Thalamic deep brain stimulation modulates cycles of seizure risk in epilepsy
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
UH2 NS095495
NINDS NIH HHS - United States
U24 NS113637
NINDS NIH HHS - United States
R01 NS092882
NINDS NIH HHS - United States
UH3 NS095495
NINDS NIH HHS - United States
U01 NS073557
NINDS NIH HHS - United States
PubMed
34930926
PubMed Central
PMC8688461
DOI
10.1038/s41598-021-03555-7
PII: 10.1038/s41598-021-03555-7
Knihovny.cz E-zdroje
- MeSH
- cirkadiánní rytmus MeSH
- elektroencefalografie MeSH
- epilepsie prevence a kontrola MeSH
- hluboká mozková stimulace metody MeSH
- lidé MeSH
- psi MeSH
- riziko MeSH
- thalamus fyziologie MeSH
- záchvaty prevence a kontrola MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- psi MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
Chronic brain recordings suggest that seizure risk is not uniform, but rather varies systematically relative to daily (circadian) and multiday (multidien) cycles. Here, one human and seven dogs with naturally occurring epilepsy had continuous intracranial EEG (median 298 days) using novel implantable sensing and stimulation devices. Two pet dogs and the human subject received concurrent thalamic deep brain stimulation (DBS) over multiple months. All subjects had circadian and multiday cycles in the rate of interictal epileptiform spikes (IES). There was seizure phase locking to circadian and multiday IES cycles in five and seven out of eight subjects, respectively. Thalamic DBS modified circadian (all 3 subjects) and multiday (analysis limited to the human participant) IES cycles. DBS modified seizure clustering and circadian phase locking in the human subject. Multiscale cycles in brain excitability and seizure risk are features of human and canine epilepsy and are modifiable by thalamic DBS.
Cadence Neuroscience Seattle WA 98052 USA
Department of Neurosurgery Mayo Clinic Rochester MN 55905 USA
Department of Veterinary Clinical Sciences University of California Davis CA 95616 USA
Faculty of Biomedical Engineering Czech Technical University Prague 272 01 Kladno Czech Republic
Institute for Biomedical Engineering Oxford University Oxford OX3 7DQ UK
International Clinical Research Center St Anne's University Hospital 656 91 Brno Czech Republic
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Gowers WR. Epilepsy and Other Chronic Convulsive Diseases: Their Causes, Symptoms, and Treatment. Churchill; 1901.
Griffiths G, Fox JT. Rhythm in epilepsy. Lancet. 1938;232(5999):409–416.
Langdon-Down M, Russell W. Brain, time of day in relation to convulsions in epilepsy. Lancet. 1929;213(5516):1029–1032.
Baud MO, et al. Multi-day rhythms modulate seizure risk in epilepsy. Nat. Commun. 2018;9(1):88. PubMed PMC
Karoly PJ, et al. Interictal spikes and epileptic seizures: Their relationship and underlying rhythmicity. Brain. 2016;139(Pt 4):1066–1078. PubMed
Karoly PJ, et al. Circadian and circaseptan rhythms in human epilepsy: A retrospective cohort study. Lancet Neurol. 2018;17(11):977–985. PubMed
Gregg NM, et al. Circadian and multiday seizure periodicities, and seizure clusters in canine epilepsy. Brain Commun. 2020;2(1):fcaa008. PubMed PMC
Baud MO, et al. Endogenous multidien rhythm of epilepsy in rats. Exp. Neurol. 2019;315:82–87. PubMed
Debski KJ, et al. The circadian dynamics of the hippocampal transcriptome and proteome is altered in experimental temporal lobe epilepsy. Sci. Adv. 2020;6:41. PubMed PMC
Leguia MG, et al. Seizure cycles in focal epilepsy. JAMA Neurol. 2021;78(4):454–463. PubMed PMC
Karoly PJ, et al. Cycles in epilepsy. Nature reviews. Neurology. 2021;20:21. PubMed
Khan S, et al. Circadian rhythm and epilepsy. Lancet Neurol. 2018;17(12):1098–1108. PubMed
Chang WC, et al. Loss of neuronal network resilience precedes seizures and determines the ictogenic nature of interictal synaptic perturbations. Nat. Neurosci. 2018;21(12):1742–1752. PubMed
Jensen MS, Yaari Y. The relationship between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Ann. Neurol. 1988;24(5):591–598. PubMed
Ly JQM, et al. Circadian regulation of human cortical excitability. Nat. Commun. 2016;7:11828. PubMed PMC
Maturana MI, et al. Critical slowing down as a biomarker for seizure susceptibility. Nat. Commun. 2020;11(1):2172. PubMed PMC
Meisel C, et al. Intrinsic excitability measures track antiepileptic drug action and uncover increasing/decreasing excitability over the wake/sleep cycle. Proc. Natl. Acad. Sci. USA. 2015;112(47):14694–14699. PubMed PMC
Pigorini A, et al. Bistability breaks-off deterministic responses to intracortical stimulation during non-REM sleep. Neuroimage. 2015;112:105–113. PubMed
Smith MJ, et al. Menstrual cycle effects on cortical excitability. Neurology. 1999;53(9):2069–2072. PubMed
Usami K, et al. The neural tides of sleep and consciousness revealed by single-pulse electrical brain stimulation. Sleep. 2019;42:6. PubMed PMC
Wright MA, et al. Cortical excitability predicts seizures in acutely drug-reduced temporal lobe epilepsy patients. Neurology. 2006;67(9):1646–1651. PubMed
Bunford N, et al. Canis familiaris as a model for non-invasive comparative neuroscience. Trends Neurosci. 2017;40(7):438–452. PubMed
Hare B, et al. The domestication of social cognition in dogs. Science. 2002;298(5598):1634–1636. PubMed
Tang R, et al. Candidate genes and functional noncoding variants identified in a canine model of obsessive-compulsive disorder. Genome Biol. 2014;15(3):R25. PubMed PMC
Heske L, et al. A cohort study of epilepsy among 665,000 insured dogs: Incidence, mortality and survival after diagnosis. Vet. J. 2014;202(3):471–476. PubMed
Berendt M, et al. Electroencephalography in dogs with epilepsy: Similarities between human and canine findings. Acta Neurol. Scand. 1999;99(5):276–283. PubMed
Fisher R, et al. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010;51(5):899–908. PubMed
Paz JT, et al. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 2013;16(1):64–70. PubMed PMC
Guye M, et al. The role of corticothalamic coupling in human temporal lobe epilepsy. Brain. 2006;129(Pt 7):1917–1928. PubMed
Gregg NM, et al. Anterior nucleus of the thalamus seizure detection in ambulatory humans. Epilepsia. 2021;62(10):e158–e164. PubMed PMC
Yu T, et al. High-frequency stimulation of anterior nucleus of thalamus desynchronizes epileptic network in humans. Brain. 2018;141(9):2631–2643. PubMed
Chen R, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48(5):1398–1403. PubMed
Lundstrom BN, et al. Chronic subthreshold cortical stimulation and stimulation-related EEG biomarkers for focal epilepsy. Brain Commun. 2019;1(1):10. PubMed PMC
Kile KB, Tian N, Durand DM. Low frequency stimulation decreases seizure activity in a mutation model of epilepsy. Epilepsia. 2010;51(9):1745–1753. PubMed PMC
Koubeissi MZ, et al. Low-frequency electrical stimulation of a fiber tract in temporal lobe epilepsy. Ann. Neurol. 2013;74(2):223–231. PubMed
Cook MJ, et al. Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: A first-in-man study. Lancet Neurol. 2013;12(6):563–571. PubMed
Kremen V, et al. Integrating brain implants with local and distributed computing devices: A next generation epilepsy management system. IEEE J. Transl. Eng. Health Med. 2018;6:2500112. PubMed PMC
Pavlova MK, et al. Is there a circadian variation of epileptiform abnormalities in idiopathic generalized epilepsy? Epilepsy Behav. 2009;16(3):461–467. PubMed PMC
Quigg M, et al. Effects of circadian regulation and rest-activity state on spontaneous seizures in a rat model of limbic epilepsy. Epilepsia. 2000;41(5):502–509. PubMed
Dell KL, et al. Seizure likelihood varies with day-to-day variations in sleep duration in patients with refractory focal epilepsy: A longitudinal electroencephalography investigation. EClinicalMedicine. 2021;20:100934. PubMed PMC
Bódizs R, et al. Sleep in the dog: Comparative, behavioral and translational relevance. Curr. Opin. Behav. Sci. 2020;33:25–33.
Aschoff J. Circadian rhythms in man. Science. 1965;148(3676):1427–1432. PubMed
Leguia MG, et al. Measuring synchrony in bio-medical timeseries. Chaos. 2021;31(1):013138. PubMed
Proix T, et al. Forecasting seizure risk in adults with focal epilepsy: A development and validation study. Lancet Neurol. 2021;20(2):127–135. PubMed PMC
Rao VR, et al. Cues for seizure timing. Epilepsia. 2021;62(Suppl 1):S15–S31. PubMed
Voges BR, et al. Deep brain stimulation of anterior nucleus thalami disrupts sleep in epilepsy patients. Epilepsia. 2015;56(8):e99–e103. PubMed
Baud MO, Rao VR. Gauging seizure risk. Neurology. 2018;91(21):967–973. PubMed
Caciagli L, et al. Thalamus and focal to bilateral seizures: A multiscale cognitive imaging study. Neurology. 2020;95(17):e2427–e2441. PubMed PMC
Dinkelacker V, et al. Hippocampal-thalamic wiring in medial temporal lobe epilepsy: Enhanced connectivity per hippocampal voxel. Epilepsia. 2015;56(8):1217–1226. PubMed
He X, et al. Presurgical thalamic "hubness" predicts surgical outcome in temporal lobe epilepsy. Neurology. 2017;88(24):2285–2293. PubMed
Mueller SG, et al. Involvement of the thalamocortical network in TLE with and without mesiotemporal sclerosis. Epilepsia. 2010;51(8):1436–1445. PubMed PMC
O'Muircheartaigh J, et al. Abnormal thalamocortical structural and functional connectivity in juvenile myoclonic epilepsy. Brain. 2012;135(Pt 12):3635–3644. PubMed PMC
Lozano AM, et al. Deep brain stimulation: Current challenges and future directions. Nat. Rev. Neurol. 2019;15(3):148–160. PubMed PMC
Ashkan K, et al. Insights into the mechanisms of deep brain stimulation. Nat. Rev. Neurol. 2017;13(9):548–554. PubMed
Dostrovsky JO, Lozano AM. Mechanisms of deep brain stimulation. Mov. Disord. 2002;17(Suppl 3):S63–S68. PubMed
Mirski MA, Fisher RS. Electrical stimulation of the mammillary nuclei increases seizure threshold to pentylenetetrazol in rats. Epilepsia. 1994;35(6):1309–1316. PubMed
Stypulkowski PH, Stanslaski SR, Giftakis JE. Modulation of hippocampal activity with fornix deep brain stimulation. Brain Stimul. 2017;10(6):1125–1132. PubMed
Mihaly I, et al. Amygdala low-frequency stimulation reduces pathological phase–amplitude coupling in the pilocarpine model of epilepsy. Brain Sci. 2020;10:11. PubMed PMC
Miller JW, Turner GM, Gray BC. Anticonvulsant effects of the experimental induction of hippocampal theta activity. Epilepsy Res. 1994;18(3):195–204. PubMed
Silva AB, et al. Effects of anterior thalamic nuclei stimulation on hippocampal activity: Chronic recording in a patient with drug-resistant focal epilepsy. Epilepsy Behav. Rep. 2021;16:100467. PubMed PMC
Frye RE, et al. Transcranial magnetic stimulation in child neurology: Current and future directions. J. Child Neurol. 2008;23(1):79–96. PubMed PMC
Janca R, et al. Detection of interictal epileptiform discharges using signal envelope distribution modelling: Application to epileptic and non-epileptic intracranial recordings. Brain Topogr. 2015;28(1):172–183. PubMed
Baldassano SN, et al. Crowdsourcing seizure detection: Algorithm development and validation on human implanted device recordings. Brain. 2017;140(6):1680–1691. PubMed PMC
MathWorks(R). cwt Continuous 1-D wavelet transform. 2021. https://www.mathworks.com/help/wavelet/ref/cwt.html?searchHighlight=cwt&s_tid=srchtitle_cwt_1.
Berens, P., CircStat: A MATLAB Toolbox for Circular Statistics. 2009. 31(10): 21.
Cremers J, Klugkist I. One direction? A tutorial for circular data analysis using R with examples in cognitive psychology. Front. Psychol. 2018;9:2040. PubMed PMC
Acute to long-term characteristics of impedance recordings during neurostimulation in humans
Acute to long-term characteristics of impedance recordings during neurostimulation in humans
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Embedding digital chronotherapy into bioelectronic medicines