Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
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Striatal Glutamate and GABA after High Frequency Subthalamic Stimulation in Parkinsonian Rat

  • Lee, Kyung Jin (Department of Neurosurgery, Yeoido Saint Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Shim, Insop (Acupuncture & Meridian Science Research Center, College of Oriental Medicine, Kyung Hee University) ;
  • Sung, Jae Hoon (Department of Neurosurgery, St. Vincent's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Hong, Jae Taek (Department of Neurosurgery, St. Vincent's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Kim, Il sup (Department of Neurosurgery, St. Vincent's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Cho, Chul Bum (Department of Neurosurgery, St. Vincent's Hospital, College of Medicine, The Catholic University of Korea)
  • Received : 2016.02.25
  • Accepted : 2016.09.12
  • Published : 2017.03.01
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Abstract

Objective : High frequency stimulation (HFS) of the subthalamic nucleus (STN) is recognized as an effective treatment of advanced Parkinson's disease. However, the neurochemical basis of its effects remains unknown. The aim of this study is to investigate the effects of STN HFS in intact and 6-hydroxydopamine (6-OHDA)-lesioned hemiparkinsonian rat model on changes of principal neurotransmitters, glutamate, and gamma-aminobutyric acid (GABA) in the striatum. Methods : The authors examined extracellular glutamate and GABA change in the striatum on sham group, 6-OHDA group, and 6-OHDA plus deep brain stimulation (DBS) group using microdialysis methods. Results : High-pressure liquid chromatography was used to quantify glutamate and GABA. The results show that HFS-STN induces a significant increase of extracellular glutamate and GABA in the striatum of 6-OHDA plus DBS group compared with sham and 6-OHDA group. Conclusion : Therefore, the clinical results of STN-HFS are not restricted to the direct STN targets but involve widespread adaptive changes within the basal ganglia.

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References

  1. Abosch A, Kapur S, Lang A, Hussey D, Sime E, Miyasaki J, et al. : Stimulation of the subthalamic nucleus in Parkinson's disease does not produce striatal dopamine release. Neurosurgery 53 : 1095-1102, 2003 https://doi.org/10.1227/01.NEU.0000088662.69419.1B
  2. Bar Gad I, Elias S, Vaadia E, Bergman H : Complex locking rather than complete cessation of neuronal activity in the globus pallidus of a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primate in response to pallidal microstimulation. J Neurosci 24 : 7410-7419, 2004 https://doi.org/10.1523/JNEUROSCI.1691-04.2004
  3. Bruet N, Windels F, Carcenac C, Feuerstein C, Bertrand A, Poupard A, et al. : Neurochemical mechanisms induced by high frequency stimulation of the subthalamic nucleus : increase of extracellular striatal glutamate and GABA in normal and hemiparkinsonian rats. J Neuropathol Exp Neurol 62 : 1228-1240, 2003 https://doi.org/10.1093/jnen/62.12.1228
  4. Carman LS, Gage FH, Shults CW : Partial lesion of the substantia nigra : relation between extent of lesion and rotational behavior. Brain Res 553 : 275-283, 1991 https://doi.org/10.1016/0006-8993(91)90835-J
  5. Chevalier G, Deniau JM : Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci 13 : 277-280, 1990 https://doi.org/10.1016/0166-2236(90)90109-N
  6. DeLong MR : Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13 : 281-285, 1990 https://doi.org/10.1016/0166-2236(90)90110-V
  7. Deumens R, Blokland A, Prickaerts J : Modeling Parkinson's disease in rats : an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol 175 : 303-317, 2002 https://doi.org/10.1006/exnr.2002.7891
  8. Henning J, Koczan D, Glass A, Karopka T, Pahnke J, Rolfs A, et al. : Deep brain stimulation in a rat model modulates TH, CaMKIIa and Homer1 gene expression. Eur J Neurosci 25 : 239-250, 2007 https://doi.org/10.1111/j.1460-9568.2006.05264.x
  9. Hodaie M, Wennberg R, Dostrovsky J, Lozano A : Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 43 : 603-608, 2002 https://doi.org/10.1046/j.1528-1157.2002.26001.x
  10. Krack P, Batir A, Van Blercom Ng, Chabardes S, Fraix Vr, Ardouin C, et al. : Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349 : 1925-1934, 2003 https://doi.org/10.1056/NEJMoa035275
  11. Krack P, Pollak P, Limousin P, Benazzouz A, Benabid AL : Stimulation of subthalamic nucleus alleviates tremor in Parkinson's disease. Lancet 350 : 1675, 1997 https://doi.org/10.1016/S0140-6736(97)24049-3
  12. Lacombe E, Carcenac C, Boulet S, Feuerstein C, Bertrand A, Poupard A, et al. : High-frequency stimulation of the subthalamic nucleus prolongs the increase in striatal dopamine induced by acute l-3,4-dihydroxyphenylalanine in dopaminergic denervated rats. Eur J Neurosci 26 : 1670-1680, 2007 https://doi.org/10.1111/j.1460-9568.2007.05747.x
  13. Lang AE, Widner H : Deep brain stimulation for Parkinson's disease : patient selection and evaluation. Mov Disord 17 Suppl 3 : S94-S101, 2002 https://doi.org/10.1002/mds.10149
  14. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Broussolle E, Perret JE, et al. : Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov Disord 10 : 672-674, 1995 https://doi.org/10.1002/mds.870100523
  15. McIntyre CC, Savasta M, Kerkerian-Le Goff L, Vitek JL : Uncovering the mechanism(s) of action of deep brain stimulation : activation, inhibition, or both. Clin Neurophysiol 115 : 1239-1248, 2004 https://doi.org/10.1016/j.clinph.2003.12.024
  16. Megias M, Emri Z, Freund TF, Gulyas AI : Total number and distribu-tion of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102 : 527-540, 2001 https://doi.org/10.1016/S0306-4522(00)00496-6
  17. Meissner W, Harnack D, Reese R, Paul G, Reum T, Ansorge M, et al. : High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J Neurochem 85 : 601-609, 2003 https://doi.org/10.1046/j.1471-4159.2003.01665.x
  18. Nambu A : A new approach to understand the pathophysiology of Parkinson's disease. J Neurol 252 Suppl 4 : IV1-IV4, 2005
  19. Papa SM, Engber TM, Kask AM, Chase TN : Motor fluctuations in levodopa treated parkinsonian rats : relation to lesion extent and treatment duration. Brain Res 662 : 69-74, 1994 https://doi.org/10.1016/0006-8993(94)90796-X
  20. Paxinos G : The rat nervous system. Amsterdam ; Boston : Elsevier Academic Press, 2004
  21. Pollak P, Benabid AL, Gross C, Gao DM, Laurent A, Benazzouz A, et al. : Effects of the stimulation of the subthalamic nucleus in Parkinson disease. Rev Neurol (Paris) 149 : 175-176, 1993
  22. Segovia G, Del Arco A, Mora F : Endogenous glutamate increases extracellular concentrations of dopamine, GABA, and taurine through NMDA and AMPA/kainate receptors in striatum of the freely moving rat : a microdialysis study. J Neurochem 69 : 1476-1483, 1997 https://doi.org/10.1046/j.1471-4159.1997.69041476.x
  23. Shipton EA : Movement disorders and neuromodulation. Neurol Res Int 2012 : 309431, 2012
  24. Visser-Vandewalle V, van der Linden C, Temel Y, Celik H, Ackermans L, Spincemaille G, et al. : Long-term effects of bilateral subthalamic nucleus stimulation in advanced Parkinson disease : a four year follow-up study. Parkinsonism Relat Disord 11 : 157-165, 2005 https://doi.org/10.1016/j.parkreldis.2004.10.011
  25. Wichmann T, Delong MR : Deep-brain stimulation for basal ganglia disorders. Basal Ganglia 1 : 65-77, 2011 https://doi.org/10.1016/j.baga.2011.05.001
  26. Wichmann T, DeLong MR, Guridi J, Obeso JA : Milestones in research on the pathophysiology of Parkinson's disease. Mov Disord 26 : 1032-1041, 2011 https://doi.org/10.1002/mds.23695
  27. Zhao C, Deng W, Gage FH : Mechanisms and functional implications of adult neurogenesis. Cell 132 : 645-660, 2008 https://doi.org/10.1016/j.cell.2008.01.033

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