Current progress on characteristics of intracranial electrophysiology related to prolonged disorders of consciousness_Journal of Biomedical Engineering

Authors：

 HUANG Yongzhi ¹ , WU Jiarou ¹ , XU Minpeng ^1,2 , HE Jianghong ³ , MING Dong ^1,2

1. Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin 300072, P. R. China;
2. School of Precision Instrument and Optoelectronics Engineering, Tianjin University, Tianjin 300072, P. R. China;
3. Department of Neurosurgery, Beijing Tiantan Hospital Affiliated to Capital Medical University, Beijing 100070, P. R. China;

Corresponding author：

HUANG Yongzhi, Email: yongzhi_huang@tju.edu.cn

Keywords：

Prolonged disorders of consciousness; Spike; Local field potential; Intracranial electrophysiology

DOI：

10.7507/1001-5515.202403023

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Prolonged disorders of consciousness (pDOC) are pathological conditions of alterations in consciousness caused by various severe brain injuries, profoundly affecting patients’ life ability and leading to a huge burden for both the family and society. Exploring the mechanisms underlying pDOC and accurately assessing the level of consciousness in the patients with pDOC provide the basis of developing therapeutic strategies. Research of non-invasive functional neuroimaging technologies, such as functional magnetic resonance (fMRI) and scalp electroencephalography (EEG), have demonstrated that the generation, maintenance and disorders of consciousness involve functions of multiple cortical and subcortical brain regions, and their networks. Invasive intracranial neuroelectrophysiological technique can directly record the electrical activity of subcortical or cortical neurons with high signal-to-noise ratio and spatial resolution, which has unique advantages and important significance for further revealing the brain function and disease mechanism of pDOC. Here we reviewed the current progress of pDOC research based on two intracranial electrophysiological signals, spikes reflecting single-unit activity and field potential reflecting multi-unit activities, and then discussed the current challenges and gave an outlook on future development, hoping to promote the study of pathophysiological mechanisms related to pDOC and provide guides for the future clinical diagnosis and therapy of pDOC.

Citation： HUANG Yongzhi, WU Jiarou, XU Minpeng, HE Jianghong, MING Dong. Current progress on characteristics of intracranial electrophysiology related to prolonged disorders of consciousness. Journal of Biomedical Engineering, 2024, 41(4): 826-832. doi: 10.7507/1001-5515.202403023 Copy

1.	何超, 吴海涛. 重型颅脑创伤后慢性意识障碍促醒治疗研究进展. 中国医药导报, 2021, 18(27): 47-50.
2.	Bodien Y G, Katz D I, Schiff N D, et al. Behavioral assessment of patients with disorders of consciousness. Semin Neurol, 2022, 42(03): 249-258.
3.	Edlow B L, Sanz L R D, Polizzotto L, et al. Therapies to restore consciousness in patients with severe brain injuries: a gap analysis and future directions. Neurocrit Care, 2021, 35: 68-85.
4.	Driessen D M F, Utens C M A, Ribbers G M, et al. Outcome registry of early intensive neurorehabilitation in patients with disorders of consciousness: study protocol of a prospective cohort study. BMC Neurol, 2021, 21: 1-10.
5.	Raguž M, Predrijevac N, Dlaka D, et al. Structural changes in brains of patients with disorders of consciousness treated with deep brain stimulation. Sci Rep, 2021, 11(1): 4401.
6.	Jang S H, Choi E B. Differences in the thalamocortical tract of the ascending reticular activating system in disorders of consciousness after hypoxic-ischemic brain injury: A pilot study. Medicine, 2022, 101(35): 30199.
7.	Shine J M. The thalamus integrates the macrosystems of the brain to facilitate complex, adaptive brain network dynamics. Prog Neurobiol, 2021, 199: 101951.
8.	Thibaut A, Panda R, Annen J, et al. Preservation of brain activity in unresponsive patients identifies MCS star. Ann Neurol, 2021, 90(1): 89-100.
9.	Edlow B L, Claassen J, Schiff N D, et al. Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nat Rev Neurol, 2021, 17(3): 135-156.
10.	Panda R, Thibaut A, Lopez-Gonzalez A, et al. Disruption in structural–functional network repertoire and time-resolved subcortical fronto-temporoparietal connectivity in disorders of consciousness. Elife, 2022, 11: 77462.
11.	Mashour G A, Palanca B J, Basner M, et al. Recovery of consciousness and cognition after general anesthesia in humans. Elife, 2021, 10: 59525.
12.	Dung L, Newen A J C. Profiles of animal consciousness: A species-sensitive, two-tier account to quality and distribution. Cognition, 2023, 235: 105409.
13.	Chen Y, Li S, Wu F, et al. Altered functional and directed connectivity in propofol-induced loss of consciousness: A source-space resting-state EEG study. Clin Neurophysiol, 2022, 142: 209-219.
14.	Huels E R, Groenhout T, Fields C W, et al. Inactivation of prefrontal cortex delays emergence from sevoflurane anesthesia. Front Syst Neurosci, 2021, 15: 690717.
15.	Magrassi L, Zippo A G, Azzalin A, et al. Single unit activities recorded in the thalamus and the overlying parietal cortex of subjects affected by disorders of consciousness. PLoS One, 2018, 13(11): 0205967.
16.	Redinbaugh M J, Phillips J M, Kambi N A, et al. Thalamus modulates consciousness via layer-specific control of cortex. Neuron, 2020, 106(1): 66-75.
17.	He J, Zhang H, Dang Y, et al. Electrophysiological characteristics of CM-pf in diagnosis and outcome of patients with disorders of consciousness. Brain Stimul, 2023, 16(5): 1522-1532.
18.	Lee H, Wang S, Hudetz A G. State-dependent cortical unit activity reflects dynamic brain state transitions in anesthesia. J Neurosci, 2020, 40(49): 9440-9454.
19.	Patel P R, Welle E J, Letner J G, et al. Utah array characterization and histological analysis of a multi-year implant in non-human primate motor and sensory cortices. J Neural Eng, 2023, 20(1): 014001.
20.	Huang Y, He J, Green A L, et al. Characteristics of thalamic local field potentials in patients with disorders of consciousness// Proceedings of the 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). Milan: IEEE, 2015: 3779-3782.
21.	Schroeder K E, Irwin Z T, Gaidica M, et al. Disruption of corticocortical information transfer during ketamine anesthesia in the primate brain. Neuroimage, 2016, 134: 459-465.
22.	Kundishora A J, Gummadavelli A, Ma C, et al. Restoring conscious arousal during focal limbic seizures with deep brain stimulation. Cereb Cortex, 2017, 27(3): 1964-1975.
23.	Xu J, Galardi M M, Pok B, et al. Thalamic stimulation improves postictal cortical arousal and behavior. J Neurosci, 2020, 40(38): 7343-7354.
24.	Ching S, Brown E N. Modeling the dynamical effects of anesthesia on brain circuits. Curr Opin Neurobiol, 2014, 25: 116-122.
25.	Wojtecki L, Petri D, Elben S, et al. Modulation of central thalamic oscillations during emotional-cognitive processing in chronic disorder of consciousness. Cortex, 2014, 60: 94-102.
26.	Bastos A M, Donoghue J A, Brincat S L, et al. Neural effects of propofol-induced unconsciousness and its reversal using thalamic stimulation. Elife, 2021, 10: 60824.
27.	Krom A J, Marmelshtein A, Gelbard-Sagiv H, et al. Anesthesia-induced loss of consciousness disrupts auditory responses beyond primary cortex. Proc Natl Acad Sci U S A, 2020, 117(21): 11770-11780.
28.	Mofakham S, Fry A, Adachi J, et al. Electrocorticography reveals thalamic control of cortical dynamics following traumatic brain injury. Commun Biol, 2021, 4(1): 1210.
29.	Lange N, Schleifer S, Berndt M, et al. Permutation entropy in intraoperative ECoG of brain tumour patients in awake tumour surgery–a robust parameter to separate consciousness from unconsciousness. Sci Rep, 2019, 9(1): 16482.
30.	Wang Z, Zhang F, Yue L, et al. Utah array characterization and histological analysis of a multi-year implant in non-human primate motor and sensory cortices. J Neural Eng, 2022, 19(3): 036009.
31.	Afrasiabi M, Redinbaugh M J, Phillips J M, et al. Consciousness depends on integration between parietal cortex, striatum, and thalamus. Cell Syst, 2021, 12(4): 363-373.
32.	Jiang X, Wen X, Ou G, et al. Propofol modulates neural dynamics of thalamo-cortical system associated with anesthetic levels in rats. Cogn Neurodyn, 2023, 17(6): 1541-1559.
33.	Huang Y, Hu K, Green A L, et al. Dynamic changes in rhythmic and arrhythmic neural signatures in the subthalamic nucleus induced by anaesthesia and tracheal intubation. Br J Anaesth, 2020, 125(1): 67-76.
34.	Muthukumaraswamy S D, Liley D T J. 1/f electrophysiological spectra in resting and drug-induced states can be explained by the dynamics of multiple oscillatory relaxation processes. Neuroimage, 2018, 179: 582-595.
35.	Coste J, Pontier B, Sontheimer A, et al. Intraoperative electrophysiology during deep brain surgeries in disorders of consciousness// 24th Congress, European Society for Stereotactic and Functional Neurosurgery. Marseille: ESSFN, 2021, 99: 1342.
36.	Servider J, Saadon J R, Adachi J, et al. Cortical recordings reveal hidden early signs of recovery following traumatic brain injury: A case report. Brain Res, 2022, 1786: 147903.
37.	De La Fuente L A, Zamberlan F, Bocaccio H, et al. Temporal irreversibility of neural dynamics as a signature of consciousness. Cereb Cortex, 2023, 33(5): 1856-1865.
38.	Schmidt D, English G, Gent T, et al. Electrocorticography based monitoring of anaesthetic depth in mice. bioRxiv, 2021: 452032.
39.	Huang Y, Wu D, Bahuri N A, et al. Spectral and phase-amplitude coupling signatures in human deep brain oscillations during propofol-induced anaesthesia. Br J Anaesth, 2018, 121(1): 303-313.
40.	Kantserova A, Oknina L, Pitskhelauri D, et al. Evoked potentials of the midbrain associated with the beginning and end of a sound of a simple tone. Hum Physiol, 2022, 48(3): 229-236.
41.	Müller E J, Munn B R, Redinbaugh M J, et al. The non-specific matrix thalamus facilitates the cortical information processing modes relevant for conscious awareness. Cell Rep, 2023, 42(8): 112844.
42.	Liang Z, Cheng L, Shao S, et al. Information integration and mesoscopic cortical connectivity during propofol anesthesia. Anesthesiology, 2020, 132(3): 504-524.
43.	Liang Z, Jin X, Ren Y, et al. Propofol anesthesia decreased the efficiency of long-range cortical interaction in humans. IEEE Trans Biomed Eng, 2021, 69(1): 165-175.
44.	Lord L D, Carletti T, Fernandes H, et al. Altered dynamical integration/segregation balance during anesthesia-induced loss of consciousness. Front Netw Physiol, 2023, 3: 1279646.
45.	Xie T, Chen K, Ma L, et al. Brain connectivity analysis in anesthetized and awake states: An ECoG study in monkeys// Proceedings of the 2021 43rd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC). Seattle: IEEE, 2021: 117-120.
46.	Northoff G, Zilio F. Temporo-spatial Theory of Consciousness (TTC)–Bridging the gap of neuronal activity and phenomenal states. Behav Brain Res, 2022, 424: 113788.
47.	Oberholzer M, Müri R M. Neurorehabilitation of traumatic brain injury (TBI): a clinical review. Med Sci (Basel), 2019, 7(3): 47.
48.	Fleming J E, Dunn E, Lowery M M. Simulation of closed-loop deep brain stimulation control schemes for suppression of pathological beta oscillations in Parkinson’s disease. Front Neurosci, 2020, 14: 166.

1. 何超, 吴海涛. 重型颅脑创伤后慢性意识障碍促醒治疗研究进展. 中国医药导报, 2021, 18(27): 47-50.
2. Bodien Y G, Katz D I, Schiff N D, et al. Behavioral assessment of patients with disorders of consciousness. Semin Neurol, 2022, 42(03): 249-258.
3. Edlow B L, Sanz L R D, Polizzotto L, et al. Therapies to restore consciousness in patients with severe brain injuries: a gap analysis and future directions. Neurocrit Care, 2021, 35: 68-85.
4. Driessen D M F, Utens C M A, Ribbers G M, et al. Outcome registry of early intensive neurorehabilitation in patients with disorders of consciousness: study protocol of a prospective cohort study. BMC Neurol, 2021, 21: 1-10.
5. Raguž M, Predrijevac N, Dlaka D, et al. Structural changes in brains of patients with disorders of consciousness treated with deep brain stimulation. Sci Rep, 2021, 11(1): 4401.
6. Jang S H, Choi E B. Differences in the thalamocortical tract of the ascending reticular activating system in disorders of consciousness after hypoxic-ischemic brain injury: A pilot study. Medicine, 2022, 101(35): 30199.
7. Shine J M. The thalamus integrates the macrosystems of the brain to facilitate complex, adaptive brain network dynamics. Prog Neurobiol, 2021, 199: 101951.
8. Thibaut A, Panda R, Annen J, et al. Preservation of brain activity in unresponsive patients identifies MCS star. Ann Neurol, 2021, 90(1): 89-100.
9. Edlow B L, Claassen J, Schiff N D, et al. Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nat Rev Neurol, 2021, 17(3): 135-156.
10. Panda R, Thibaut A, Lopez-Gonzalez A, et al. Disruption in structural–functional network repertoire and time-resolved subcortical fronto-temporoparietal connectivity in disorders of consciousness. Elife, 2022, 11: 77462.
11. Mashour G A, Palanca B J, Basner M, et al. Recovery of consciousness and cognition after general anesthesia in humans. Elife, 2021, 10: 59525.
12. Dung L, Newen A J C. Profiles of animal consciousness: A species-sensitive, two-tier account to quality and distribution. Cognition, 2023, 235: 105409.
13. Chen Y, Li S, Wu F, et al. Altered functional and directed connectivity in propofol-induced loss of consciousness: A source-space resting-state EEG study. Clin Neurophysiol, 2022, 142: 209-219.
14. Huels E R, Groenhout T, Fields C W, et al. Inactivation of prefrontal cortex delays emergence from sevoflurane anesthesia. Front Syst Neurosci, 2021, 15: 690717.
15. Magrassi L, Zippo A G, Azzalin A, et al. Single unit activities recorded in the thalamus and the overlying parietal cortex of subjects affected by disorders of consciousness. PLoS One, 2018, 13(11): 0205967.
16. Redinbaugh M J, Phillips J M, Kambi N A, et al. Thalamus modulates consciousness via layer-specific control of cortex. Neuron, 2020, 106(1): 66-75.
17. He J, Zhang H, Dang Y, et al. Electrophysiological characteristics of CM-pf in diagnosis and outcome of patients with disorders of consciousness. Brain Stimul, 2023, 16(5): 1522-1532.
18. Lee H, Wang S, Hudetz A G. State-dependent cortical unit activity reflects dynamic brain state transitions in anesthesia. J Neurosci, 2020, 40(49): 9440-9454.
19. Patel P R, Welle E J, Letner J G, et al. Utah array characterization and histological analysis of a multi-year implant in non-human primate motor and sensory cortices. J Neural Eng, 2023, 20(1): 014001.
20. Huang Y, He J, Green A L, et al. Characteristics of thalamic local field potentials in patients with disorders of consciousness// Proceedings of the 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC). Milan: IEEE, 2015: 3779-3782.
21. Schroeder K E, Irwin Z T, Gaidica M, et al. Disruption of corticocortical information transfer during ketamine anesthesia in the primate brain. Neuroimage, 2016, 134: 459-465.
22. Kundishora A J, Gummadavelli A, Ma C, et al. Restoring conscious arousal during focal limbic seizures with deep brain stimulation. Cereb Cortex, 2017, 27(3): 1964-1975.
23. Xu J, Galardi M M, Pok B, et al. Thalamic stimulation improves postictal cortical arousal and behavior. J Neurosci, 2020, 40(38): 7343-7354.
24. Ching S, Brown E N. Modeling the dynamical effects of anesthesia on brain circuits. Curr Opin Neurobiol, 2014, 25: 116-122.
25. Wojtecki L, Petri D, Elben S, et al. Modulation of central thalamic oscillations during emotional-cognitive processing in chronic disorder of consciousness. Cortex, 2014, 60: 94-102.
26. Bastos A M, Donoghue J A, Brincat S L, et al. Neural effects of propofol-induced unconsciousness and its reversal using thalamic stimulation. Elife, 2021, 10: 60824.
27. Krom A J, Marmelshtein A, Gelbard-Sagiv H, et al. Anesthesia-induced loss of consciousness disrupts auditory responses beyond primary cortex. Proc Natl Acad Sci U S A, 2020, 117(21): 11770-11780.
28. Mofakham S, Fry A, Adachi J, et al. Electrocorticography reveals thalamic control of cortical dynamics following traumatic brain injury. Commun Biol, 2021, 4(1): 1210.
29. Lange N, Schleifer S, Berndt M, et al. Permutation entropy in intraoperative ECoG of brain tumour patients in awake tumour surgery–a robust parameter to separate consciousness from unconsciousness. Sci Rep, 2019, 9(1): 16482.
30. Wang Z, Zhang F, Yue L, et al. Utah array characterization and histological analysis of a multi-year implant in non-human primate motor and sensory cortices. J Neural Eng, 2022, 19(3): 036009.
31. Afrasiabi M, Redinbaugh M J, Phillips J M, et al. Consciousness depends on integration between parietal cortex, striatum, and thalamus. Cell Syst, 2021, 12(4): 363-373.
32. Jiang X, Wen X, Ou G, et al. Propofol modulates neural dynamics of thalamo-cortical system associated with anesthetic levels in rats. Cogn Neurodyn, 2023, 17(6): 1541-1559.
33. Huang Y, Hu K, Green A L, et al. Dynamic changes in rhythmic and arrhythmic neural signatures in the subthalamic nucleus induced by anaesthesia and tracheal intubation. Br J Anaesth, 2020, 125(1): 67-76.
34. Muthukumaraswamy S D, Liley D T J. 1/f electrophysiological spectra in resting and drug-induced states can be explained by the dynamics of multiple oscillatory relaxation processes. Neuroimage, 2018, 179: 582-595.
35. Coste J, Pontier B, Sontheimer A, et al. Intraoperative electrophysiology during deep brain surgeries in disorders of consciousness// 24th Congress, European Society for Stereotactic and Functional Neurosurgery. Marseille: ESSFN, 2021, 99: 1342.
36. Servider J, Saadon J R, Adachi J, et al. Cortical recordings reveal hidden early signs of recovery following traumatic brain injury: A case report. Brain Res, 2022, 1786: 147903.
37. De La Fuente L A, Zamberlan F, Bocaccio H, et al. Temporal irreversibility of neural dynamics as a signature of consciousness. Cereb Cortex, 2023, 33(5): 1856-1865.
38. Schmidt D, English G, Gent T, et al. Electrocorticography based monitoring of anaesthetic depth in mice. bioRxiv, 2021: 452032.
39. Huang Y, Wu D, Bahuri N A, et al. Spectral and phase-amplitude coupling signatures in human deep brain oscillations during propofol-induced anaesthesia. Br J Anaesth, 2018, 121(1): 303-313.
40. Kantserova A, Oknina L, Pitskhelauri D, et al. Evoked potentials of the midbrain associated with the beginning and end of a sound of a simple tone. Hum Physiol, 2022, 48(3): 229-236.
41. Müller E J, Munn B R, Redinbaugh M J, et al. The non-specific matrix thalamus facilitates the cortical information processing modes relevant for conscious awareness. Cell Rep, 2023, 42(8): 112844.
42. Liang Z, Cheng L, Shao S, et al. Information integration and mesoscopic cortical connectivity during propofol anesthesia. Anesthesiology, 2020, 132(3): 504-524.
43. Liang Z, Jin X, Ren Y, et al. Propofol anesthesia decreased the efficiency of long-range cortical interaction in humans. IEEE Trans Biomed Eng, 2021, 69(1): 165-175.
44. Lord L D, Carletti T, Fernandes H, et al. Altered dynamical integration/segregation balance during anesthesia-induced loss of consciousness. Front Netw Physiol, 2023, 3: 1279646.
45. Xie T, Chen K, Ma L, et al. Brain connectivity analysis in anesthetized and awake states: An ECoG study in monkeys// Proceedings of the 2021 43rd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC). Seattle: IEEE, 2021: 117-120.
46. Northoff G, Zilio F. Temporo-spatial Theory of Consciousness (TTC)–Bridging the gap of neuronal activity and phenomenal states. Behav Brain Res, 2022, 424: 113788.
47. Oberholzer M, Müri R M. Neurorehabilitation of traumatic brain injury (TBI): a clinical review. Med Sci (Basel), 2019, 7(3): 47.
48. Fleming J E, Dunn E, Lowery M M. Simulation of closed-loop deep brain stimulation control schemes for suppression of pathological beta oscillations in Parkinson’s disease. Front Neurosci, 2020, 14: 166.

Journal of Biomedical Engineering

Current progress on characteristics of intracranial electrophysiology related to prolonged disorders of consciousness

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content