Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2020 | 80 | 3 |
Tytuł artykułu

Diazepam and electrical stimulation of paleocerebellar cortex inhibits seizures in pentylenetetrazol‑kindled rats

Warianty tytułu
Języki publikacji
The cerebellum is a potent anti‑epileptic target for deep brain stimulation in patients with drug‑resistant epilepsy. The effects of such stimulation, however, may also favor seizure activity. Our goal was to investigate the effect of cerebellar electrical stimulation (ES) alone and in combination with the anti‑epileptic drug diazepam (DIA) on seizure outcome. We used a rat model of pentylenetetrazol kindling, which is characterized by seizures followed by deteriorations in central benzodiazepine‑GABAA (BDZ‑GABAA) receptors. We tested the effects of ES alone and in combination with DIA (0.1 and 1.0 mg/kg) on seizures. Our data demonstrated: 20 ES trials can prevent the recurrence of clonic‑tonic kindled seizures, administration of either DIA‑0.1 or ES (5 trials) alone is ineffective on seizures, and combining DIA‑0.1 and 5 ES or DIA‑1.0 and 5 ES caused an additive effect, prolonged the latency to seizure onset, and prevented recurrence of clonic‑tonic seizures. We also observed that ES alone produced either facilitation or inhibition of seizures on EEG. In contrast, the same ES inhibited EEG seizures when delivered after a combination of DIA‑1.0 and 5 ES and ultimately prevented the facilitation of the discharges. Lastly, we demonstrated that seizure suppression is intensified when cortical ES is performed after DIA administration. Our data supported the hypothesis that both BDZ‑GABAA receptor activity along with cerebellar output comprise the potential mechanisms underlying the peculiar effects of deep brain stimulation in the cerebellum on seizures.
Słowa kluczowe
Opis fizyczny
  • Department of Biophysics, Informatics and Medical Devices, Odessa National Medical University, Odessa, Ukraine
  • Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia, USA
  • Department of Simulative Medicine, Odessa National Medical University, Odessa, Ukraine
  • Department of Physiology, Odessa National Medical University, Odessa, Ukraine
  • Asgari A, Semnanian S, Atapour N, Shojaei A, Moradi H, Mirnajafi‑Zadeh J (2014) Combined sub‑threshold dosages of phenobarbital and low‑frequency stimulation effectively reduce seizures in amygdala‑kindled rats. Neurol Sci 35: 1255–1260.
  • Asgari A, Semnanian S, Atapour N, Shojaei A, Moradi‑Chameh H, Ghafouri S, Sheibani V, Mirnajafi‑Zadeh J (2016) Low‑frequency electrical stimulation enhances the effectiveness of phenobarbital on GABAergic currents in hippocampal slices of kindled rats. Neuroscience 330: 26–38.
  • Bantli H, Bloedel JR, Tolbert D (1976) Activation of neurons in the cerebellar nuclei and ascending reticular formation by stimulation of the cerebellar surface. J Neurosurg 45: 539–554.
  • Bazyan AS, Zhulin VV, Karpova MN, Klishina NY, Glebov RN (2001) Long‑term reduction of benzodiazepine receptor density in the rat cere‑ bellum by acute seizures and kindling and its recovery 6 months later by a pentylenetetrazole challenge. Brain Res 888: 212–220.
  • Besio  W, Cuellar‑Herrera  M, Luna‑Munguia H, Orozco‑Suarez S, Rocha  L (2013) Effects of transcranial focal electrical stimulation alone and associated with a sub‑effective dose of diazepam on pilocarpine‑induced status epilepticus and subsequent neuronal damage in rats. Epilepsy Behav 28: 432–436.
  • Christian CA, Herbert AG, Holt RL, Peng K, Sherwood KD, Pangratz‑Fuehrer  S, Rudolph U, Huguenard JR (2013) Endogenous positive al‑ losteric modulation of GABA(A) receptors by diazepam binding inhibi‑ tor. Neuron 78: 1063–1074.
  • Clark  M, Massenburg GS, Weiss SR, Post RM (1994) Analysis of the hippocampal GABAA receptor system in kindled rats by autoradiographic and in situ hybridization techniques: contingent tolerance to carbamazepine. Brain Res Mol Brain Res 26: 309–319.
  • Cuellar‑Herrera M, Velasco M, Velasco F, Velasco AL, Jimenez F, Orozco S, Briones M, Rocha L (2004) Evaluation of GABA system and cell damage in parahippocampus of patients with temporal lobe epilepsy showing antiepileptic effects after subacute electrical stimulation. Epilepsia 45: 459–466.
  • Cuellar‑Herrera  M, Pena F, Alcantara‑Gonzalez D, Neri‑Bazan  L, Rocha  L (2010) Antiepileptic drugs combined with high‑frequency electrical stimulation in the ventral hippocampus modify pilocarpine‑induced status epilepticus in rats. Epilepsia 51: 432–437.
  • Daskalakis ZJ, Paradiso GO, Christensen BK, Fitzgerald PB, Gunraj C, Chen R (2004) Exploring the connectivity between the cerebellum and motor cortex in humans. J Physiol 557: 689–700.
  • Dauth GW, Dell S, Gilman S (1978) Alteration of Purkinje cell activity from transfolial stimulation of the cerebellum in the cat. Neurology 28: 654–660.
  • Davis R (2009) Cerebellar stimulation for seizure control. In: Textbook of Stereotactic and Functional Neurosurgery (Lozano AM, Gildenberg PL, Tasker RR, Ed.) Springer Berlin Heidelberg, Berlin, Heidelberg, p. 2823–2837.
  • Erkeç ÖE, Arihan O (2015) Pentylenetetrazole kindling epilepsy model. Ep‑ ilepsi Modeli 21: 6–12.
  • Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, Engel  JJr, Forsgren  L, French JA, Glynn  M, Hesdorffer DC, Lee BI, Mathern GW, Moshe SL, Perucca E, Scheffer IE, Tomson T, Watanabe M, Wiebe S (2014) ILAE official report: a practical clinical definition of epi‑ lepsy. Epilepsia 55: 475–482.
  • Fisher RS, Velasco AL (2014) Electrical brain stimulation for epilepsy. Nat Rev Neurol 10: 261–270.
  • Fleischmann A, Makman MH, Etgen AM (1995) GABAA receptor activation induces GABA and glutamate release from preoptic area. Life Sci 56: 1665–1678.
  • Fountas KN, Kapsalaki E, Hadjigeorgiou G (2010) Cerebellar stimulation in the management of medically intractable epilepsy: a systematic and critical review. 29: E8.
  • Gersner R, Dhamne SC, Zangen A, Pascual‑Leone A, Rotenberg A (2016) Bursts of high‑frequency repetitive transcranial magnetic stimulation (rTMS), together with lorazepam, suppress seizures in a rat kainate status epilepticus model. Epilepsy Behav 62: 136–139.
  • Godlevsky LS, Muratova TN, Kresyun NV, van Luijtelaar G, Coenen AM (2014) Anxiolytic and antidepressive effects of electric stimulation of the paleocerebellar cortex in pentylenetetrazol kindled rats. Acta Neurobiol Exp 74: 456–464.
  • Groenewegen HJ, Witter MP (2004) Thalamus. In: The rat nervous system. Third ed. (Paxinos G, Ed.). Academic Press, Burlington, USA, p. 407–453.
  • Hablitz JJ, McSherry JW, Kellaway P (1975) Cortical seizures following cerebellar stimulation in primates. Electroenceph Clin Neurophysiol 38: 423–426.
  • Hutton JT, Frost Jr JD, Foster J (1972) The influence of the cerebellum in cat penicillin epilepsy. Epilepsia 13: 401–408.
  • Ishizawa K, Chen Z, Okuma C, Sugimoto Y, Fujii Y, Kamei C (2000) Participation of GABAergic and histaminergic systems in inhibiting amygdaloid kindled seizures. Jpn J Pharmacol 82: 48–53.
  • Kamakura R, Kovalainen M, Leppaluoto J, Herzig KH, Makela KA (2016) The effects of group and single housing and automated animal monitoring on urinary corticosterone levels in male C57BL/6 mice. Physiol Rep 4. pii: e12703.
  • Kim SH, Lim SC, Kim J, Son BC, Lee KJ, Shon YM (2017) Long‑term follow‑up of anterior thalamic deep brain stimulation in epilepsy: a 11‑year, single center experience. Seizure 52: 154–161.
  • Klinger NV, Mittal S (2016) Clinical efficacy of deep brain stimulation for the treatment of medically refractory epilepsy. Clin Neurol Neurosurg 140: 11–25.
  • Komulainen H, Keranen A, Saano V (1995) Triethyllead decreases central benzodiazepine receptor binding in rat cerebellum ex vivo. Teur J Phar‑ macol 293: 167–171.
  • Krook‑Magnuson E, Szabo GG, Armstrong C, Oijala M, Soltesz I (2014) Cere‑ bellar directed optogenetic intervention inhibits spontaneous hippocam‑ pal seizures in a mouse model of temporal lobe epilepsy. 1. pii: e.2014.
  • Maiti A, Snider RS (1975) Cerebellar control of basal forebrain seizures: amygdala and hippocampus. Epilepsia 16: 521–533.
  • Ojemann, GA (1980) Basic mechanisms implicated in surgical treatments of epilepsy. In: Epilepsy: a Window to Brain Mechanisms (Ward Jr AA, Lockard JS, Ed.). Raven Press, New York, p. 261–277.
  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Sydney: Academic Press Inc. Reimer GR, Grimm RJ, Dow RS (1967) Effects of cerebellar stimulation on cobalt‑induced epilepsy in the cat. Electroenceph Clin Neurophysiol 23: 456–462.
  • Rijkers K, Moers‑Hornikx VM, Hemmes RJ, Aalbers MW, Temel Y, Vles JS, Hoogland G (2015) Sustained reduction of cerebellar activity in experimental epilepsy. Biomed Res Int 15: 718591.
  • Riss J, Cloyd J, Gates J, Collins S (2008) Benzodiazepines in epilepsy: pharmacology and pharmacokinetics. Acta Neurol Scand 118: 69–86.
  • Salt TE, Copeland CS (2017) Metabotropic glutamate receptor function in thalamocortical circuitry. In: mGLU Receptors (Ngomba RT, Di Giovanni G, Battaglia G, Nicoletti F, Ed.). Springer International Publishing, Cham., p. 149–159.
  • Shandra AA, Godlevsky LS (1990) Antiepileptic effects of cerebellar nucleus dentatus electrical stimulation under different conditions of brain epileptisation. Indian J Exp Biol 28: 158–161.
  • Sprengers M, Vonck K, Carrette E, Marson AG, Boon P (2017) Deep brain and cortical stimulation for epilepsy. Cochrane Database Syst Rev 7: CD008497.
  • van Luijtelaar G, Luttjohann A, Makarov VV, Maksimenko VA, Koronovskiim  AA, Hramov AE (2016) Methods of automated absence seizure detection, interference by stimulation, and possibilities for prediction in genetic absence models. J Neurosci Methods 260: 144–158.
  • Velasco F, Carrillo‑Ruiz JD, Brito F, Velasco  M, Velasco AL, Marquez I, Davis R (2005) Double‑blind, randomized controlled pilot study of bilateral cerebellar stimulation for treatment of intractable motor seizures. Epilepsia 46: 1071–1081.
  • Verotti A, Milioni M, Zaccara G (2015) Safety and efficacy of diazepam autoinjector for the management of epilepsy. Expert Rev Neurother 15: 127–133.
  • Wang S, Wu DC, Ding MP, Li Q, Zhuge ZB, Zhang SH, Chen Z (2008) Low‑frequency stimulation of cerebellar fastigial nucleus inhibits amygdaloid kindling acquisition in Sprague‑Dawley rats. Neurobiol Dis 29: 52–58.
  • Wisden W, Murray AJ, McClure C, Wulff P (2009) Studying cerebellar circuits by remote control of selected neuronal types with GABAA  receptors. Front Mol Neurosci 2: 29.
  • Wyckhuys T, Geerts PJ, Raedt R, Vonck K, Wadman W, Boon P (2009) Deep brain stimulation for epilepsy: knowledge gained from experimental animal models. Acta Neurol Belg 109: 63–80.
Typ dokumentu
Identyfikator YADDA
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.