Toward Asleep DBS: Cortico-basal Ganglia Spectral and Coherence Activity During Interleaved Propofol/ketamine Sedation Mimics NREM/REM Sleep Activity

Overview

Journal NPJ Parkinsons Dis

Date 2021 Aug 3

PMID 34341348

Citations 4

Authors

Jing Guang

Halen Baker

Orilia Ben-Yishay Nizri

Shimon Firman

Uri Werner-Reiss

Vadim Kapuller

Zvi Israel

Hagai Bergman

Affiliations

Soon will be listed here.

Abstract

Deep brain stimulation (DBS) is currently a standard procedure for advanced Parkinson's disease. Many centers employ awake physiological navigation and stimulation assessment to optimize DBS localization and outcome. To enable DBS under sedation, asleep DBS, we characterized the cortico-basal ganglia neuronal network of two nonhuman primates under propofol, ketamine, and interleaved propofol-ketamine (IPK) sedation. Further, we compared these sedation states in the healthy and Parkinsonian condition to those of healthy sleep. Ketamine increases high-frequency power and synchronization while propofol increases low-frequency power and synchronization in polysomnography and neuronal activity recordings. Thus, ketamine does not mask the low-frequency oscillations used for physiological navigation toward the basal ganglia DBS targets. The brain spectral state under ketamine and propofol mimicked rapid eye movement (REM) and Non-REM (NREM) sleep activity, respectively, and the IPK protocol resembles the NREM-REM sleep cycle. These promising results are a meaningful step toward asleep DBS with nondistorted physiological navigation.

Citing Articles

Is the Subthalamic Nucleus Sleeping Under Nitrous Oxide-Ketamine General Anesthesia?.

Baker Erdman H, Bergman H, Haya K, Glowinsky S, Warhaftig L, Leon J Eur J Neurosci. 2025; 61(5):e70039.

PMID: 40045163 PMC: 11882488. DOI: 10.1111/ejn.70039.

Local orchestration of distributed functional patterns supporting loss and restoration of consciousness in the primate brain.

Luppi A, Uhrig L, Tasserie J, Signorelli C, Stamatakis E, Destexhe A Nat Commun. 2024; 15(1):2171.

PMID: 38462641 PMC: 10925605. DOI: 10.1038/s41467-024-46382-w.

Dexmedetomidine depresses neuronal activity in the subthalamic nucleus during deep brain stimulation electrode implantation surgery.

Amlong C, Rusy D, Sanders R, Lake W, Raz A BJA Open. 2023; 3:100088.

PMID: 37588575 PMC: 10430856. DOI: 10.1016/j.bjao.2022.100088.

Spontaneous pauses in firing of external pallidum neurons are associated with exploratory behavior.

Kaplan A, Mizrahi-Kliger A, Rappel P, Iskhakova L, Fonar G, Israel Z Commun Biol. 2022; 5(1):612.

PMID: 35729350 PMC: 9213498. DOI: 10.1038/s42003-022-03553-z.

Proceedings of the Ninth Annual Deep Brain Stimulation Think Tank: Advances in Cutting Edge Technologies, Artificial Intelligence, Neuromodulation, Neuroethics, Pain, Interventional Psychiatry, Epilepsy, and Traumatic Brain Injury.

Wong J, Deuschl G, Wolke R, Bergman H, Muthuraman M, Groppa S Front Hum Neurosci. 2022; 16:813387.

PMID: 35308605 PMC: 8931265. DOI: 10.3389/fnhum.2022.813387.

References

Kurdi M, Theerth K, Deva R . Ketamine: Current applications in anesthesia, pain, and critical care. Anesth Essays Res. 2015; 8(3):283-90. PMC: 4258981. DOI: 10.4103/0259-1162.143110. View

Khan M, Mewes K, Gross R, Skrinjar O . Assessment of brain shift related to deep brain stimulation surgery. Stereotact Funct Neurosurg. 2007; 86(1):44-53. DOI: 10.1159/000108588. View

Sklar G, Zukin S, Reilly T . Adverse reactions to ketamine anaesthesia. Abolition by a psychological technique. Anaesthesia. 1981; 36(2):183-7. DOI: 10.1111/j.1365-2044.1981.tb08721.x. View

Kocsis B . Differential role of NR2A and NR2B subunits in N-methyl-D-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol Psychiatry. 2011; 71(11):987-95. PMC: 3276718. DOI: 10.1016/j.biopsych.2011.10.002. View

Rincon-Cortes M, Grace A . Antidepressant effects of ketamine on depression-related phenotypes and dopamine dysfunction in rodent models of stress. Behav Brain Res. 2019; 379:112367. PMC: 6948930. DOI: 10.1016/j.bbr.2019.112367. View

Gilron R, Little S, Perrone R, Wilt R, de Hemptinne C, Yaroshinsky M . Long-term wireless streaming of neural recordings for circuit discovery and adaptive stimulation in individuals with Parkinson's disease. Nat Biotechnol. 2021; 39(9):1078-1085. PMC: 8434942. DOI: 10.1038/s41587-021-00897-5. View

Okun M, Fernandez H, Wu S, Kirsch-Darrow L, Bowers D, Bova F . Cognition and mood in Parkinson's disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: the COMPARE trial. Ann Neurol. 2009; 65(5):586-95. PMC: 2692580. DOI: 10.1002/ana.21596. View

Raz A, Eimerl D, Zaidel A, Bergman H, Israel Z . Propofol decreases neuronal population spiking activity in the subthalamic nucleus of Parkinsonian patients. Anesth Analg. 2010; 111(5):1285-9. DOI: 10.1213/ANE.0b013e3181f565f2. View

Zarate Jr C, Niciu M . Ketamine for depression: evidence, challenges and promise. World Psychiatry. 2015; 14(3):348-50. PMC: 4592658. DOI: 10.1002/wps.20269. View

10.

Goldberg J, Rokni U, Boraud T, Vaadia E, Bergman H . Spike synchronization in the cortex/basal-ganglia networks of Parkinsonian primates reflects global dynamics of the local field potentials. J Neurosci. 2004; 24(26):6003-10. PMC: 6729228. DOI: 10.1523/JNEUROSCI.4848-03.2004. View

11.

Benazzouz A, Boraud T, Dubedat P, Boireau A, Stutzmann J, Gross C . Riluzole prevents MPTP-induced parkinsonism in the rhesus monkey: a pilot study. Eur J Pharmacol. 1995; 284(3):299-307. DOI: 10.1016/0014-2999(95)00362-o. View

12.

Carlson A, Abbas M, Alunday R, Qeadan F, Shuttleworth C . Spreading depolarization in acute brain injury inhibited by ketamine: a prospective, randomized, multiple crossover trial. J Neurosurg. 2018; 130(5):1513-1519. PMC: 6279620. DOI: 10.3171/2017.12.JNS171665. View

13.

Hutchison W, Lang A, Dostrovsky J, Lozano A . Pallidal neuronal activity: implications for models of dystonia. Ann Neurol. 2003; 53(4):480-8. DOI: 10.1002/ana.10474. View

14.

van den Munckhof P, Contarino M, Bour L, Speelman J, de Bie R, Schuurman P . Postoperative curving and upward displacement of deep brain stimulation electrodes caused by brain shift. Neurosurgery. 2010; 67(1):49-53. DOI: 10.1227/01.NEU.0000370597.44524.6D. View

15.

Lozano C, Ranjan M, Boutet A, Xu D, Kucharczyk W, Fasano A . Imaging alone versus microelectrode recording-guided targeting of the STN in patients with Parkinson's disease. J Neurosurg. 2018; 130(6):1847-1852. DOI: 10.3171/2018.2.JNS172186. View

16.

Vesuna S, Kauvar I, Richman E, Gore F, Oskotsky T, Sava-Segal C . Deep posteromedial cortical rhythm in dissociation. Nature. 2020; 586(7827):87-94. PMC: 7553818. DOI: 10.1038/s41586-020-2731-9. View

17.

Wang S, Li Y, Qiu S, Zhang C, Wang G, Xian J . Reorganization of rich-clubs in functional brain networks during propofol-induced unconsciousness and natural sleep. Neuroimage Clin. 2020; 25:102188. PMC: 6997627. DOI: 10.1016/j.nicl.2020.102188. View

18.

Kita H . Globus pallidus external segment. Prog Brain Res. 2007; 160:111-33. DOI: 10.1016/S0079-6123(06)60007-1. View

19.

Okun M, Tagliati M, Pourfar M, Fernandez H, Rodriguez R, Alterman R . Management of referred deep brain stimulation failures: a retrospective analysis from 2 movement disorders centers. Arch Neurol. 2005; 62(8):1250-5. DOI: 10.1001/archneur.62.8.noc40425. View

20.

Hippard H, Watcha M, Stocco A, Curry D . Preservation of microelectrode recordings with non-GABAergic drugs during deep brain stimulator placement in children. J Neurosurg Pediatr. 2014; 14(3):279-86. DOI: 10.3171/2014.5.PEDS13103. View