Behavioural and electrophysiological features of WAG/Rij rats with different forms of genetic epilepsy

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WAG/Rij rats are widely used as a genetic model of absence epilepsy. Approximately 15–50% rats of the strain are susceptible to audiogenic seizures. WAG/Rij rats demonstrate depressive-like behavior. After preliminary sound provocation an increased level of anxiety was found in audiogenic susceptible WAG/Rij subgroup. Electrophysiological and behavioral studies suggest the involvement of the dopaminergic system in both absence and audiogenic epilepsy. An increased binding density to dopamine receptors was found in the dorsal striatum subregions in audiogenic prone rats compared to non-audiogenic. The study aims were (1) to determine whether behavioral changes in WAG/Rij rats were genetically determined or induced by prior sound stimulation; (2) how regions of the dorsal striatum with different density of dopamine receptors in subpopulations of WAG/Rij rats are involved in the absence epilepsy control. The study was conducted using two rat groups: WAG/Rij-nonAGS (absence epilepsy) and WAG/Rij-AGS (mixed epilepsy). The study was performed using tests: “Elevated plus maze”, “Forced swimming” and “Three chamber sociability test”. High-frequency deep brain stimulation was performed for evaluation of dorsal striatum involvement in the absence seizure control. After experiments animals were tested for the susceptibility to audiogenic seizures. It demonstrated that the increased level of anxiety in WAG/Rij-AGS rats is genetically determined, while depressive-like behavior in WAG/Rij rats is not dependent on a predisposition to audiogenic seizures. Deviations in social behavior were observed in WAG/Rij-AGS rats. Stimulation of the dorsal striatum indicates differences in the control of absence and mixed forms of epilepsy in the

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Sobre autores

К. Abbasova

Lomonosov Moscow State University

Autor responsável pela correspondência
Email: abbasovakr@my.msu.ru
Rússia, Moscow

S. Kuzhuget

Lomonosov Moscow State University

Email: abbasovakr@my.msu.ru
Rússia, Moscow

Е. Tsyba

Lomonosov Moscow State University

Email: abbasovakr@my.msu.ru
Rússia, Moscow

Bibliografia

  1. Yuen AWC, Keezer MR, Sander JW (2018) Epilepsy is a neurological and a systemic disorder. Epilepsy Behav 78: 57–61. https://doi.org/10.1016/j.yebeh.2017.10.010
  2. Alsaadi T, El Hammasi K, Shahrour TM, Shakra M, Turkawi L, Almaskari B, Diab L, Raoof M (2015) Prevalence of depression and anxiety among patients with epilepsy attending the epilepsy clinic at Sheikh Khalifa Medical City, UAE: A cross-sectional study. Epilepsy Behav 52(Pt A): 194–199. https://doi.org/10.1016/j.yebeh.2015.09.008
  3. Coenen AM, Van Luijtelaar EL (2003) Genetic animal models for absence epilepsy: a review of the WAG/Rij strain of rats. Behav Genet 33(6): 635–655. https://doi.org/10.1023/a:1026179013847
  4. Midzyanovskaya IS, Kuznetsova GD, Vinogradova LV, Shatskova AB, Coenen AML, van Luijtelaar G (2004) Mixed forms of epilepsy in a subpopulation of WAG/Rij rats. Epilepsy Behav 5: 655–661. https://doi.org/10.1016/j.yebeh.2004.06.021
  5. Hughes JR (2009) Absence seizures: A review of recent reports with new concepts. Epilepsy Behav 15(4): 404–412. https://doi.org/10.1016/j.yebeh.2009.06
  6. Clément Y, Bondoux D, Launay JM, Chapouthier G (1997) Convulsive effects of a benzodiazepine receptor inverse agonist: are they related to anxiogenic processes? J Physiol (Paris) 91(1): 21–29. https://doi.org/10.1016/s0928-4257(99)80162-4
  7. Depaulis A, Helfer V, Deransart C, Marescaux C (1997) Anxiogenic-like consequences in animal models of complex partial seizures. Neurosci Biobehav Rev 21(6): 767–774. https://doi.org/10.1016/s0149-7634(96)00060-7
  8. Sarkisova KY, Kulikov MA (2006) Behavioral characteristics of WAG/Rij rats susceptible and non-susceptible to audiogenic seizures. Behav Brain Res 166(1): 9–18. https://doi.org/10.1016/j.bbr.2005.07.024
  9. Tsyba E, Midzyanovskaya I, Birioukova L, Tuomisto L, van Luijtelaar G, Abbasova K (2023) Striatal Patchwork of D1-like and D2-like Receptors Binding Densities in Rats with Genetic Audiogenic and Absence Epilepsies. Diagnostics 13: 587. https://doi.org/10.3390/diagnostics13040587
  10. Ross KC, Coleman JR (2000) Developmental and genetic audiogenic seizure models: behavior and biological substrates. Neurosci Biobehav Rev 24(6): 639–653. https://doi.org/10.1016/s0149-7634(00)00029-4
  11. Gale K, Proctor M, Veliskova J, Nehlig A (2008) BASAL GANGLIA AND BRAINSTEM ANATOMY AND PHYSIOLOGY. Epilepsy Comprehensive Textbook 3: 367. https://www.researchgate.net/publication/281392567
  12. Cools AR, Coolen JMM, Smit JCA, Ellenbroek BA (1984) The striato-nigro-collicular pathway and explosive running behaviour: Functional interaction between neostriatal dopamine and collicular GABA. Eur J Pharmacol 100(1): 71–77. https://doi.org/10.1016/0014-2999(84)90316-9
  13. 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(3): 371–376. https://doi.org/10.1001/archneur.62.3.371
  14. Abbasova KR, Chepurnov SA, Chepurnova NE, van Luijtelaar G (2010) The role of perioral afferentation in the occurrenceof spike-wave discharges in the WAG/Rij model of absence epilepsy. Brain Res 1366: 257–262. https://doi.org/10.1016/j.brainres.2010.10.007
  15. Tugba EK, Medine GIO, Ozlem A, Deniz K, Filiz OY (2022) Prolongation of absence seizures and changes in serotonergic and dopaminergic neurotransmission by nigrostriatal pathway degeneration in genetic absence epilepsy rats. Pharmacol Biochem Behav 213: 173317. https://doi.org/10.1016/j.pbb.2021.173317
  16. Kanner AM (2008) Mood disorder and epilepsy: a neurobiologic perspective of their relationship. Dialogues Clin Neurosci 10(1): 39–45. https://doi.org/10.31887/DCNS.2008.10.1/amkanner
  17. Jones NC, O'Brien TJ (2013) Stress, epilepsy, and psychiatric comorbidity: how can animal models inform the clinic? Epilepsy Behav 26(3): 363–369. https://doi.org/10.1016/j.yebeh.2012.09.002
  18. Birioukova LM, Midzyanovskaya IS, Lensu S, Tuomisto L, van Luijtelaar G (2005) Distribution of D1-like and D2-like dopamine receptors in the brain of genetic epileptic WAG/Rij rats. Epilepsy Res 63(2–3): 89–96. https://doi.org/10.1016/j.eplepsyres.2004.12.001
  19. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14(3): 149–167. https://doi.org/10.1016/0165-0270(85)90031-7
  20. Landauer MR, Balster RL (1982) A new test for social investigation in mice: Effects of d-amphetamine. Psychopharmacology (Berl) 78(4): 322–325. https://doi.org/10.1007/BF00433734
  21. Wee B (1995) Mate preference and avoidance in female rats following treatment with scopolamine. Physiol Behav 58(1): 97–100. https://doi.org/10.1016/0031-9384(95)00029-i
  22. Porsolt RD, Anton G, Blavet N, Jalfre M (1978) Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47(4): 379–391. https://doi.org/10.1016/0014-2999(78)90118-8
  23. Щетинин ЕВ, Батурин ВА, Арушанян ЕБ, Ованесов КБ, Попов АВ (1989) Биоритмологический подход к оценке вынужденного плавания как экспериментальная модель «депрессивного» состояния. Журн высш нерв деятельн им ИП Павлова 39(5): 958–964. [Shchetinin EV, Baturin VA, Arushanian EB, Ovanesov KB, Popov AV (1989) A biorhythmologic approach to evaluating forced swimming as an experimental model of a "depressive" state. Zh Vyssh Nerv Deiat Im IP Pavlova 39(5): 958-964. (In Russ)].
  24. Paxinos G, Watson C (2005) The Rat Brain in Stereotaxic Coordinates. The New Coronal Set. 5th Edition.
  25. Cervenka S, Hedman E, Ikoma Y, Djurfeldt DR, Rück C, Halldin C, Lindefors N (2012) Changes in dopamine D2-receptor binding are associated to symptom reduction after psychotherapy in social anxiety disorder. Transl Psychiatry 2(5): e120. https://doi.org/10.1038/tp.2012.40
  26. Bogdanova OV, Kanekar S, D'Anci KE, Renshaw PF (2013) Factors influencing behavior in the forced swim test. Physiol Behav 118: 227–239. https://doi.org/10.1016/j.physbeh.2013.05.012
  27. Molendijk ML, de Kloet ER (2022) Forced swim stressor: Trends in usage and mechanistic consideration. Eur J Neurosci 55: 2813–2831. https://doi.org/10.1111/ejn.15139
  28. Anyan J, Amir S (2018) Too Depressed to Swim or Too Afraid to Stop? A Reinterpretation of the Forced Swim Test as a Measure of Anxiety-Like Behavior. Neuropsychopharmacology 43: 931–933. https://doi.org/10.1038/npp.2017.260
  29. Commons KG, Cholanians AB, Babb JA, Ehlinger DG (2017) The Rodent Forced Swim Test Measures Stress-Coping Strategy, Not Depression-like Behavior. ACS Chem Neurosci 8(5): 955–960. https://doi.org/10.1021/acschemneuro.7b00042
  30. Sarkisova KY, Kuznetsova GD, Kulikov MA, van Luijtelaar G (2010) Spike-wave discharges are necessary for the expression of behavioral depression-like symptoms. Epilepsia 51(1): 146–160. https://doi.org/10.1111/j.1528-1167.2009.02260.x
  31. Overstreet DH (1993) The Flinders sensitive line rats: a genetic animal model of depression. Neurosci Biobehav Rev17(1): 51–68. https://doi.org/10.1016/s0149-7634(05)80230-1
  32. Broadhurst PL (1975) The Maudsley reactive and nonreactive strains of rats: a survey. Behav Genet 5(4): 299–319. https://doi.org/10.1007/BF01073201
  33. Broadhurst PL, Bignami G (1965) Correlative effects of psychogenetic selection: a study of the Roman high and low avoidance strains of rats. Behav Res Ther 3: 273–280. https://doi.org/10.1016/0005-7967(64)90033-6
  34. Overstreet DH, Friedman E, Mathé AA, Yadid G (2005) The Flinders Sensitive Line rat: a selectively bred putative animal model of depression. Neurosci Biobehav Rev 29(4–5): 739–759. https://doi.org/10.1016/j.neubiorev.2005.03.015
  35. Rebik AA, Riga VD, Smirnov KS, Sysoeva OV, Midzyanovskaya IS (2022) Social Behavioral Deficits in Krushinsky-Molodkina Rats, an Animal Model of Audiogenic Epilepsy. J Pers Med 12(12): 2062. https://doi.org/10.3390/jpm12122062
  36. Rebik A, Broshevitskaya N, Kuzhuget S, Aleksandrov P, Abbasova K, Zaichenko M, Midzyanovskaya I (2023) Audiogenic Seizures and Social Deficits: No Aggravation Found in Krushinsky – Molodkina Rats. Biomedicines 11(9): 2566. https://doi.org/10.3390/biomedicines11092566
  37. Midzyanovskaya IS, Shatskova AB, MacDonald E, Van Luijtelaar G, Tuomisto L (2020) Brain Aminergic Deficiency in Absence Epileptic Rats: Dependency on Seizure Severity and Their Functional Coupling at Rest. J Behav Brain Sci 10: 29–45. https://doi.org/10.4236/jbbs.2020.101003
  38. Wicker E, Beck VC, Kulick-Soper C, Kulick-Soper CV, Hyder SK, Campos-Rodriguez C, Khan T, N'Gouemo P, Forcelli PA (2019) Descending projections from the substantia nigra pars reticulata differentially control seizures. Proc Natl Acad Sci U S A 116(52): 27084–27094. https://doi.org/10.1073/pnas.1908176117
  39. Lu E, Pyatka N, Burant CJ, Sajatovic M (2021) Systematic Literature Review of Psychiatric Comorbidities in Adults with Epilepsy. J Clin Neurol 17(2): 176–186. https://doi.org/10.3988/jcn.2021.17.2.176
  40. Gómez-Arias B, Crail-Meléndez D, López-Zapata R, Martínez-Juárez IE (2012) Severity of anxiety and depression are related to a higher perception of adverse effects of antiepileptic drugs. Seizure 21(8): 588–594. https://doi.org/10.1016/j.seizure.2012.06.003
  41. Nanau RM, Neuman MG (2013) Adverse drug reactions induced by valproic acid. Clin Biochem 46(15): 1323–1338. https://doi.org/10.1016/j.clinbiochem.2013.06.012
  42. Boylan LS, Flint LA, Labovitz DL, Jackson SC, Starner K, Devinsky O (2004) Depression but not seizure frequency predicts quality of life in treatment-resistant epilepsy. Neurology 62(2): 258–261. https://doi.org/10.1212/01.wnl.0000103282.62353.85

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2. Fig. 1. Research scheme.

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3. Fig. 2. Schematic diagram of the electrophysiological experiment. SSC – somatosensory cortex, DS – dorsal striatum.

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4. Fig. 3. Elevated Plus Maze test. Comparison of the Wistar-nonAGS, WAG/Rij-nonAGS, and WAG/Rij-AGS groups. (a) Time in closed arms, * p < 0.05, One-way ANOVA with Tukey's correction for multiple comparisons, data are presented as M ± SEM; (b) Time in the light, * p < 0.05, One-way ANOVA with Tukey's correction for multiple comparisons, M ± SEM; (c) Number of hangings from open arms, * p < 0.05, Kruskal–Wallis test using Dunn's multiple comparison test, Me ± IQR.

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5. Fig. 4. Three-chamber social maze test, first landing. * – reliable differences from the time spent in the compartment next to the stimulus (Two-way ANOVA, Sidak correction for multiple comparisons). Data are presented as the mean and standard error of the mean.

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6. Fig. 5. Forced swimming test. Comparison of active swimming time (a) and immobility time (b) in Wistar-nonAGS, WAG/Rij-nonAGS, and WAG/Rij-AGS rats. * – significant differences from Wistar-nonAGS (One-way ANOVA with Tukey’s correction), no significant differences were found between WAG/Rij-nonAGS and WAG/Rij-AGS rats. Comparison of active swimming time (c) and immobility time (d) in Wistar (WS) and WAG/Rij (WR) rats. # – significant differences, unpaired t-test. Data are presented as the mean and standard error of the mean.

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7. Fig. 6. Average duration of discharges before (baseline), during (130 Hz) and after (1/2/3h) high-frequency stimulation of the dorsal striatum (a, b) and somatosensory cortex (c, d) in non-audiogenic and audiogenic WAG/Rij rats. *p < 0.05, **p < 0.01 (DS – one-way ANOVA, Holm–Sidak test; SSC – Friedman criterion). Data are presented as mean and standard error of the mean.

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