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Clinical and Developmental Immunology
Volume 2013, Article ID 698634, 9 pages
http://dx.doi.org/10.1155/2013/698634
Research Article

Chronic Deep Brain Stimulation of the Hypothalamic Nucleus in Wistar Rats Alters Circulatory Levels of Corticosterone and Proinflammatory Cytokines

1Laboratory of Neuroimmunoendocrinology, National Institute of Neurology and Neurosurgery “Manuel Velasco Suárez”, Avenida Insurgentes Sur 3877, La Fama, Tlalpan, 14269 Mexico City, DF, Mexico
2Laboratory of Reticular Formation Physiology, National Institute of Neurology and Neurosurgery “Manuel Velasco Suárez”, Avenida Insurgentes Sur 3877, La Fama, Tlalpan, 14269 Mexico City, DF, Mexico
3Department of Pharmacology, School of Medicine, National Autonomous University of Mexico, P.O. Box 70-297, Coyoacan, 04510 Mexico City, DF, Mexico
4Department of Psychoimmunology, National Institute of Psychiatry “Ramón de la Fuente”, Calzada México-Xochimilco 101, Col. San Lorenzo Huipulco, Tlalpan, 14370 Mexico City, DF, Mexico

Received 20 July 2013; Revised 4 September 2013; Accepted 5 September 2013

Academic Editor: Oscar Bottasso

Copyright © 2013 Juan Manuel Calleja-Castillo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. L. Benabid, “What the future holds for deep brain stimulation,” Expert Review of Medical Devices, vol. 4, no. 6, pp. 895–903, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. A. L. Benabid, A. Benazzous, and P. Pollak, “Mechanisms of deep brain stimulation,” Movement Disorders, vol. 17, supplement 3, pp. S73–S74, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. A. M. Lozano, P. Giacobbe, C. Hamani et al., “A multicenter pilot study of subcallosal cingulate area deep brain stimulation for treatment-resistant depression: clinical article,” Journal of Neurosurgery, vol. 116, no. 2, pp. 315–322, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Boon, R. Raedt, V. de Herdt, T. Wyckhuys, and K. Vonck, “Electrical Stimulation for the Treatment of Epilepsy,” Neurotherapeutics, vol. 6, no. 2, pp. 218–227, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. H. J. M. Majoie, K. Rijkers, M. W. Berfelo et al., “Vagus nerve stimulation in refractory epilepsy: effects on pro-and anti-inflammatory cytokines in peripheral blood,” NeuroImmunoModulation, vol. 18, no. 1, pp. 52–56, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. V. de Herdt, S. Bogaert, K. R. Bracke et al., “Effects of vagus nerve stimulation on pro- and anti-inflammatory cytokine induction in patients with refractory epilepsy,” Journal of Neuroimmunology, vol. 214, no. 1-2, pp. 104–108, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Nishida, Z.-L. Huang, N. Mikuni, Y. Miura, Y. Urade, and N. Hashimoto, “Deep brain stimulation of the posterior hypothalamus activates the histaminergic system to exert antiepileptic effect in rat pentylenetetrazol model,” Experimental Neurology, vol. 205, no. 1, pp. 132–144, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. C. E. Marras, M. Rizzi, F. Villani et al., “Deep brain stimulation for the treatment of drug-refractory epilepsy in a patient with a hypothalamic hamartoma: case report,” Neurosurgical Focus, vol. 30, no. 2, article E4, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Rahman, M. M. Abd-El-Barr, V. Vedam-Mai et al., “Disrupting abnormal electrical activity with deep brain stimulation: is epilepsy the next frontier?” Neurosurgical Focus, vol. 29, no. 2, p. E7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. S. J. Rizvi, M. Donovan, P. Giacobbe, F. Placenza, S. Rotzinger, and S. H. Kennedy, “Neurostimulation therapies for treatment resistant depression: a focus on vagus nerve stimulation and deep brain stimulation,” International Review of Psychiatry, vol. 23, no. 5, pp. 424–436, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. M. Lozano, J. Dostrovsky, R. Chen, and P. Ashby, “Deep brain stimulation for Parkinson's disease: disrupting the disruption,” The Lancet Neurology, vol. 1, no. 4, pp. 225–231, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Rowbottom and C. Susskind, Electricity and Medicine: History of Their Interaction, San Francisco Press, 1984.
  13. J. O. Dostrovsky and A. M. Lozano, “Mechanisms of deep brain stimulation,” Movement Disorders, vol. 17, supplement 3, pp. S63–S68, 2002. View at Google Scholar · View at Scopus
  14. J. L. Vitek, “Mechnisms of deep brain stimulation: excitation or inhibition,” Movement Disorders, vol. 17, supplement 3, pp. S69–S72, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. C. B. McCracken and A. A. Grace, “Nucleus accumbens deep brain stimulation produces region-specific alterations in local field potential oscillations and evoked responses In vivo,” Journal of Neuroscience, vol. 29, no. 16, pp. 5354–5363, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. R. L. Sjöberg and P. Blomstedt, “The psychological neuroscience of depression: implications for understanding effects of deep brain stimulation,” Scandinavian Journal of Psychology, vol. 52, no. 5, pp. 411–419, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Sesia, V. Bulthuis, S. Tan et al., “Deep brain stimulation of the nucleus accumbens shell increases impulsive behavior and tissue levels of dopamine and serotonin,” Experimental Neurology, vol. 225, no. 2, pp. 302–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. van Dijk, A. A. Klompmakers, M. G. Feenstra, and D. Denys, “Deep brain stimulation of the accumbens increases dopamine, serotonin, and noradrenaline in the prefrontal cortex,” Journal of Neurochemistry, vol. 123, no. 6, pp. 897–903, 2012. View at Publisher · View at Google Scholar
  19. V. A. Pavlov, H. Wang, C. J. Czura, S. G. Friedman, and K. J. Tracey, “The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation,” Molecular Medicine, vol. 9, no. 5–8, pp. 125–134, 2003. View at Google Scholar · View at Scopus
  20. K. J. Tracey, “The inflammatory reflex,” Nature, vol. 420, no. 6917, pp. 853–859, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. E. R. de Kloet, M. Joëls, and F. Holsboer, “Stress and the brain: from adaptation to disease,” Nature Reviews Neuroscience, vol. 6, no. 6, pp. 463–475, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. U. Andersson and K. J. Tracey, “Reflex principles of immunological homeostasis,” Annual Review of Immunology, vol. 30, pp. 313–335, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Corcoran, T. J. Connor, V. O'Keane, and M. R. Garland, “The effects of vagus nerve stimulation on pro- and anti-inflammatory cytokines in humans: a preliminary report,” NeuroImmunoModulation, vol. 12, no. 5, pp. 307–309, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Wu, W. Dong, X. Cui et al., “Ghrelin down-regulates proinflammatory cytokines in sepsis through activation of the vagus nerve,” Annals of Surgery, vol. 245, no. 3, pp. 480–486, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. A. D. Niederbichler, S. Papst, L. Claassen et al., “Burn-induced organ dysfunction: vagus nerve stimulation attenuates organ and serum cytokine levels,” Burns, vol. 35, no. 6, pp. 783–789, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. W. J. de Jonge, E. P. van der Zanden, F. O. The et al., “Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway,” Nature Immunology, vol. 6, no. 8, pp. 844–851, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. V. de Herdt, L. Puimege, J. De Waele et al., “Increased rat serum corticosterone suggests immunomodulation by stimulation of the vagal nerve,” Journal of Neuroimmunology, vol. 212, no. 1-2, pp. 102–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. R. P. A. Gaykema, I. Dijkstra, and F. J. H. Tilders, “Subdiaphragmatic vagotomy suppresses endotoxin-induced activation of hypothalamic corticotropin-releasing hormone neurons and ACTH secretion,” Endocrinology, vol. 136, no. 10, pp. 4717–4720, 1995. View at Google Scholar · View at Scopus
  29. M. Fleshner, L. E. Goehler, J. Hermann, J. K. Relton, S. F. Maier, and L. R. Watkins, “Interleukin-1β induced corticosterone elevation and hypothalamic NE depletion is vagally mediated,” Brain Research Bulletin, vol. 37, no. 6, pp. 605–610, 1995. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Fleshner, L. Silbert, T. Deak et al., “TNF-α-induced corticosterone elevation but not serum protein or corticosteroid binding globulin reduction is vagally mediated,” Brain Research Bulletin, vol. 44, no. 6, pp. 701–706, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Fleshner, L. E. Goehler, B. A. Schwartz et al., “Thermogenic and corticosterone responses to intravenous cytokines (IL-1β and TNF-α) are attenuated by subdiaphragmatic vagotomy,” Journal of Neuroimmunology, vol. 86, no. 2, pp. 134–141, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Wieczorek and A. J. Dunn, “Effect of subdiaphragmatic vagotomy on the noradrenergic and HPA axis activation induced by intraperitoneal interleukin-1 administration in rats,” Brain Research, vol. 1101, no. 1, pp. 73–84, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. H.-R. Berthoud and W. L. Neuhuber, “Functional and chemical anatomy of the afferent vagal system,” Autonomic Neuroscience, vol. 85, no. 1–3, pp. 1–17, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. E. T. Cunningham Jr. and P. E. Sawchenko, “Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus,” Journal of Comparative Neurology, vol. 274, no. 1, pp. 60–76, 1988. View at Google Scholar · View at Scopus
  35. K. Vonck, P. Boon, and D. van Roost, “Anatomical and physiological basis and mechanism of action of neurostimulation for epilepsy,” Acta Neurochirurgica, Supplementum, vol. 97, part 2, pp. 321–328, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. T. R. Henry, R. A. E. Bakay, P. B. Pennell, C. M. Epstein, and J. R. Votaw, “Brain blood-flow alterations induced by therapeutic vagus nerve stimulation in partial epilepsy: II. Prolonged effects at high and low levels of stimulation,” Epilepsia, vol. 45, no. 9, pp. 1064–1070, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Hosoi, Y. Okuma, and Y. Nomura, “Electrical stimulation of afferent vagus nerve induces IL-1β expression in the brain and activates HPA axis,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 279, no. 1, pp. R141–R147, 2000. View at Google Scholar · View at Scopus
  38. L. V. Borovikova, S. Ivanova, D. Nardi et al., “Role of vagus nerve signaling in CNI-1493-mediated suppression of acute inflammation,” Autonomic Neuroscience, vol. 85, no. 1–3, pp. 141–147, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, Calif, USA, 1998.
  40. D. Wrona and W. Trojniar, “Suppression of natural killer cell cytotoxicity following chronic electrical stimulation of the ventromedial hypothalamic nucleus in rats,” Journal of Neuroimmunology, vol. 163, no. 1-2, pp. 40–52, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Keppler and K. Decker, “Metabolites,” in Methods of Enzymatic Analysis, H. U. Bergmeyer, J. Bergmeyer, and M. Grab, Eds., vol. 6, pp. 11–118, VCH, New York, NY, USA, 1984. View at Google Scholar
  42. M. E. Hernandez, D. Martinez-Fong, M. Perez-Tapia, I. Estrada-Garcia, S. Estrada-Parra, and L. Pavón, “Evaluation of the effect of selective serotonin-reuptake inhibitors on lymphocyte subsets in patients with a major depressive disorder,” European Neuropsychopharmacology, vol. 20, no. 2, pp. 88–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Besedovsky and A. del Rey, “Brain Cytokines as integrators of the immune-neuroendocrine network,” in Handbook of Neurochemistry and Molecular Neurobiology, A. Lajtha, Ed., Springer, New York, NY, USA, 2008. View at Google Scholar
  44. R. M. Sapolsky and P. M. Plotsky, “Hypercortisolism and its possible neural bases,” Biological Psychiatry, vol. 27, no. 9, pp. 937–952, 1990. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Novakova, M. Haluzik, R. Jech, D. Urgosik, F. Ruzicka, and E. Ruzicka, “Hormonal regulators of food intake and weight gain in Parkinson's disease after subthalamic nucleus stimulation,” Neuroendocrinology Letters, vol. 32, no. 4, pp. 437–441, 2011. View at Google Scholar
  46. C. Seifried, S. Boehncke, J. Heinzmann et al., “Diurnal variation of hypothalamic function and chronic subthalamic nucleus stimulation in parkinson's disease,” Neuroendocrinology, vol. 97, no. 3, pp. 283–390, 2013. View at Google Scholar
  47. P. P. de Koning, M. Figee, E. Endert, J. G. Storosum, E. Fliers, and D. Denys, “Deep brain stimulation for obsessive-compulsive disorder is associated with cortisol changes,” Psychoneuroendocrinology, vol. 38, no. 8, pp. 1455–1459, 2013. View at Google Scholar
  48. B. Ballanger, M. Jahanshahi, E. Broussolle, and S. Thobois, “PET functional imaging of deep brain stimulation in movement disorders and psychiatry,” Journal of Cerebral Blood Flow and Metabolism, vol. 29, no. 11, pp. 1743–1754, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. E. R. Kandel, J. H. Schwartz, and T. M. Jessell, Principles of Neural Science, McGraw-Hill, New York, NY, USA, 2000.
  50. I. J. Elenkov, “Glucocorticoids and the Th1/Th2 balance,” Annals of the New York Academy of Sciences, vol. 1024, pp. 138–146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Viswanathan, B. Pilo, J. C. George, and R. J. Etches, “Effects of vagotomy on circulating levels of catecholamines and corticosterone in the pigeon,” Comparative Biochemistry and Physiology C, vol. 86, no. 1, pp. 7–9, 1987. View at Google Scholar · View at Scopus
  52. A. J. Bugajski, D. Zurowski, P. Thor, and A. Ģdek-Michalska, “Effect of subdiaphragmatic vagotomy and cholinergic agents in the hypothalamic-pituitary-adrenal axis activity,” Journal of Physiology and Pharmacology, vol. 58, no. 2, pp. 335–347, 2007. View at Google Scholar · View at Scopus
  53. K. V. Thrivikraman, F. Zejnelovic, R. W. Bonsall, and M. J. Owens, “Neuroendocrine homeostasis after vagus nerve stimulation in rats,” Psychoneuroendocrinology, vol. 38, no. 7, pp. 1067–1077, 2013. View at Publisher · View at Google Scholar
  54. A. Carbia-Nagashima and E. Arzt, “Intracellular Proteins and Mechanisms Involved in the Control of gp130/JAK/STAT Cytokine Signaling,” IUBMB Life, vol. 56, no. 2, pp. 83–88, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. R. Schindler, J. Mancilla, S. Endres, R. Ghorbani, S. C. Clark, and C. A. Dinarello, “Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononuclear cells: IL-6 suppresses IL-1 and TNF,” Blood, vol. 75, no. 1, pp. 40–47, 1990. View at Google Scholar · View at Scopus
  56. K. Gil, A. Bugajski, M. Kurnik, and P. Thor, “Electrical chronic vagus nerve stimulation activates the hypothalamic-pituitary-adrenal axis in rats fed high-fat diet,” Neuroendocrinology Letters, vol. 34, no. 4, pp. 314–321, 2013. View at Google Scholar
  57. F. Wasinski, R. F. Bacurau, M. R. Moraes et al., “Exercise and caloric restriction alter the immune system of mice submitted to a high-fat diet,” Mediators of Inflammation, vol. 2013, Article ID 395672, 8 pages, 2013. View at Publisher · View at Google Scholar
  58. K. Ebner, P. Muigg, and N. Singewald, “Inhibitory function of the dorsomedial hypothalamic nucleus on the hypothalamic-pituary-adrenal axis response to an emotional stressor but not immune challenge,” Journal of Neuroendocrinology, vol. 25, no. 1, pp. 48–55, 2013. View at Publisher · View at Google Scholar