Effect of High- and low-frequency stimulation of olfactory bulb on open field activity monitoring indices in kindled rats

Document Type : Original Research

Authors
P. Zarei 1
A. Shojaei 1
Y. Fathollahi 1
M. R. Raoufy 1
J. Mirnajafi-Zadeh 2
1 Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
2 Department of Physiology, Faculty of Medical Sciences, Tarbiast Modates University, Tehran, Iran
Abstract
Deep brain stimulation (DBS) stands as an alternative treatment for drug-resistant temporal lobe epilepsies. In this study, we investigated the effects of both low- and high-frequency stimulation (LFS and HFS) of the olfactory bulb on locomotor activity and preferences for spending time in the central or border regions. Rats underwent a kindling procedure involving semi-rapid electrical stimulation (6 stimulations per day) of the hippocampal CA1 region. Fully kindled animals received LFS (1 Hz) or HFS (130 Hz) at four time points: 5 min, 6 h, 24 h, and 30 h after the last kindling stimulation. Subsequently, rats were placed in the open field chamber and allowed free, uninterrupted movement within the respective quadrant of the maze for a single 10-minute period. During this time, tracking software recorded movement, and locomotor activity as well as preferences for spending time in the central or border regions were evaluated. Overall, applying DBS in the olfactory bulb at both low and high frequencies decreased exploration time in the center and increased exploration time in the border for the rats. Furthermore, a higher intensity of HFS was more effective than a lower intensity of HFS in reducing anxiety or altering locomotor behavior. According to the results of the present study it may be suggested that applying DBS affects some aspects of the animals’ activity and therefore, the activity monitoring tests have to be done following DBS application.

Keywords

1. Deng J, Luan G. Mechanisms of Deep Brain Stimulation for Epilepsy and Associated Comorbidities. Neuropsychiatry. 2017:31–7.
2. Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55(4):475-82.
3. Banerjee PN, Filippi D, Allen Hauser W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res. 2009;85(1):31-45.
4. Dell KL, Cook MJ, Maturana MI. Deep Brain Stimulation for Epilepsy: Biomarkers for Optimization. Current Treatment Options in Neurology. 2019;21(10):47.
5. Fiest KM, Sauro KM, Wiebe S, Patten SB, Kwon CS, Dykeman J, et al. Prevalence and incidence of epilepsy: A systematic review and meta-analysis of international studies. Neurology. 2017;88(3):296-303.
6. Halpern CH, Samadani U, Litt B, Jaggi JL, Baltuch GH. Deep brain stimulation for epilepsy. Neurotherapeutics. 2008;5(1):59-67.
7. Löscher W. Animal models of intractable epilepsy. Progress in neurobiology. 1997;53(2):239-58.
8. Bernard C, Anderson A, Becker A, Poolos NP, Beck H, Johnston D. Acquired dendritic channelopathy in temporal lobe epilepsy. Science. 2004;305(5683):532-5.
9. Spencer SS, Spencer DD. Entorhinal‐hippocampal interactions in medial temporal lobe epilepsy. Epilepsia. 1994;35(4):721-7.
10. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993;361(6407):31.
11. Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR. Recognition memory and the human hippocampus. Neuron. 2003;37(1):171-80.
12. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. Journal of neuroscience methods. 1984;11(1):47-60.
13. Téllez-Zenteno JF, Hernández-Ronquillo L. A review of the epidemiology of temporal lobe epilepsy. Epilepsy research and treatment. 2012;2012.
14. Matos G, Ribeiro DA, Alvarenga TA, Hirotsu C, Scorza FA, Le Sueur-Maluf L, et al. Behavioral and genetic effects promoted by sleep deprivation in rats submitted to pilocarpine-induced status epilepticus. Neuroscience letters. 2012;515(2):137-40.
15. Gourévitch B, Kay LM, Martin C. Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task. Journal of neurophysiology. 2010;103(5):2633-41.
16. Esmaeilpour K, Sheibani V, Shabani M, Mirnajafi-Zadeh J, Akbarnejad Z. Low frequency stimulation reverses the kindling-induced impairment of learning and memory in the rat passive-avoidance test. Basic and clinical neuroscience. 2018;9(1):51.
17. Ghafouri S, Fathollahi Y, Javan M, Shojaei A, Asgari A, Mirnajafi-Zadeh J. Effect of low frequency stimulation on impaired spontaneous alternation behavior of kindled rats in Y-maze test. Epilepsy research. 2016;126:37-44.
18. Ghorbani P, Mohammad-Zadeh M, Mirnajafi-Zadeh J, Fathollahi Y. Effect of different patterns of low-frequency stimulation on piriform cortex kindled seizures. Neuroscience letters. 2007;425(3):162-6.
19. Li MC, Cook MJ. Deep brain stimulation for drug‐resistant epilepsy. Epilepsia. 2018;59(2):273-90.
20. Klinger N, Mittal S. Deep brain stimulation for seizure control in drug-resistant epilepsy. Neurosurgical focus. 2018;45(2):E4.
21. Goodman JH, Berger RE, Tcheng TK. Preemptive low‐frequency stimulation decreases the incidence of amygdala‐kindled seizures. Epilepsia. 2005;46(1):1-7.
22. Mohammad-Zadeh M, Mirnajafi-Zadeh J, Fathollahi Y, Javan M, Jahanshahi A, Noorbakhsh S, et al. The role of adenosine A1 receptors in mediating the inhibitory effects of low frequency stimulation of perforant path on kindling acquisition in rats. Neuroscience. 2009;158(4):1632-43.
23. Jiang Y, Pun RY, Peariso K, Holland KD, Lian Q, Danzer SC. Olfactory bulbectomy leads to the development of epilepsy in mice. PLoS One. 2015;10(9):e0138178.
24. Hall CS. Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. Journal of Comparative psychology. 1934;18(3):385.
25. Walsh RN, Cummins RA. The open-field test: a critical review. Psychological bulletin. 1976;83(3):482.
26. Paxinos G, Watson C. The rat brain in stereotaxic coordinates: hard cover edition: Elsevier; 2006.
27. Imai T, editor Construction of functional neuronal circuitry in the olfactory bulb. Seminars in cell & developmental biology; 2014: Elsevier.
28. Soudry Y, Lemogne C, Malinvaud D, Consoli S-M, Bonfils P. Olfactory system and emotion: common substrates. European annals of otorhinolaryngology, head and neck diseases. 2011;128(1):18-23.
29. Vaughan DN, Jackson GD. The piriform cortex and human focal epilepsy. Frontiers in neurology. 2014;5:259.
30. Powell T, Cowan W, Raisman G. The central olfactory connexions. Journal of Anatomy. 1965;99(Pt 4):791.
31. Espinosa‐Jovel C, Toledano R, Jiménez‐Huete A, Aledo‐Serrano Á, García‐Morales I, Campo P, et al. Olfactory function in focal epilepsies: Understanding mesial temporal lobe epilepsy beyond the hippocampus. Epilepsia open. 2019;4(3):487-92.
32. Young JC, Vaughan DN, Nasser HM, Jackson GD. Anatomical imaging of the piriform cortex in epilepsy. Experimental neurology. 2019;320:113013.
33. Young JC, Vaughan DN, Paolini AG, Jackson GD. Electrical stimulation of the piriform cortex for the treatment of epilepsy: a review of the supporting evidence. Epilepsy & Behavior. 2018;88:152-61.
34. Desai M, Agadi J, Karthik N, Praveenkumar S, Netto A. Olfactory abnormalities in temporal lobe epilepsy. Journal of Clinical Neuroscience. 2015;22(10):1614-8.
35. Hummel T, Henkel S, Negoias S, Galván JR, Bogdanov V, Hopp P, et al. Olfactory bulb volume in patients with temporal lobe epilepsy. Journal of neurology. 2013;260(4):1004-8.
36. Morales-Medina J, Juarez I, Venancio-Garcia E, Cabrera S, Menard C, Yu W, et al. Impaired structural hippocampal plasticity is associated with emotional and memory deficits in the olfactory bulbectomized rat. Neuroscience. 2013;236:233-43.
Pathobiology Reserach
Volume 25, Issue 2
February 2022
Pages 47-54