ESTABLISHING DRUG EFFECTS ON ELECTROCORTICOGRAPHIC ACTIVITY IN A GENETIC ABSENCE EPILEPSY MODEL: ADVANCES AND PITFALLS MODERN PRINCIPLES AND TECHNICAL SUPPORT OF RESEARCH ON THE MODEL OF GENETIC FORM OF ABSENT EPILEPSY
DOI:
https://doi.org/10.11603/mie.1996-1960.2020.1.11129Keywords:
WAG/Rij's rats, antiepiletic drugs, electroencephalogram-behavioral relationship, genetic absence models, spike-wave dischargesAbstract
Background. The identification of a valid experimental model of absence epilepsy is important for the investigations of its mechanisms and for the evaluation and justification of new experimental treatment options. The genetic rat models such as rats of the WAG/Rij strain and GAERS were developed as models for generalized genetic epilepsy and, in particular, for childhood absence epilepsy, and are currently at the forefront of new theoretical insights regarding the site of origin of absence epilepsy.
Material and methods. In this review article, 40-years of experience in the field of experimental absence epilepsy is summarized in order to work out suitable and most optimal protocols for the proper evaluation of treatment, often drug effects on the electroencephalogram of genetic WAG/Rij rat.
Results. The genetic absence epilepsy animal models, first described in the eighties of the previous century, have, among others, face, construct, and predictive validity. Genetic models were and are currently used as models to predict the action of antiepileptic medication and other experimental treatments, to elucidate neurobiological mechanisms of the for absence epilepsy characteristic spike-wave discharges and to study epileptogenesis. The electroencephalogram or electrocorticogram is imperative for recognizing absence seizures and for quantifying the spike-wave discharges, monitoring the animal's behavior is equally necessary for proper interpretation of the electroencephalogram data. Here an overview is given regarding the design of drug evaluation studies, which animals to use, classical and new electroencephalogram variables, among other wavelet analyses and various types of network analyses, the necessity of monitoring and quantification of the rats' behavior during the electroencephalogram registration, some pitfalls regarding the interpretation of the data, and some recent developments in electroencephalogram technology.
Conclusions. The genetic models have replaced the pharmacological seizure models considering that it is possible to study mechanisms in a truly epileptic brain, although it is acknowledged that also the seizure models have a great merit. The predictive validity is better than in the previously used pharmacologically induced seizure models. Combined electroencephalogram-behavioural studies in adult symptomatic male and female WAG/Rij rats have a great potential to predict both anti-and proabsence actions of treatments and compounds.
References
Ahnaou A., Huysmans, H., Jacobs, T., Drinkenburg, W. H. (2014). Cortical EEG oscillations and network connectivity as efficacy indices for assessing drugs with cognition enhancing potential. Neuropharmacology 86, 362-377. doi: 10.1016/j.neuropharm.2014.08.015.
Ball, D., Kliese, R., Windels, F., Nolan, C., Stratton, P., Sah, P., et al. (2014). Rodent Scope: A user-configurable digital wireless telemetry system for freely behaving animals. PloS One 9 (2), e89949. doi: 10.1371/journal. pone.0089949.
Bastos, A. M., Schoffelen, J. M. (2016). A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front. Syst. Neurosci. 9, 175. doi: 10.1016/j.neubiorev.2010.07.002
Beery, A. K., Zucker, I. (2011). Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 35, 565-572. doi: 10.3389/fnsys.2015.00175.
Blumenfeld, H., Klein, J. P., Schridde, U., Vestal, M., Rice, T., Khera, D. S., et al. (2008). Early treatment suppresses the development of spike-wave epilepsy in a rat model. Epilepsia 49, 400- 409. doi: 10.1111/j.1528-1167.2007.01458.x.
Bosnyakova, D., Gabova, A., Zharikova, A., Gnezditski, V., Kuznetsova, G., van Luijtelaar, G. (2007). Some peculiarities of time-frequency dynamics of spike-wave discharges in humans and rats. Clin. Neurophysiol. 118, 1736-1743. doi: 10.1016/j.clinph.2007.04.013.
Bouwman, B. M., Suffczynski, P., Midzyanovskaya, I. S., Maris, E., van den Broek, P. L., van Rijn, C. M. (2007). The effects of vigabatrin on spike and wave discharges in WAGZRij rats. Epilepsy Res. 76, 34-40. doi: 10.1016/j.eplepsyres.2007.06.006.
Buzsaki, G., Bickford, R. G., Armstrong, D. M., Ponomareff, G., Chen, K. S., Ruiz, R., et al. (1988). Electric activity in the neocortex of freely moving young and aged rats. Neuroscience 26, 735-744. doi: 10.1016/0306-4522(88)90095-4.
Casillas-Espinosa, P. M., Sargsyan, A., Melkonian, D., O'Brien, T. J. (2019). A universal automated tool for reliable detection of seizures in rodent models of acquired and genetic epilepsy. Epilepsia 60, 783-791. doi: 10.1111/epi.14691.
Celli, R., Santolini, I., van Luijtelaar, G., Ngomba, R. T., Bruno, V., Nicoletti, F. (2019). Targeting metabotropic glutamate receptors in the treatment of epilepsy: rationale and current status. Expert Opin. Ther. Targets 23, 341-351. doi: 10.1080/14728222.2019.1586885.
Citraro, R., Russo, E., Ngomba, R. T., Nicoletti, F., Scicchitano, F., Whalley, B. J., et al. (2013). CB1 agonists, locally applied to the cortico-thalamic circuit of rats with genetic absence epilepsy, reduce epileptic manifestations. Epilepsy Res. 106, 74-82. doi: 10.1016/j. eplepsyres.2013.06.004.
Coenen, A. M., van Luijtelaar, G. (1987). The WAG! Rij rat model for absence epilepsy: Age and sex factors. Epilepsy Res. 1, 297-301. doi: 10.1016/0920-1211(87)90005-2.
Coenen, A. M., Drinkenburg, W. H., Peeters, B. W., Vossen, J. M., van Luijtelaar, E. (1991). Absence epilepsy and the level of vigilance in rats of the WAGZ Rij strain. Neurosci. Biobehav. Rev. 15, 259-263. doi: 10.1016/S0149-7634(05)80005-3.
Coenen, A. M., Stephens, D. N., Van Luijtelaar, E. L. (1992). Effects of the beta-carboline abecarnil on epileptic activity, EEG, sleep and behavior of rats. Pharmacol. Biochem. Behav. 42, 401-405. doi: 10.1016/0091-3057(92)90132-Y.
Coenen, A. M., Blezer, E. H., van Luijtelaar, E. L. (1995). Effects of the GABA-uptake inhibitor tiagabine on electroencephalogram, spike-wave discharges and behaviour of rats. Epilepsy Res. 21, 89-94. doi: 10.1016/0920-1211(95)00015-3.
Coenen, A., Smit, A., van Lier, H., van Oijen, G. (2004). "Recording the EEG in humans and animals," in Essentials and applications of EEG research in preclinical and clinical pharmacology. Eds. Drinkenburg, W. H. I. M., Ruigt, G. S. F, Jobert, M. (Berlin: IPEG 'International Pharmaco-EEG Group), 25-40.
Crunelli, V., Hughes, S. W. (2010). The slow (<1 Hz) rhythm of non REM sleep: a dialogue between three cardinal oscillators. Nat. Neurosci. 13, 9-17. doi: 10.1038/nn.2445.
D'Amore, V., Raaymakers, R. L., Santolini, I., van Rijn, C. M., Ngomba, R., Nicoletti, F., et al. (2016). The antiabsence effect of mGlu5 receptor amplification with
VU0360172 is maintained in WAGІRij rats chronically treated with ethosuximide. Pharmacol. Biochem. Behav. 146 (147), 50-59. doi: 10.1016/j.pbb.2016.05.004.
Depaulis, A., van Luijtelaar, G. (2006). "Genetic models of absence epilepsy in the rat," in Models of Seizures and Epilepsy. Eds. Pitkanen, A., Schwartkroin, P. A., Moshe, S. L. (Amsterdam: Elsevier), 233-248.
Deransart, C., Hellwig, B., Heupel-Reuter, M., Leger, J. F., Heck, D., Lucking, C. H. (2003). Single-unit analysis of substantia nigra pars reticulata neurons in freely behaving rats with genetic absence epilepsy. Epilepsia 44,1513-1520. doi: 10.1111/j.0013-9580.2003.26603.x
Ding, L., Satish, S., Zhou, C., Gallagher, M. J. (2019). Cortical activation in generalized seizures. Epilepsia 60, 1932-1941. doi: 10.1111/epi.16306.
Drinkenburg, W. H., Coenen, A. M., Vossen, J. M., van Luijtelaar, E. L. (1991). Spike-wave discharges and sleep-wake states in rats with absence epilepsy. Epilepsy Res. 9, 218-224. doi: 10.1016/0920-1211(91)90055-K.
Drinkenburg, W. H., van Schaijk, W. J., van Luijtelaar, E. L., Coenen, A. M. (1993). Aberrant transients in the EEG of epileptic rats: a spectral analytical approach. Physiol. Behav. 54,779-783. doi: 10.1016/0031-9384(93)90092-T.
Glauser, T. A., Cnaan, A., Shinnar, S., Hirtz, D. G., Dlugos, D., Masur, D., et al. (2010). Childhood Absence Epilepsy Study Group. Ethosuximide, valproic acid, and lamotrigine in childhood absence epilepsy. N. Engl. J. Med. 362, 790-799. doi: 10.1056/NEJMoa0902014.
Godlevsky, L. S., Kobolev, E. V., van Luijtelaar, E. L., Coenen, A. M., Stepanenko, K. I., Smirnov, I. V. (2006). Influence of transcranial magnetic stimulation on spike-wave discharges in a genetic model of absence epilepsy. Indian J. Exp. Biol. 44, 949-954.
Gottesmann, C., Gandolfo, G. (1986). A massive but short lasting forebrain deafferentation during sleep in the rat and cat. Arch. Ital. Biol. 124, 257-269.
Gower, A. J., Hirsch, E., Boehrer, A., Noyer, M., Marescaux, C. (1995). Effects of levetiracetam, a novel antiepileptic drug, on convulsant activity in two genetic rat models of epilepsy. Epilepsy Res. 22, 207- 213. doi: 10.1016І0920-1211(95)00077-1.
Inoue, M., Ates, N., Vossen, J. M., Coenen, A. M. (1994). Effects of the neuroleptanalgesic fentanyl-fluanisone (Hypnorm) on spike-wave discharges in epileptic rats. Pharmacol. Biochem. Behav. 48, 547-551. doi: 10.1016І0091-3057(94)90569-Х.
Jando, G., Carpi, D., Kandel, A., Urioste, R., Horvath, Z., Pierre, E., et al. (1995). Spike-and-wave epilepsy in rats: sex differences and inheritance of physiological traits. Neuroscience 64, 301-317. doi: 10.1016І0306-4522(94)00329-4.
Jarre, G., Altwegg-Boussac, T., Williams, M. S., Studer, F., Chipaux, M., David, O., et al. (2017). Building Up Absence Seizures in the Somatosensory Cortex: From Network to Cellular Epileptogenic Processes. Cereb. Cortex 27, 4607-4623. doi: 10.1093ІcercorІbhx174.
Jonak, C. R., Lovelace, J. W., Ethell, I. M., Razak, K. A., Binder, D. K. (2018). Reusable Multielectrode Array Technique for Electroencephalography in Awake Freely Moving Mice. Front. Integr. Neurosci. 12, 53. doi: 10.3389/fnint.2018.00053.
Kovacs, Z., Dobolyi, A., Juhasz, G., Kekesi, K. A. (2014). Lipopolysaccharide induced increase in seizure activity in two animal models of absence epilepsy WAG/ Rij and GAERS rats and Long Evans rats. Brain Res. Bull. 104, 7-18. doi: 10.1016/j.brainresbull.2014.03.003.
Kovacs, Z., Kekesi, K. A., Dobolyi, А, Lakatos, R., Juhasz, G. (2015). Absence epileptic activity changing effects of non-adenosine nucleoside inosine, guanosine and uridine in Wistar Albino Glaxo Rijswijk rats. Neuroscience 300, 593-608. doi: 10.1016/j. neuroscience.2015.05.054.
Lancel, M., Faulhaber, J., Deisz, R. A. (1998). Effect of the GABA uptake inhibitor tiagabine on sleep and EEG power spectra in the rat. Br. J. Pharmacol. 123, 1471-1477. doi: 10.1038/sj.bjp.0701769.
Lannes, B., Micheletti, G., Vergnes, M., Marescaux, C., Depaulis, A., Warter, J. M. (1988). Relationship between spike-wave discharges and vigilance levels in rats with spontaneous petit mal-like epilepsy. Neurosci. Lett. 94, 187-191. doi: 10.1016І0304-3940(88)90293-5.
Leo, A., Caro, C., Nesci, V., Palma, E., Tallarico, M., Iannone, M., et al. (2019). Antiepileptogenic effects of Ethosuximide and Levetiracetam in WAG/Rij rats are only temporary. Pharmacol. Rep. 71, 833-838. doi: 10.1016/j.pharep.2019.04.017.
Lopes da Silva, F., Pijn, J. P., Boeijinga, P. (1989). Interdependence of EEG signals: linear vs. nonlinear associations and the significance of time delays and phase shifts. Brain Topogr. 2, 9-18. doi: 10.1007/ BF01128839.
Luttjohann, A., van Luijtelaar, G. (2015). Dynamics of networks during absence seizure's on- and offset in rodents and man. Front. Physiol. 5;6,16. doi: 10.3389/ fphys.2015.00016.
Marescaux, C., Vergnes, M., Micheletti, G., Depaulis, A., Reis, J., Rumbach, L., et al. (1984). A genetic form of petit mal absence in Wistar rats. Rev. Neurol. (Paris). 140, 63-66.
Maris, E., Bouwman, B. M., Suffczynski, P., Van Rijn, C. M. (2006). Starting and stopping mechanisms of absence epileptic seizures are revealed by hazard functions. J. Neurosci. Meth. 152, 107-115. doi: 10.1016/j. jneumeth.2005.08.016.
Meeren, H. K., Pijn, J. P., Van Luijtelaar, E. L., Coenen, A. M., Lopes da Silva, F. H. (2002). Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J. Neurosci. 22, 1480-1495. doi: 10.1523/JNEUROSCI.22-04-01480.2002.
Meeren, H., van Luijtelaar, G., Lopes da Silva, F., Coenen, A. (2005). Evolving concepts on the pathophysiology of absence seizures: the cortical
focus theory. Arch. Neurol. 62, 371-376. doi: 10.1001/ archneur.62.3.371.
Midzianovskaia, I. S., Kuznetsova, G. D., Coenen, A. M., Spiridonov, A. M., van Luijtelaar, E. L. (2001). Electrophysiological and pharmacological characteristics of two types of spike-wave discharges in WAG/Rij rats. Brain Res. 911, 62-70. doi: 10.1016/ S0006-8993(01)02705-6.
Ngomba, R. T., van Luijtelaar, G. (2018). Metabotropic glutamate receptors as drug targets for the treatment of absence epilepsy. Curr. Opin. Pharmacol. 38, 43-50. doi: 10.1016/j.coph.2018.01.012.
Ngomba, R. T., Santolini, I., Biagioni, F., Molinaro, G., Simonyi, A., van Rijn, C. M., et al. (2011). Protective role for type-1 metabotropic glutamate receptors against spike and wave discharges in the WAG/Rij rat model of absence epilepsy. Neuropharmacology 60 (7-8), 12811291. doi: 10.1016/j.neuropharm.2011.01.007.
Osterhagen, L., Breteler, M., van Luijtelaar, G. (2010). Does arousal interfere with operant conditioning of spike-wave discharges in genetic epileptic rats? Epilepsy Res. 90, 75-82. doi: 10.1016/j.eplepsyres.2010.03.010.
Ovchinnikov, A., Luttjohann, A., Hramov, A., van Luijtelaar, G. (2010). An algorithm for real-time detection of spike-wave discharges in rodents. J. Neurosci. Methods 194, 172-178. doi: 10.1016/j. jneumeth.2010.09.017.
Peeters, B. W., Cheung, K. S., Vossen, J. M., Coenen, A. M. (1992a). Some solvents for antiepileptics have proepileptic potencies in the WAG/Rij rat model for absence epilepsy. Brain Res. Bull. 29, 515-517. doi: 10.1016/0361-9230(92)90092-C.
Peeters, B. W., Kerbusch, J. M., Coenen, A. M., Vossen, J. M., van Luijtelaar, E. L. (1992b). Genetics of spike-wave discharges in the electroencephalogram (EEG) of the WAG/Rij inbred rat strain: a classical Mendelian crossbreeding study. Behav. Genet. 22, 361-368. doi: 10.1007/BF01066667.
Pinault, D., Leresche, N., Charpier, S., Deniau, J. M., Marescaux, C., Vergnes, M., et al. (1998). Intracellular recordings in thalamic neurones during spontaneous spike and wave discharges in rats with absence epilepsy. J. Physiol. 509, 449-456. doi: 10.1111/j.1469-7793.1998.449bn.x.
Pinault, D., Vergnes, M., Marescaux, C. (2001). Medium-voltage 5-9-Hz oscillations give rise to spike-and-wave discharges in a genetic model of absence epilepsy: in vivo dual extracellular recording of thalamic relay and reticular neurons. Neuroscience 105, 181-201. doi: 10.1016/S0306-4522(01)00182-8.
Pinault, D. (2003). Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5-9 Hz oscillations. J. Physiol. 552 (Pt 3), 881-905. doi: 10.1113/jphysiol.2003.046573.
Powell, K. L., Tang, H., Ng, C., Guillemain, I., Dieuset, G., Dezsi, G., et al. (2014). Seizure expression, behavior, and brain morphology differences in colonies of Genetic Absence Epilepsy Rats from Strasbourg. Epilepsia 55, 1959-1968. doi: 10.1111^.12840.
Przewlocka, B., Lason, W., van Luijtelaar, G., Coenen, A., Przewlocki, R. (1996). The role of nitric oxide in genetic model of absence epilepsy in rats. Neurosci. Res. Commun. 18, 125-131. doi: 10.1002/(SICI)1520-6769(199603)18:2<125::AID-NRC148>3.0.CO;2-1.
Remen, L., Bezengon, O., Simons, L., Gaston, R., Downing, D., Gatfield, J., et al. (2016). Preparation, Antiepileptic Activity, and Cardiovascular Safety of Dihydropyrazoles as Brain-Penetrant T-Type Calcium Channel Blockers. J. Med. Chem. 59, 8398-8411. doi: 10.1021Іacs.jmedchem.6b00756.
Russo, E., Andreozzi, F., Iuliano, R., Dattilo, V., Tb, P., Fiume, G., et al. (2014). Early molecular and behavioral response to lipopolysaccharide in the WAGІRij rat model of absence epilepsy and depressive-like behavior, involves interplay between AMPK, AKTmTOR pathways and neuroinflammatory cytokine release. Brain Behav. Immun. 42,157-168. doi: 10.1016/j.bbi.2014.06.016.
Russo, E., Citraro, R., Constanti, A., Leo, A., Luttjohann, A., van Luijtelaar, G., et al. (2016). Upholding WAGІ Rij rats as a model of absence epileptogenesis: Hidden mechanisms and a new theory on seizure development. Neurosci. Biobehav. Rev. 71, 388-408. doi: 10.10Щ. neubiorev.2016.09.017.
Sarkisova, K. Y., Gabova, A. V. (2018). Maternal care exerts disease-modifying effects on genetic absence epilepsy and comorbid depression. Genes Brain Behav. 17 (7), e12477. doi: 10.1111^.12477.
Sarkisova, K. Y., Kuznetsova, G. D., Kulikov, M. A., van Luijtelaar, G. (2010). Spike-wave discharges are necessary for the expression of behavioral depression-like symptoms. Epilepsia 51, 146-160. doi: 10.1111^.1528-1167.2009.02260.x.
Schridde, U., van Luijtelaar, G. (2004). The influence of strain and housing on two types of spike-wave discharges in rats. Genes Brain Behav. 3, 1-7. doi: 10.1111/j.1601-1848.2004.00034.x.
Sitnikova, E., van Luijtelaar, G. (2007). Electroencephalographic characterization of spike-wave discharges in cortex and thalamus in WAG7Rij rats. Epilepsia 48, 2296-2311. doi: 10.1111^.1528-1167.2007.01250.x.
Sitnikova, E., Hramov, A. E., Koronovsky, A. A., van Luijtelaar, G. (2009). Sleep spindles and spike-wave discharges in EEG: Their generic features, similarities and distinctions disclosed with Fourier transform and continuous wavelet analysis. J. Neurosci. Methods 180, 304-316. doi: 10.1016/j.jneumeth.2009.04.006.
Sitnikova, E., Rutskova, E. M., Raevsky, V. V. (2016). Maternal care affects EEG properties of spike-wave seizures (including pre- and post ictal periods) in adult WAG!Rij rats with genetic predisposition to absence epilepsy. Brain Res. Bull. 127,84-91. doi: 10.1016/j.brainresbull.2016.08.019
Smyk, M. K., Coenen, A. M., Lewandowski, M. H., van Luijtelaar, G. (2011). Endogenous rhythm of absence epilepsy: relationship with general motor activity and sleep-wake states. Epilepsy Res. 93, 120-127. doi: 10.1016Іj.eplepsyres.2010.11.003.
Smyk, M. K., Sysoev, I. V., Sysoeva, M. V., van Luijtelaar, G., Drinkenburg, W. H. (2019a). Can absence seizures be predicted by vigilance states?: Advanced analysis of sleep-wake states and spike-wave discharges' occurrence in rats. Epilepsy Behav. 96, 200-209. doi: 10.10Щ.УЄЬЄЬІ.2019.04.012.
Smyk, M. K., van Luijtelaar, G., Huysmans, H., Drinkenburg, W. H. (2019b). Spike-Wave Discharges and Sleep-Wake States during Circadian Desynchronization: No Effects of Agomelatine upon Re-Entrainment. Neuroscience 408, 327-338. doi: 10.1016/j.neuroscience.2019.03.062.
Stefan, H., Lopes da Silva, F. H. (2013). Epileptic neuronal networks: methods of identification and clinical relevance. Front. Neurol. Mar 14, 8. doi: 10.3389/ fneur.2013.00008.
Sysoeva, M. V., Luttjohann, A., van Luijtelaar, G., Sysoev, I. V. (2016). Dynamics of directional coupling underlying spike-wave discharges. Neuroscience 314, 75-89. doi: 10.1016/j. neuroscience.2015.11.044.
Taylor, J. A., Rodgers, K. M., Bercum, F. M., Booth, C. J., Dudek, F. E., Barth, D. S. (2017). Voluntary Control of Epileptiform Spike-Wave Discharges in Awake Rats. J. Neurosci. 37, 5861-5869. doi: 10.1523І JNEUROSCI.3235-16.2017.
Taylor, J. A., Reuter, J. D., Kubiak, R. A., Mufford, T. T., Booth, C. J., Dudek, F. E., et al. (2019). Spontaneous Recurrent Absence Seizure-like Events in Wild-Caught Rats. J. Neurosci. 39, 4829-4841. doi: 10.1523І JNEUROSCI.1167-18.2019.
Tenney, J. R., Glauser, T. A. (2013). The current state of absence epilepsy: can we have your attention? Epilepsy Curr. 13, 135-140. doi: 10.1016Іj.eplepsyres.2013.05.006.
Thatcher, R. W. (2012). Coherence, Phase Differences, Phase Shift, and Phase Lock in EEGZ ERP Analyses. Dev. Neuropsychol. 37:6, 476-496. doi: 10.1080І87565641.2011.619241.
Tolmacheva, E. A., van Luijtelaar, G. (2007). Absence seizures are reduced by the enhancement of GABA-ergic inhibition in the hippocampus in WAG!Rij rats. Neurosci. Lett. 416, 17-21. doi: 10.1016^^^.2007.01.038.
Tolmacheva, E. A., Oitzl, M. S., van Luijtelaar, G. (2012). Stress, glucocorticoids and absences in a genetic epilepsy model. Horm. Behav. 61, 706-710. doi: 10.1016Zj.yhbeh.2012.03.004.
Tringham, E., Powell, Kl, Cain, S. M., Kuplast, K., Mezeyova, J., Weerapura, M., et al. (2012). T-Type Calcium channel blockers that attenuate thalamic burst firing and suppress absence seizures. Sci. Trans. Med. 4, 121ra19. doi: 10.1126Іscitranslmed.3003120.
van Luijtelaar, E. L., Coenen, A. M. (1986). Two types of electrocortical paroxysms in an inbred strain of rats. Neurosci. Lett. 70, 393-397. doi: 10.1016/0304-3940(86)90586-0.
van Luijtelaar, E. L., Coenen, A. M. (1988). Circadian rhythmicity in absence epilepsy in rats. Epilepsy Res. 2, 331-336. doi: 10.1016І0920-1211(88)90042-3.
van Luijtelaar, G., Zobeiri, M. (2014). Progress and outlooks in a genetic absence epilepsy model (WAG/ Rij). Curr. Med. Chem. 21, 704-721. doi: 10.2174/092 9867320666131119152913.
van Luijtelaar, E. L., Van der Werf, S. J., Vossen, J. M., Coenen, A. M. (1991). Arousal, performance and absence seizures in rats. Electroencephalogr. Clin. Neurophysiol. 79, 430-434. doi: 10.1016/0013-4694(91)90208-L.
van Luijtelaar, E. L., Ates, N., van der Staay, F. J. (1994). The effects of chronic treatment with a calcium channel antagonist on two types of generalized epilepsies in rats. Pharmacol Biochem Behav. 48, 575-579.
van Luijtelaar, E. L., Dirksen, R., Vree, T., van Haaren, F. (1996). Effects of acute and chronic cocaine administration on EEG and behaviour in intact and castrated male and intact and ovariectomized female rats. Brain Res. Bull. 40, 43-50. doi: 10.1016/0361-9230(96)00005-6.
van Luijtelaar, G., Budziszewska, B., Jaworska-Feil, L., Ellis, J., Coenen, A., Lason, W. (2001). The ovarian hormones and absence epilepsy: a long-term EEG study and pharmacological effects in a genetic absence epilepsy model. Epilepsy Res. 6, 225-239. doi: 10.1016/ S0920-1211(01)00277-7.
van Luijtelaar, G., Sitnikova, E., Luttjohann, A. (2011). On the origin and suddenness of absences in genetic absence models. Clin. EEG Neurosci. 42, 83-97. doi: 10.1177/155005941104200209.
van Luijtelaar, G., Lyashenko, S., Vastyanov, R., Verbeek, G., Oleinik, A., van Rijn, C., et al. (2012a). Cytokines and absence seizures in a genetic rat model neurophysiology 43, 478-486. doi: 10.1007/s11062-012-9252-6.
van Luijtelaar, G., Wilde, M., Citraro, R., Scicchitano, F., van Rijn, C. (2012b). Does antiepileptogenesis affect sleep in genetic epileptic rats? Int. J. Psychophysiol. 85, 49-54. doi: 10.1016/j.ijpsycho.2011.09.010.
van Luijtelaar, G., Mishra, A. M., Edelbroek, P., Coman, D., Frankenmolen, N., Schaapsmeerders, P., et al. (2013). Anti-epileptogenesis: Electrophysiology, diffusion tensor imaging and behavior in a genetic absence model. Neurobiol. Dis. 60, 126-138. doi: 10.1016/j.nbd.2013.08.013.
van Luijtelaar, G., Onat, F. Y., Gallagher, M. J. (2014). Animal models of absence epilepsies: What do they model and do sex and sex hormones matter? Neurobiol. Dis. 72 (Pt B), 167-179. doi: 10.1016/j. nbd.2014.08.014.
van Luijtelaar, G., Luttjohann, A., Makarov, V. V., Maksimenko, V. A., Koronovskii, A. A., Hramov, A. E. (2016). Methods of automated absence seizure detection, interference by stimulation, and possibilities for prediction in genetic absence models. J. Neurosci. Methods 260, 144-158. doi: 10.1016/j. jneumeth.2015.07.010.
van Luijtelaar, G., Zobeiri, M., Luttjohann, A., Depaulis,
A. (2017). "Experimental treatment options in absence epilepsy," in Current Pharmaceutical design", vol. 23 .Eds. Aguglia, U., Beghi, E. (Liverpool: Bentham Science Publishers), 5577-5592.
van Rijn, C. M., Weyn Banningh, E. W., Coenen, A. M. (1994). Effects of lamotrigine on absence seizures in rats. Pol. J. Pharmacol. 46, 467-470.
van Rijn, C. M., Gaetani, S., Santolini, I., Badura, A., Gabova, A., Fu, J., et al. (2010). WAG/Rij rats show a reduced expression of CB1 receptors in thalamic nuclei and respond to the CB1 receptor agonist, R(+) WIN55,212-2, with a reduced incidence of spike-wave discharges. Epilepsia 51, 1511-1521. doi: 10.1111/j.1528-1167.2009.02510.x.
Vyssotski, A. L., Serkov, A. N., Itskov, P. M., Dell'Omo, G., Latanov, A. V., Wolfer, D. P., et al. (2006). Miniature neurologgers for flying pigeons: multichannel EEG and action and field potentials in combination with GPS recording. J. Neurophysiol. 95, 1263-1273. doi: 10.1152/ jn.00879.2005.
Wang, J., Ethridge, L. E., Mosconi, M. W., White, S. P., Binder, D. K., Pedapati, E. V., et al. (2017). A resting EEG study of neocortical hyperexcitability and altered functional connectivity in fragile X syndrome. J. Neurodevelop Disord. 9, 11. doi: 10.1186/s11689-017-9191-z.
Wasilczuk, A. Z., Proekt, A., Max, B., Kelz, M.
B., McKinstry-Wu, A. R. (2016). High-density electroencephalographic acquisition in a rodent model using low-cost and open-source resources. J. Vis. Exp. (117), e54908. doi: 10.3791/54908.
Weir, B. (1965). The morphology of the spike-wave complex. Electroencephalogr. Clin. Neurophysiol. 19, 284-290. doi: 10.1016І0013-4694(65)90208-7.
Westerhuis, F., van Schaijk, W., van Luijtelaar, G. (1996). "Automatic detection of spike-wave discharges in the cortical EEG of rats," in Measuring Behaviour 96, vol. p. Ed. Beaujean (Noldus Information Technology), 109-110.
Westmijse, I., Ossenblok, P., Gunning, B., van Luijtelaar, G. (2009). Onset and propagation of spike and slow wave discharges in human absence epilepsy: A MEG study. Epilepsia 50, 2538-2548. doi: 10.1111/j.1528-1167.2009.02162.x.
Willoughby, J. O., Mackenzie, L. (1992). Nonconvulsive electrocorticographic paroxysms (absence epilepsy) in rat strains. Lab. Anim. Sci. 42, 551-554.
Downloads
Published
How to Cite
Issue
Section
License
Journal Medical Informatics and Engineering allows the author(s) to hold the copyright without registration
The majority of Medical Informatics and Engineering Open Access journals publish open access articles under the terms of the Creative Commons Attribution (CC BY) License which permits use, distribution and reproduction in any medium, provided the original work is properly cited. The remaining journals offer a choice of licenses.
This journal is available through Creative Commons (CC) License CC-BY 4.0
