Features of residual brain activity in patients with chronic disorders of consciousness on resting-state functional MRI
- 作者: Legostaeva L.1, Kremneva E.1, Sinitsyn D.1, Iazeva E.1, Sergeev D.1, Poydasheva A.1, Bakulin I.1, Lagoda D.1, Sergeeva A.1, Morozova S.1, Ryabinkina Y.1, Krotenkova M.1, Suponeva N.1, Piradov M.1
-
隶属关系:
- Research Center of Neurology
- 期: 卷 16, 编号 2 (2022)
- 页面: 15-24
- 栏目: Original articles
- URL: https://journals.rcsi.science/2075-5473/article/view/124047
- DOI: https://doi.org/10.54101/ACEN.2022.2.2
- ID: 124047
如何引用文章
全文:
详细
Introduction. Rapid advances in critical care medicine have led to an increased survival rate of patients with severe brain damage and, consequently, to an increased prevalence of chronic disorders of consciousness (CDC). The lack of or fluctuations in signs of consciousness, which accompany the restoration of alertness after recovery from coma, indicate whether the type of CDC is a vegetative state or minimally conscious state. Correct diagnosis determines not only the rehabilitation outcome but also the economic outlook for a particular patient. However, the subjective nature of signs of consciousness, which are identified during clinical examination using neurological scales, is a common cause of diagnostic errors. The study of spontaneous activity using resting-state functional magnetic resonance imaging (fMRI) has helped to identify resting state networks. The default mode network (DMN) is one of the most studied brain networks. Its signal can change or be absent in patients with various types of CDC.
Purpose. To study the signal of residual spontaneous brain activity in patients with CDC at rest.
Materials and methods. Twenty-two patients with permanent CDC underwent resting state fMRI as an additional tool in the differential diagnosis between vegetative state and minimally conscious state at the Research Centre of Neurology.
Results. It was found that the nature of the signal coming from anatomical regions that are part of the DMN changes when signs of consciousness emerge.
Conclusion. These changes confirm that resting state fMRI is an important additional tool for differential diagnosis of CDC types. Accumulating knowledge about the brain's functional state helps us to expand our overall understanding of the nature of consciousness.
作者简介
Liudmila Legostaeva
Research Center of Neurology
编辑信件的主要联系方式.
Email: legostaeva@neurology.ru
ORCID iD: 0000-0001-7778-6687
Cand. Sci. (Med.), researcher, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Elena Kremneva
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0001-9396-6063
Cand. Sci. (Med.), senior researcher, Radiology department
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Dmitry Sinitsyn
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0001-9951-9803
Cand. Sci. (Phys.-Math.), researcher, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Elizaveta Iazeva
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0003-0382-7719
neurologist, Intensive care unit
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Dmitry Sergeev
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0002-9130-1292
Cand. Sci. (Med.), neurologist, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Alexandra Poydasheva
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0003-1841-1177
junior researcher, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Ilya Bakulin
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0003-0716-3737
Cand. Sci. (Med.), researcher, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Dmitry Lagoda
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0002-9267-8315
junior researcher, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Anastasia Sergeeva
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0002-2481-4565
Cand. Sci. (Med.), researcher, Radiology department
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Sofya Morozova
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0002-9093-344X
Cand. Sci. (Med.), researcher, Neuroradiology department
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Yulia Ryabinkina
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0001-8576-9983
D. Sci. (Med.), Head, Intensive care unit department
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Marina Krotenkova
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0003-3820-4554
D. Sci. (Med.), Head, Radiology department
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Natalia Suponeva
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0003-3956-6362
D. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences, Head, Neurorehabilitation department with TMS group
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80Michail Piradov
Research Center of Neurology
Email: legostaeva@neurology.ru
ORCID iD: 0000-0002-6338-0392
D. Sci. (Med.), Professor, Academician of the Russian Academy of Sciences, Director
俄罗斯联邦, 125367, Russia, Moscow, Volokolamskoye shosse, 80参考
- Пирадов М.А., Супонева Н.А., Вознюк И.А. и др. Хронические нарушения сознания: терминология и диагностические критерии. Результаты первого заседания Российской рабочей группы по проблемам хронических нарушений сознания. Анналы клинической и экспериментальной неврологии. 2020; 14(1): 5–16. Piradov M.A., Suponeva N.A., Voznyuk I.A. et al. Russian workgroup on chronic disorders of consciousness. Chronic disorders of consciousness: terminology and diagnostic criteria. The results of the first meeting of the Russian Working Group for Chronic Disorders of Consciousness. Annals of clinical and experimental neurology. 2020; 14(1): 5–16. (In Russ.) doi: 10.25692/ACEN.2020.1.1
- Бакулин И.С., Кремнева Е.И., Кузнецов А.В. и др. Хронические нарушения сознания. Под ред. М.А. Пирадова. М., 2020. 288 с. Bakulin I.S., Kremneva E.I., Kuznetsov A.V. et al. Chronic disorders of consciousness. Ed. M.A. Piradov. Moscow, 2020. 288 p. (In Russ.)
- von Wild K., Laureys S.T., Gerstenbrand F. et al. The vegetative state — a syndrome in search of a name. J. Med. Life. 2012; 5(1): 3–15.
- Кондратьева Е.А., Авдунина И.А., Кондратьев А.Н. и др. Определение признаков сознания и прогнозирование исхода у пациентов в вегетативном состоянии. Вестник Российской академии медицинских наук. 2016; 71(4): 273–280. Kondratyeva E.А., Avdunina I.A., Kondratyev A.N. et al. Vegetative state: difficulty in identifying consciousness and predicting outcome. Annals of the Russian Academy of Medical Sciences. 2016; 71(4): 273–280. (In Russ.) doi: 10.15690/vramn728
- Cairns H. Head injuries in motor-cyclists the importance of the crash helmet. Br. Med. J. 1941; 2(4213): 465–471. doi: 10.1136/bmj.2.4213.465
- Thibaut A., Bodien Y.G, Laureys S., Giacino J.T. Minimally conscious state “plus”: diagnostic criteria and relation to functional recovery. J. Neurol. 2020; 267(5): 1245–1254. doi: 10.1007/s00415-019-09628
- Giacino J.T., Katz D.I., Schiff N.D., et al. Practice guideline update recommendations summary: disorders of consciousness: report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology; the American Congress of Rehabilitation Medicine; and the National Institute on Disability, Independent Living, and Rehabilitation Research. Arch. Phys. Med. Rehabil. 2018; 99(9): 1699–1709. doi: 10.1016/j.apmr.2018.07.001
- Wade D.T. How often is the diagnosis of the permanent vegetative state incorrect? A review of the evidence. Eur. J. Neurol. 2018; 25(4):619–625. doi: 10.1111/ene.13572
- Iazeva E G., Legostaeva L.A., Zimin A.A. et al. A Russian validation study of the Coma Recovery Scale-Revised (CRS-R). Brain Inj. 2018; 33(2): 218–225. doi: 10.1080/02699052.2018.1539248
- Пирадов М.А., Супонева Н.А., Селиверстов Ю.А. и др. Возможности современных методов нейровизуализации в изучении спонтанной активности головного мозга в состоянии покоя. Неврологический журнал. 2016; 21(1): 4–12. Piradov M.A., Suponeva N.A., Seliverstov Yu.A. et al. The opportunities of modern imaging methods in the study of spontaneous brain activity in state. Nevrologicheskiy Zhurnal. 2016; 21(1): 4–12. doi: 10.18821/1560-9545-2016-21-1-4-12
- Salvador R., Suckling J., Coleman M.R. et al. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb. Cortex. 2005; 15(9): 1332–1342. doi: 10.1093/cercor/bhi016
- Baars B.J., Banks W.P., Newman J.B. (eds.) Essential sources in the scientific study of consciousness. Cambridge, 2003. 1192 p.
- Owen A.M., Coleman M.R, Boly M. et al. Detecting awareness in the vegetative state. Science. 2006; 313(5792): 1402. doi: 10.1126/science.1130197
- Beckmann C.F., DeLuca M., Devlin J.T. et al. Investigations into res-ting-state connectivity using independent component analysis . Philos. Trans. R. Soc. B Biol. Sci. 2005; 360(1457): 1001–1013. doi: 10.1098/rstb.2005.1634
- Biswal B., Zerrin Yetkin F., 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(4): 537–541. doi: 10.1002/mrm.1910340409
- Blumenfeld H. Neuroanatomical basis of consciousness. Elsevier; 2016. doi: 10.1016/B978-0-12-800948-2.00001-7
- Crick F.C., Koch C. What is the function of the claustrum? Philos. Trans. R. Soc. B Biol. Sci. 2005; 360(1458): 1271–1279. doi: 10.1098/rstb.2005.1661
- Dreher J., Grafman J. The roles of the cerebellum and basal ganglia in timing and error prediction. Eur. J. Neurosci. 2002; 16(8): 1609–1619. doi: 10.1046/j.1460-9568.2002.02212.x
- van Erp W.S., Lavrijsen J.C.M., van de Laar F.A. et al. The vegetative state/unresponsive wakefulness syndrome: a systematic review of prevalence studies. Eur. J. Neurol. 2014; 21(11): 1361–1368. doi: 10.1111/ene.12483
- Medina J.P., Nigri A., Stanziano M. et al. Resting-state fMRI in chronic patients with disorders of consciousness: the role of lower-order networks for clinical assessment. Brain Sci. 2022; 12(3): 355. doi: 10.3390/brainsci12030355
- Damoiseaux J.S., Beckmann C.F., Sanz Arigita E.J. Reduced resting-state brain activity in the “default network” in normal aging. Cereb. Cortex. 2007; 18(8): 1856–1864. doi: 10.1093/cercor/bhm207
- Fransson P., Marrelec G. The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: evidence from a partial correlation network analysis. Neuroimage. 2008; 42(3): 1178–1184. doi: 10.1016/j.neuroimage.2008.05.059
- Giacino J., Kalmar K. Diagnostic and prognostic guidelines for the vegetative and minimally conscious states. Neuropsychol. Rehabil. 2005; 15(3–4): 166–174. doi: 10.1080/09602010443000498
- Demertzi A., Soddu A., Laureys S. Consciousness supporting networks. Curr. Opin. Neurobiol. 2013; 23(2): 239–244. doi: 10.1016/j.conb.2012.12.003
- Vincent J.L., Kahn I., Snyder A.Z. et al. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J. Neurophysiol. 2008; 100(6): 3328–3342. doi: 10.1152/jn.90355.2008
- Vanhaudenhuyse A., Demertzi A., Schabus M. et al. Two distinct neuronal networks mediate the awareness of environment and of self. J. Cogn. Neurosci. 2011; 23(3): 570–578. doi: 10.1162/jocn.2010.21488
- Heuvel M.P. van den, Pol H.E.H. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur. Neuropsychopharmacol. 2010; 20(8): 519–534. doi: 10.1016/j.euroneuro.2010.03.008
- Honey C.J., Sporns O., Cammoun L. et al. Predicting human resting-state functional connectivity from structural connectivity. Proc. Natl. Acad. Sci. U. S. A. 2009; 106(6): 2035–2040. doi: 10.1073/pnas.0811168106
- Schiff N.D. Modeling the minimally conscious state: measurements of brain function and therapeutic possibilities. Prog. Brain Res. 2005; 150: 473–610. doi: 10.1016/S0079-6123(05)50033-5
- Monti M.M., Schnakers C. To fMRI or not to fMRI? A flowchart translating guidelines for management of patients with disorders of consciousness into routine practice. PsyArXiv. 3 May 2021. doi: 10.31234/osf.io/cvx65
- Piradov M.A., Suponeva N.A., Ryabinkina Y.V. et al. Study of chronic post-comatose states: on the way to understanding the phenomenon of consciousness. Advances in cognitive research, artificial intelligence and neuroinformatics. In: Proceedings of the 9th International Conference on Cognitive Sciences, INTERCOGNSCI-2020. Moscow, 2020: 523–532. (In Russ.) doi: 10.1007/978-3-030-71637-0_60
- Edlow B.L. Covert consciousness: searching for volitional brain activity in the unresponsive. Curr. Biol. 2018; 28(23): R1345–R1348. doi: 10.1016/j.cub.2018.10.022
- Gębska-Kośla K., Głąbiński A., Sabiniewicz M. et al. The use of functional magnetic resonance imaging techniques in the evaluation of patients with disorders of consciousness: a case report. Pol. J. Radiol. 2020; 85: e118–e124. doi: 10.5114/pjr.2020.93664
- Thomson H. Hidden consciousness. New Scientist. 2019; 242(3236): 38–42.
- Cruse D., Owen A.M. Consciousness revealed: new insights into the vegetative and minimally conscious states. Curr. Opin. Neurol. 2010; 23(6): 656–660. doi: 10.1097/WCO.0b013e32833fd4e7
- Petrenko V.F., Mitina O.V., Suprun A.P. Conscious and unconscious cognition in psychosemantics. Psychology. Journal of Higher School of Economics. 2021; 18(4): 930–943. doi: 10.17323/1813-8918-2021-4-930-943
- Sontheimer A., Pontier B., Claise B. et al. Disrupted pallido-thalamo-cortical functional connectivity in chronic disorders of consciousness. Brain Sci. 2021; 11(3): 356. doi: 10.3390/brainsci11030356
- Northoff G., Lamme V. Neural signs and mechanisms of consciousness: is there a potential convergence of theories of consciousness in sight? Neurosci. Biobehav. Rev. 2020; 118: 568–587. doi: 10.1016/j.neubiorev.2020.07.019
- Qin P., Di H., Liu Y. et al. Anterior cingulate activity and the self in disorders of consciousness. Human Brain Mapp. 2010; 31(12): 1993–2002. doi: 10.1002/hbm.20989
- Shea N., Bayne T. The vegetative state and the science of consciousness. Br. J. Philos. Sci. 2020; 61(3): 459–484. doi: 10.1093/bjps/axp046
- Aubinet C., Larroque S.K., Heine L. et al. Clinical subcategorization of mini- mally conscious state according to resting functional connectivity. Human Brain Mapp. 2018; 39(11): 4519–4532. doi: 10.1002/hbm.24303
- Sanz L.R.D., Thibaut A., Edlow B.L. et al. Update on neuroimaging in disorders of consciousness. Curr. Opin. Neurol. 2021; 34(4): 488–496. doi: 10.1097/WCO.0000000000000951
- López-González A., Panda R., Ponce-Alvarez A. et al. Loss of consciousness reduces the stability of brain hubs and the heterogeneity of brain dynamics. Commun. Biol. 2021; 4(1): 1–15. doi: 10.1038/s42003-021-02537-9
- Horovitz S.G., Braun A.R., Carr W.S. et al. Decoupling of the brain’s default mode network during deep sleep. Proc. Natl. Acad. Sci. U. S. A. 2009; 106(27): 11376–11381. doi: 10.1073/pnas.0901435106
- Hong C.C.H., Fallon J.H., Friston K.J. fMRI evidence for default mode network deactivation associated with rapid eye movements in sleep. Brain Sci. 2021; 11(11): 1528. doi: 10.3390/brainsci11111528
- Larson-Prior L.J., Zempel J.M., Nolan T.S. et al. Cortical network functional connectivity in the descent to sleep. Proc. Natl. Acad. Sci. U. S. A. 2009; 106(11): 4489–4494. doi: 10.1073/pnas.0900924106
- Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 2005; 9(12): 556–559. doi: 10.1016/j.tics.2005.10.010
- Scheidegger M., Walter M., Lehmann M. et al. Ketamine decreases resting state functional network connectivity in healthy subjects: implications for antidepressant drug action. PLoS One. 2012; 7(9):e44799. doi: 10.1371/journal.pone.0044799
- Sarasso S., Boly M., Napolitani M. et al. Consciousness and complexity during unresponsiveness induced by propofol, xenon, and ketamine. Curr. Biol. 2015; 25(23): 3099–3105. doi: 10.1016/j.cub.2015.10.014
- Piorecky M., Koudelka V., Miletinova E. et al. Simultaneous fMRI-EEG-based characterisation of NREM parasomnia disease: methods and limitations. Diagnostics. 2020; 10(12): 1087. doi: 10.3390/diagnostics10121087
- Krauzlis R.J., Lovejoy L.P., Zénon A. Superior colliculus and visual spatial attention. Annu. Rev. Neurosci. 2013; 36: 165–182. doi: 10.1146/annurev-neuro-062012-170249
- Adhikari B., Deckert J., Hipp J. et al. T150. Evaluating the effects of keta- mine and midazolam using enigma resting state fMRI pipeline. Biol. Psychiatry. 2019; 85(10): S187. doi: 10.1016/j.biopsych.2019.03.473
- Scheidegger M., Walter M., Lehmann M. et al. Ketamine decreases resting state functional network connectivity in healthy subjects: implications for antidepressant drug action. PLoS One. 2012; 7(9): e44799. doi: 10.1371/journal.pone.0044799
- Forsyth A.E.M., McMillan R., Dukart J. et al. Effects of ketamine and mida- zolam on simultaneous EEG/fMRI data during working memory processes. Brain Topogr. 2021; 34(6): 863–880. doi: 10.1007/s10548-021-00876-8
- Mueller F., Musso F., London M. et al. Pharmacological fMRI: effects of subanesthetic ketamine on resting-state functional connectivity in the default mode network, salience network, dorsal attention network and executive control network. NeuroImage Clin. 2018; 19: 745–757. doi: 10.1016/j.nicl.2018.05.037
补充文件
![](/img/style/loading.gif)