Changes in event-related synchronization/desynchronization of brain electric activity in cardiosurgical patients with postoperative cognitive dysfunction

Aim of the study was to analyze the event-related synchronization/desynchronization of brain electrical activity during visual selection task in patients underwent on-pump coronary artery bypass grafting (CABG) with and without postoperative cognitive dysfunction (POCD). Material and methods. The study included 32 men who underwent on-pump CABG, mean age 57.2 ± 6.08 years. All patients carried out extended neuropsychological testing, a multi-channel computer electroencephalography (EEG) 3-5 days before CABG and on the 7-10th day after the surgery. The POCD was determined according to the criterion: 20 % decrease in the cognitive indicator compared to that at baseline on 20 % of the tests included in the neuropsychological battery. Monopolar EEGs were recorded in 62 sites of 10-20 system with NEUVO encephalograph (Compumedics, USA) during cognitive task performing in patients wi h and without POCD. Statistical processing was performed using the STATISTICA 10.0. Results. It was found that the POCD patients had less pronounced theta desynchronization in the left frontal-central regions during the stage of 200-400 ms at the 7-10 days after CABG in comparison to patients without cognitive decline. Moreover, in the left parietal leads POCD patients had decreased theta desynchronization during the stage of 200-400 ms even before the surgery. At the 7-10 days after CABG, only the patients without POCD had a decrease of event-related theta activity in the left parietal leads compared with baseline. During the stage of 600-800 ms, the POCD patients had a lower degree of theta-desynchronization of both frontal-central and parietal regions of right hemisphere compared to patients without cognitive decline. Conclusion. The cognitive decline in patients after CABG determined according to neuropsychological testing is accompanied by pathological changes in the event-related theta activity. An analysis of event-related synchronization/desynchronization can be used both as predictor of postoperative cognitive impairment and as objective marker of POCD.

1. Patel N., Minhas J.S., Chung E.M. Risk factors associated with cognitive decline after cardiac surgery: a systematic review. Cardiovasc. Psychiatry Neurol. 2015; 2015: 370612. doi: 10.1155/2015/370612

2. Тибекина Л.М., Смертина Е.Г., Золотов В.Д., Зайцева А.О., Крецу А.П., Столяров М.С., Каменских М.С., Старосоцкая М.В., Шматов Д.В. Факторы риска церебральных осложнений после кардиохирургических операций. Вестн. хирургии. 2017; 176 (3): 61–66. doi: 10.24884/0042-4625-2017-176-3-61- 66 Tibekina L.M., Smertina E.G., Zolotov V.D., Zaitseva A.O., Kretsu A.P., Stolyarov M.S., Kamenskikh M.S., Starosotskaya M.V., Shmatov D.V. Risk factors of cerebral complications after cardiac surgery. Vestnik khirurgii imeni Ivana Ivanovicha Grekova = Grekov’s Bulletin of Surgery. 2017; 176 (3): 61–66. [In Russian]. doi: 10.24884/0042-4625-2017-176-3-61-66

3. Bhamidipati D., Goldhammer J.E., Sperling M.R., Torjman M.C., McCarey M.M., Whellan D.J. Cognitive outcomes after coronary artery bypass grafting. J. Cardiothorac. Vasc. Anesth. 2017; 31 (2): 707–718. doi: 10.1053/j.jvca.2016.09.028

4. Indja B., Seco M., Seamark R., Kaplan J., Bannon P.G., Grieve S.M., Vallely M.P. Neurocognitive and psychiatric issues post cardiac surgery. Heart Lung Circ. 2017; 26 (8): 779–785. doi: 10.1016/j.hlc.2016.12.010

5. Evered L., Silbert B., Knopman D.S., Scott D.A., DeKosky S.T., Rasmussen L.S., Oh E.S., Crosby G., Berger M., Eckenhoff R.G.; Nomenclature Consensus Working Group. Recommendations for the nomenclature of cognitive change associated with anaesthesia and surgery-2018. Br. J. Anaesth. 2018; 121 (5): 1005–1012. doi: 10.1016/j.bja.2017.11.087

6. Fraga F.J., Mamani G.Q., Johns E., Tavares G., Falk T.H., Phillips N.A. Early diagnosis of mild cognitive impairment and Alzheimer’s with eventrelated potentials and event-related desynchronization in N-back working memory tasks. Comput. Methods Programs Biomed. 2018; 164: 1–13. doi: 10.1016/j.cmpb.2018.06.011

7. Erickson M.A., Smith D., Albrecht M.A., Silverstein S. Alpha-band desynchronization reflects memory-specific processes during visual change detection. Psychophysiology. 2019; 56 (11): 13442. doi: 10.1111/psyp.13442

8. Gorelick P.B., Scuteri A., Black S.E., Decarli C., Greenberg S.M., Iadecola C., Launer L.J., Laurent S., Lopez O.L., Nyenhuis D., Petersen R.C., Schneider J.A., Tzourio C., Arnett D.K., Bennett D.A., Chui H.C., Higashida R.T., Lindquist R., Nilsson P.M., Roman G.C., Sellke F.W., Seshadri S., American heart association stroke council, Council on epidemiology and prevention, council on cardiovascular nursing, Council on cardiovascular radiology and intervention, and Council on cardiovascular surgery and anesthesia. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American heart association / American stroke association. Stroke. 2011; 42 (9): 2672. doi: 10.1161/STR.0b013e3182299496

9. Gasparovic C., Prestopnik J., Thompson J., Taheri S., Huisa B., Schrader R., Adair J.C., Rosenberg G.A. 1H-MR spectroscopy metabolite levels correlate with executive function in vascular cognitive impairment. J. Neurol. Neurosurg. Psychiatry. 2013; 84 (7): 715–721. doi: 10.1136/jnnp-2012-303878

10. Waragai M., Moriya M., Nojo T. Decreased N-acetyl aspartate/myo-inositol ratio in the posterior cingulate cortex shown by magnetic resonance spectroscopy may be one of the risk markers of preclinical Alzheimer’s disease: A 7-Year Follow-Up Study. J. Alzheimers Dis. 2017; 60 (4): 1411–1427. doi: 10.3233/JAD-170450

11. Sheremata S.L., Somers D.C., Shomstein S. Visual short-term memory activity in parietal lobe reflects cognitive processes beyond attentional selection. J. Neurosci. 2018; 38 (6): 1511–1519. doi: 10.1523/JNEUROSCI.1716-17.2017

12. Fellows L.K. The neuroscience of human decision-making through the lens of learning and memory. Curr. Top. Behav. Neurosci. 2018; 37: 231–251. doi: 10.1007/7854_2016_468

13. Yu Q., Shim W.M. Occipital, parietal, and frontal cortices selectively maintain task-relevant features of multi-feature objects in visual working memory. Neuroimage. 2017; 157: 97–107. doi: 10.1016/j.neuroimage.2017.05.055

14. Verleger R., Grauhan N., Śmigasiewicz K. Is P3 a strategic or a tactical component? Relationships of P3 sub-components to response times in oddball tasks with go, no-go and choice responses. Neuroimage. 2016; 143: 223–234. doi: 10.1016/j.neuroimage.2016.08.049

15. Karamacoska D., Barry R.J., Steiner G.Z. Resting state intrinsic EEG impacts on go stimulus-response processes. Psychophysiology. 2017; 54 (6): 894–903. doi: 10.1111/psyp.1285

16. Афтанас Л.И., Пустовойт С.М., Новожилова Н.В., Ахметова О.А., Овчинников А.А. Индивидуальный баланс оборонительной и подкрепляющей мотивационных систем мозга как вероятный нейрофизиологический эндофенотип депрессии в метрике когнитивных вызванных потенциалов. Сиб. науч. мед. журн. 2019; 39 (1): 13–20. doi:10.15372/SSMJ20190102 Aftanas L.I., Pustovoyt S.M., Novozhilova N.V., Akhmetova O.A., Ovchinnikov A.A. Individual balance of defensive and appetitive motivational systems of the brain as a likely neurophysiological endophenotype of depression in the metric of cognitive evoked potentials. Sibirskiy nauchnyy meditsinskiy zhurnal = Siberian Scientific Medical Journal. 2019; 39 (1): 13–20. [In Russian]. doi:10.15372/SSMJ20190102

17. Milner R., Rusiniak M., Lewandowska M., Wolak T., Ganc M., Piątkowska-Janko E., Bogorodzki P., Skarżyński H. Towards neural correlates of auditory stimulus processing: a simultaneous auditory evoked potentials and functional magnetic resonance study using an odd-ball paradigm. Med. Sci. Monit. 2014; 20: 35–46. doi: 10.12659/MSM.889712

18. Tarasova I.V., Trubnikova O.A., Barbarash O.L. EEG and clinical factors associated with mild cognitive impairment in coronary artery disease patients. Dement. Geriatr. Cogn. Disord. 2018; 46 (5-6): 275–284. doi: 10.1159/000493787

19. Тарасова И.В. Значение фоновой электроэнцефалограммы для диагностики когнитивных расстройств у кардиохирургических пациентов. Сиб. мед. журн. (Томск). 2019; 34 (1): 18–23. doi:10.29001/2073-8552-2019-34-1-18-23 Tаrаsovа I.V. Significance of resting state electroencephalogram for diagnosis of cognitive disorders in cardiac surgery patients. Sibirskiy meditsinskiy zhurnal (Tomsk) = Siberian Medical Journal (Tomsk). 2019; 34 (1): 18–23. [In Russian]. doi:10.29001/2073-8552-2019-34-1-18-23

20. Beck A.T., Steer R.A., Brown G.K. Beck depression inventory. 2nd edition manual. New York: The Psychological Corporation, 1996. 38 p.

21. Spielberger C.D., Gorsuch R.L., Lushene R.E. State-Trait Anxiety Inventory for adults: sampler set: manual, test, scoring key. Redwood City, CA: Mind Garden, 1983. 70 p.

22. Трубникова О.А., Тарасова И.В., Мамонтова А.С., Сырова И.Д., Малева О.В., Барбараш О.Л. Структура когнитивных нарушений и динамика биоэлектрической активности мозга у пациентов после прямой реваскуляризации миокарда. Рос. кардиол. ж. 2014; (8): 57–62. doi: 10.15829/1560-4071-2014-8-57-62 Trubnikova O.A., Tarasova I.V., Mamontova A.S., Syrova I.D., Maleva O.V., Barbarash O.L. Structure of cognitive disorders and dynamics of bioelectric activity of the brain in patients after direct myocardial revascularization. Rossiyskiy kardiologicheskiy zhurnal = Russian Journal of Cardiology. 2014; (8): 57–62. [In Russian]. doi: 10.15829/1560-4071-2014-8-57-62

23. Cross-Villasana F., Finke K., HennigFast K., Kilian B., Wiegand I., Müller H.J., Möller H.J., Töllner T. The speed of visual attention and motor-response decisions in adult attention-deficit/ hyperactivity disorder. Biol. Psychiatry. 2015; 78 (2): 107–115. doi: 10.1016/j.biopsych.2015.01.016

24. Orme E., Brown L.A., Riby L.M. Retrieval and monitoring processes during visual working memory: an ERP study of the benefit of visual semantics. Front. Psychol. 2017; (8): 1080. doi: 10.3389/fpsyg.2017.01080

25. Приводнова Е.Ю., Вольф Н.В. Особенности временнóй динамики осцилляторной активности мозга при решении творческой задачи у молодых и пожилых испытуемых. Физиол. человека. 2016; 42 (5): 5–12. doi: 10.7868/S0131164616050131 Privodnova E.Yu., Volf N.V. Features of temporal dynamics of oscillatory brain activity during creative problem solving in young and elderly adults. Fiziologiya cheloveka = Human Physiology (Hum. Physiol.). 2016; 42 (5): 469–475. [In Russian]. doi: 10.7868/S0131164616050131

26. Гнездицкий В.В., Чацкая А.В., Корепина О.С., Клочкова О.И. Оценка объема оперативной памяти по данным эндогенных вызванных потенциалов (метод Р300) без психологического тестирования. Анналы клин. и эксперим. неврол. 2016; 10 (1): 27–34. Gnezditskiy V.V., Chatskaya A.V., Korepina O.S., Klochkova O.I. Assessment of the operative memory capacity based on endogenous evoked potentials (P300 method) without neuropsychological testing. Annaly klinicheskoy i eksperimental’noy nevrologii = Annals of Clinical and Experimental Neurology. 2016; 10 (1): 27–34. [In Russian].

27. Wang Y., Liu G., Hong D., Chen F., Ji X., Cao G. White matter injury in ischemic stroke. Prog. Neurobiol. 2016; 141: 45–60. doi: 10.1016/j.pneurobio.2016.04.005

28. Weinstein G.S. Left hemispheric strokes in coronary surgery: implications for end-hole aortic cannulas. Ann. Thorac. Surg. 2001; 71 (1): 128–132. doi: 10.1016/s0003-4975(00)02208-6

29. Messerotti Benvenuti S., Zanatta P., Valfrè C., Polesel E., Palomba D. Preliminary evidence for reduced preoperative cerebral blood flow velocity as a risk factor for cognitive decline three months after cardiac surgery: an extension study. Perfusion. 2012; 27 (6): 486-492. doi: 10.1177/0267659112453475

30. Zanatta P., Messerotti Benvenuti S., Valfrè C., Baldanzi F., Palomba D. The role of asymmetry and the nature of microembolization in cognitive decline after heart valve surgery: a pilot study. Perfusion. 2012; 27 (3): 199–206. doi: 10.1177/0267659112437776

31. Ponomareva N., Klyushnikov S., Abramycheva N., Malina D., Scheglova N., Fokin V., Ivanova-Smolenskaia I., Illarioshkin S. Alpha-theta border EEG abnormalities in preclinical Huntington’s disease. J. Neurol. Sci. 2014; 344 (1-2): 114–120. doi: 10.1016/j.jns.2014.06.035

32. van den Berg E., Geerlings M.I., Biessels G.J., Nederkoorn P.J., Kloppenborg R.P. White matter hyperintensities and cognition in mild cognitive impairment and Alzheimer’s disease: a domain-specific meta-analysis. J. Alzheimers Dis. 2018; 63 (2): 515– 527. doi: 10.3233/JAD-170573

33. Uhlhaas P.J., Haenschel C., Nikolić D., Singer W. The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr. Bull. 2008; 34 (5): 927–943. doi: 10.1093/schbul/sbn062