Sensing with deep brain stimulation device in epilepsy: Aperiodic changes in thalamic local field potential during seizures.
anterior nucleus of the thalamus
centromedian nucleus
deep brain stimulation
epilepsy
local field potential
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
20
08
2023
received:
19
04
2023
accepted:
21
08
2023
medline:
7
11
2023
pubmed:
22
8
2023
entrez:
22
8
2023
Statut:
ppublish
Résumé
Thalamic deep brain stimulation (DBS) is an effective therapeutic option in patients with drug-resistant epilepsy. Recent DBS devices with sensing capabilities enable chronic, outpatient local field potential (LFP) recordings. Whereas beta oscillations have been demonstrated to be a useful biomarker in movement disorders, the clinical utility of DBS sensing in epilepsy remains unclear. Our aim was to determine LFP features that distinguish ictal from inter-ictal states, which may aid in tracking seizure outcomes with DBS. Electrophysiology data were obtained from DBS devices implanted in the anterior nucleus (N = 12) or centromedian nucleus (N = 2) of the thalamus. Power spectra recorded during patient/caregiver-marked seizure events were analyzed with a method that quantitatively separates the oscillatory and non-oscillatory/aperiodic components of the LFP using non-parametric statistics, without the need for pre-specification of the frequency bands of interest. Features of the LFP parameterized using this algorithm were compared with those from inter-ictal power spectra recorded in clinic. Oscillatory activity in multiple canonical frequency bands was identified from the power spectra in 86.48% of patient-marked seizure events. Delta oscillations were present in all patients, followed by theta (N = 10) and beta (N = 9). Although there were no differences in oscillatory LFP features between the ictal and inter-ictal states, there was a steeper decline in the 1/f slope of the aperiodic component of the LFP during seizures. Our work highlights the potential and shortcomings of chronic LFP recordings in thalamic DBS for epilepsy. Findings suggest that no single frequency band in isolation clearly differentiates seizures, and that features of aperiodic LFP activity may be clinically-relevant biomarkers of seizures.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3025-3035Informations de copyright
© 2023 International League Against Epilepsy.
Références
Wong JK, Deuschl G, Wolke R, Bergman H, Muthuraman M, Groppa S, et al. 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. Front Hum Neurosci [Internet]. 2022;16:813387. https://doi.org/10.3389/fnhum.2022.813387
Thenaisie Y, Palmisano C, Canessa A, Keulen BJ, Capetian P, Jiménez MC, et al. Towards adaptive deep brain stimulation: clinical and technical notes on a novel commercial device for chronic brain sensing. J Neural Eng. 2021;18(4):42002.
Kühn AA, Kupsch A, Schneider G-H, Brown P. Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur J Neurosci. 2006;23(7):1956-1960.
Eusebio A, Thevathasan W, Doyle Gaynor L, Pogosyan A, Bye E, Foltynie T, et al. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J Neurol Neurosurg Psychiatry. 2011;82(5):569-573.
Little S, Pogosyan A, Neal S, Zavala B, Zrinzo L, Hariz M, et al. Adaptive deep brain stimulation in advanced Parkinson disease. Ann Neurol. 2013;74(3):449-457.
Kühn AA, Trottenberg T, Kivi A, Kupsch A, Schneider G-H, Brown P. The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson's disease. Exp Neurol. 2005;194(1):212-220.
Zaidel A, Spivak A, Grieb B, Bergman H, Israel Z. Subthalamic span of β oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease. Brain. 2010;133(7):2007-2021.
Strelow JN, Dembek TA, Baldermann JC, Andrade P, Jergas H, Visser-Vandewalle V, et al. Local field potential-guided contact selection using chronically implanted sensing devices for deep brain stimulation in Parkinson's disease. Brain Sci. 2022;12(12):1726.
Dalic LJ, Warren AEL, Bulluss KJ, Thevathasan W, Roten A, Churilov L, et al. DBS of thalamic centromedian nucleus for Lennox-Gastaut syndrome (ESTEL trial). Ann Neurol. 2022;91(2):253-267.
Fisher R, Salanova V, Witt T, Worth R, Henry T, Gross R, et al. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010;51(5):899-908.
Salanova V, Sperling MR, Gross RE, Irwin CP, Vollhaber JA, Giftakis JE, et al. The SANTÉ study at 10 years of follow-up: effectiveness, safety, and sudden unexpected death in epilepsy. Epilepsia. 2021;62(6):1306-1317.
Valentín A, García Navarrete E, Chelvarajah R, Torres C, Navas M, Vico L, et al. Deep brain stimulation of the centromedian thalamic nucleus for the treatment of generalized and frontal epilepsies. Epilepsia. 2013;54(10):1823-1833.
Fisher RS, Uematsu S, Krauss GL, Cysyk BJ, McPherson R, Lesser RP, et al. Placebo-controlled pilot study of centromedian thalamic stimulation in treatment of intractable seizures. Epilepsia. 1992;33(5):841-851.
Velasco F, Velasco M, Jiménez F, Velasco AL, Brito F, Rise M, et al. Predictors in the treatment of difficult-to-control seizures by electrical stimulation of the centromedian thalamic nucleus. Neurosurgery. 2000;47(2):295-304; discussion 304-305.
Cukiert A, Cukiert CM, Burattini JA, Mariani PP. Seizure outcome during bilateral, continuous, thalamic centromedian nuclei deep brain stimulation in patients with generalized epilepsy: a prospective, open-label study. Seizure. 2020;81:304-309.
Lopes EM, Rego R, Rito M, Chamadoira C, Dias D, Cunha JPS. Estimation of ANT-DBS electrodes on target positioning based on a new PerceptTM PC LFP signal analysis. Sensors. 2022;22(17):6601.
Grinenko O, Li J, Mosher JC, Wang IZ, Bulacio JC, Gonzalez-Martinez J, et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain. 2018;141(1):117-131.
Donoghue T, Haller M, Peterson EJ, Varma P, Sebastian P, Gao R, et al. Parameterizing neural power spectra into periodic and aperiodic components. Nat Neurosci. 2020;23(12):1655-1665.
Yang JC, Bullinger KL, Isbaine F, Alwaki A, Opri E, Willie JT, et al. Centromedian thalamic deep brain stimulation for drug-resistant epilepsy: single-center experience. J Neurosurg. 2022;1:1-10.
Su JH, Thomas FT, Kasoff WS, Tourdias T, Choi EY, Rutt BK, et al. Thalamus optimized multi atlas segmentation (THOMAS): fast, fully automated segmentation of thalamic nuclei from structural MRI. Neuroimage. 2019;194:272-282.
Miller KJ, Sorensen LB, Ojemann JG, den Nijs M. Power-law scaling in the brain surface electric potential. PLoS Comput Biol. 2009;5(12):e1000609.
Raghu ALB, Eraifej J, Sarangmat N, Stein J, FitzGerald JJ, Payne S, et al. Pallido-putaminal connectivity predicts outcomes of deep brain stimulation for cervical dystonia. Brain. 2021;144(12):3589-3596.
Basile GA, Bertino S, Bramanti A, Ciurleo R, Anastasi GP, Milardi D, et al. In vivo super-resolution track-density imaging for thalamic nuclei identification. Cereb Cortex. 2021;31(12):5613-5636.
Basile GA, Quartu M, Bertino S, Serra MP, Trucas M, Boi M, et al. In vivo probabilistic atlas of white matter tracts of the human subthalamic area combining track density imaging and optimized diffusion tractography. Brain Struct Funct. 2022;227(8):2647-2665.
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62(2):782-790.
Morrell MJ, RNS System in Epilepsy Study Group. Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology. 2011;77(13):1295-1304.
Fisher RS, Blum DE, DiVentura B, Vannest J, Hixson JD, Moss R, et al. Seizure diaries for clinical research and practice: limitations and future prospects. Epilepsy Behav. 2012;24(3):304-310.
Fasano A, Gorodetsky C, Paul D, Germann J, Loh A, Yan H, et al. Local field potential-based programming: a proof-of-concept pilot study. Neuromodulation. 2022;25(2):271-275.
Toth E, Kumar SS, Chaitanya G, Riley K, Balasubramanian K, Pati S. Machine learning approach to detect focal-onset seizures in the human anterior nucleus of the thalamus. J Neural Eng. 2020;17(6):66004.
Gregg NM, Marks VS, Sladky V, Lundstrom BN, Klassen B, Messina SA, et al. Anterior nucleus of the thalamus seizure detection in ambulatory humans. Epilepsia. 2021;62(10):e158-e164.
Gao R, Peterson EJ, Voytek B. Inferring synaptic excitation/inhibition balance from field potentials. Neuroimage. 2017;158:70-78.
Jiang H, Kokkinos V, Ye S, Urban A, Bagić A, Richardson M, et al. Interictal SEEG resting-state connectivity localizes the seizure onset zone and predicts seizure outcome. Adv Sci (Weinh). 2022;9(18):e2200887.
Jabran Y, Mahmoudzadeh M, Martinez N, Heberlé C, Wallois F, Bourel-Ponchel E. Temporal and spatial dynamics of different interictal epileptic discharges: a time-frequency EEG approach in pediatric focal refractory epilepsy. Front Neurol [Internet]. 2020;11:941. https://doi.org/10.3389/fneur.2020.00941
Meisenhelter S, Quon RJ, Steimel SA, Testorf ME, Camp EJ, Moein P, et al. Interictal epileptiform discharges are task dependent and are associated with lasting electrocorticographic changes. Cereb Cortex Commun. 2021;2(2):tgab019.