Smirnov A.S. Motor fMRI responses of the brain in patients with mild post-traumatic hemiparesis. Novie informacionnie tehnologii v medicine, biologii, farmacologii I ecologii: Materials of the International Conference IT + M & Ec`2018, Gurzuf, June 1-11, 2019. Moscow: Publisher Institute of New Information Technologies Limited Liability Company, 2019: 140–143. (In Russian)

54. Gusnard D.A., Akbudak E., Shulman G.L., Raichle M.E. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc. Natl. Acad. Sci. USA. 2001; 98 (7): 4259–4264. http://doi.org/10.1073/pnas.071043098

55. Qin P., Northoff G. How is our self related to midline regions and the default-mode network? NeuroImage. 2011; 57: 1221–1233. http://doi.org/10.1016/j.neuroimage.2011.05.028

56. Sharova E.V., Kulikov M.A., Zaitsev O.S. The peculiarities of EEG dynamics during mental recovery after long-term posttraumatic coma. EEG and Clinical Neurophysiology. 1997; 103 (1): 207. (Abstracts of the 14th Intern. Congress of EEG and Clin. Neurophysiol., Florence, Italy). http://doi.org/10.1016/S0013-4694(97)88991-6


Review

For citations:


Sharova E.V., Kotovich J.V., Deza-Araujo Ya., Smirnov A.S., Gavron A.A., Fadeeva L.M., Chelyapina-Postnikova M.V., Alexandrova E.V., Zhavoronkova L.A., Boldyreva G.N., Verkhlyutov V.M., Kornienko V.N., Pronin I.N. fMRI resting state networks visualization in patients with severe traumatic brain injury. Medical Visualization. 2020;24(1):68-84. (In Russ.) https://doi.org/10.24835/1607-0763-2020-1-68-84

Views: 1328


ISSN 1607-0763 (Print)
ISSN 2408-9516 (Online)