Table of Contents
Cardiovascular Psychiatry and Neurology
Volume 2010, Article ID 506952, 16 pages
http://dx.doi.org/10.1155/2010/506952
Research Article

Forebrain Ischemia Triggers GABAergic System Degeneration in Substantia Nigra at Chronic Stages in Rats

Department of Neurology (D4-5), Cerebral Vascular Disease Research Center, University of Miami Miller School of Medicine, P.O. Box 016960, Miami, FL 33101, USA

Received 20 January 2010; Revised 10 June 2010; Accepted 11 August 2010

Academic Editor: Héctor J. Caruncho

Copyright © 2010 B. Lin 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. K. M. Barrett, W. D. Freeman, S. M. Weindling et al., “Brain injury after cardiopulmonary arrest and its assessment with diffusion-weighted magnetic resonance imaging,” Mayo Clinic Proceedings, vol. 82, no. 7, pp. 828–835, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Fujioka, K. Okuchi, T. Sakaki, K.-I. Hiramatsu, S. Miyamoto, and S. Iwasaki, “Specific changes in human brain following reperfusion after cardiac arrest,” Stroke, vol. 25, no. 10, pp. 2091–2095, 1994. View at Google Scholar · View at Scopus
  3. P. Vaagenes, M. Ginsberg, U. Ebmeyer et al., “Cerebral resuscitation from cardiac arrest: pathophysiologic mechanisms,” Critical Care Medicine, vol. 24, supplement 2, pp. S57–S68, 1996. View at Google Scholar · View at Scopus
  4. C. Madl and M. Holzer, “Brain function after resuscitation from cardiac arrest,” Current Opinion in Critical Care, vol. 10, no. 3, pp. 213–217, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. A. J. Furlan, C. A. Sila, M. I. Chimowitz, and S. C. Jones, “Neurologic complications related to cardiac surgery,” Neurologic Clinics, vol. 10, no. 1, pp. 145–166, 1992. View at Google Scholar · View at Scopus
  6. M. J. G. Harrison, “Neurologic complications of coronary artery bypass grafting: diffuse or focal ischemia?” Annals of Thoracic Surgery, vol. 59, no. 5, pp. 1356–1358, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. M. D. Ginsberg, “Carbon monoxide intoxication: clinical features, neuropathology and mechanisms of injury,” Clinical Toxicology, vol. 23, pp. 281–288, 1985. View at Google Scholar
  8. R. A. C. Roos, “Neurological complications of carbon monoxide intoxication,” in Handbook of Clinical Neurology, P. J. Vinken and G. W. Bruyn, Eds., vol. 64, pp. 31–35, Elsevier, Amsterdam, The Netherlands, 1994. View at Google Scholar
  9. K. Konaka, K. Miyashita, and H. Naritomi, “Changes in diffusion-weighted magnetic resonance imaging findings in the acute and subacute phases of anoxic encephalopathy,” Journal of Stroke and Cerebrovascular Diseases, vol. 16, no. 2, pp. 82–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Epsztein, M. Milh, R. I. Bihi et al., “Ongoing epileptiform activity in the post-ischemic hippocampus is associated with a permanent shift of the excitatory-inhibitory synaptic balance in CA3 pyramidal neurons,” Journal of Neuroscience, vol. 26, no. 26, pp. 7082–7092, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. J.-J. Soghomonian and N. Laprade, “Glutamate decarboxylase (GAD67 and GAD65) gene expression is increased in a subpopulation of neurons in the putamen of Parkinsonian monkeys,” Synapse, vol. 27, no. 2, pp. 122–132, 1997. View at Google Scholar · View at Scopus
  12. S. F. Kash, R. S. Johnson, L. H. Tecott et al., “Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 25, pp. 14060–14065, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Mendez, K. Elisevich, and B. A. Flumerfelt, “GABAergic synaptic interactions in the substantia nigra,” Brain Research, vol. 617, no. 2, pp. 274–284, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Lin, M. D. Ginsberg, R. Busto, and W. D. Dietrich, “Sequential analysis of subacute and chronic neuronal, astrocytic and microglial alterations after transient global ischemia in rats,” Acta Neuropathologica, vol. 95, no. 5, pp. 511–523, 1998. View at Google Scholar · View at Scopus
  15. B. Lin, M. Y.-T. Globus, W. D. Dietrich, R. Busto, E. Martinez, and M. D. Ginsberg, “Differing neurochemical and morphological sequelae of global ischemia: comparison of single- and multiple-insult paradigms,” Journal of Neurochemistry, vol. 59, no. 6, pp. 2213–2223, 1992. View at Google Scholar · View at Scopus
  16. J. W. Phillis and M. H. O'Regan, “Characterization of modes of release of amino acids in the ischemic/reperfused rat cerebral cortex,” Neurochemistry International, vol. 43, no. 4-5, pp. 461–467, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Gonzales, R. C.-S. Lin, and M.-F. Chesselet, “Relative sparing of GABAergic interneurons in the striatum of gerbils with ischemia-induced lesions,” Neuroscience Letters, vol. 135, no. 1, pp. 53–58, 1992. View at Publisher · View at Google Scholar · View at Scopus
  18. M. G. Erlander, N. J. K. Tillakaratne, S. Feldblum, N. Patel, and A. J. Tobin, “Two genes encode distinct glutamate decarboxylases,” Neuron, vol. 7, no. 1, pp. 91–100, 1991. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Lin, “Postischemic-anoxic encephalopathy after global forebrain ischemia,” Central Nervous System Agents in Medicinal Chemistry, vol. 8, no. 3, pp. 177–186, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. J.-Y. Wu, L. A. Denner, and S. C. Wei, “Production and characterization of polyclonal and monoclonal antibodies to rat brain l-glutamate decarboxylase,” Brain Research, vol. 373, no. 1-2, pp. 1–14, 1986. View at Google Scholar · View at Scopus
  21. G. J. Müller, A.-M. Dogonowski, B. Finsen, and F. F. Johansen, “Expression of glutamic acid decarboxylase and identification of GABAergic cells in the ischemic rat dentate gyrus,” Experimental Brain Research, vol. 175, no. 3, pp. 556–566, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Gerstein, M. Huleihel, R. Mane et al., “Remodeling of hippocampal GABAergic system in adult offspring after maternal hypoxia and magnesium sulfate load: immunohistochemical study,” Experimental Neurology, vol. 196, no. 1, pp. 18–29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Hayashi, S. Kumada, K. Shioda, and R. Fukatsu, “Neuropathological analysis of the brainstem and cerebral cortex lesions on epileptogenesis in hereditary dentatorubral-pallidoluysian atrophy,” Brain and Development, vol. 29, no. 8, pp. 473–481, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. R. J. Mullen, C. R. Buck, and A. M. Smith, “NeuN, a neuronal specific nuclear protein in vertebrates,” Development, vol. 116, no. 1, pp. 201–211, 1992. View at Google Scholar · View at Scopus
  25. K. Tsuboi, T. A. Kimber, and C. W. Shults, “Calretinin-containing axons and neurons are resistant to an intrastriatal 6-hydroxydopamine lesion,” Brain Research, vol. 866, no. 1-2, pp. 55–64, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Yamada, S. Goto, M. Yoshikawa, and Y. Ushio, “GABAergic transmission and tyrosine hydroxylase expression in the nigral dopaminergic neurons: an in vivo study using a reversible ischemia model of rats,” Neuroscience, vol. 73, no. 3, pp. 783–789, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. G. L. Clifton, J. Y. Jiang, B. G. Lyeth, L. W. Jenkins, R. J. Hamm, and R. L. Hayes, “Marked protection by moderate hypothermia after experimental traumatic brain injury,” Journal of Cerebral Blood Flow and Metabolism, vol. 11, no. 1, pp. 114–121, 1991. View at Google Scholar · View at Scopus
  28. A.-L. Ohlsson, B. B. Johansson, and S. C. Jones, “Environment influences functional outcome of cerebral infarction in rats,” Stroke, vol. 26, no. 4, pp. 644–649, 1995. View at Google Scholar · View at Scopus
  29. C. Frahm, G. Siegel, S. Grass, and O. W. Witte, “Stable expression of the vesicular GABA transporter following photothrombotic infarct in rat brain,” Neuroscience, vol. 140, no. 3, pp. 865–877, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Alfahel-Kakunda and W. F. Silverman, “Calcium-binding proteins in the substantia nigra and ventral tegmental area during development: correlation with dopaminergic compartmentalization,” Developmental Brain Research, vol. 103, no. 1, pp. 9–20, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Shuaib, S. Ijaz, J. Kalra, and W. Code, “Repetitive transient forebrain ischemia in gerbils: delayed neuronal damage in the substantia nigra reticulata,” Brain Research, vol. 574, no. 1-2, pp. 120–124, 1992. View at Google Scholar · View at Scopus
  32. M. Saji and B. T. Volpe, “Delayed histologic damage and neuron death in the substantia nigra reticulata following transient forebrain ischemia depends on the extent of initial striatal injury,” Neuroscience Letters, vol. 155, no. 1, pp. 47–50, 1993. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Siucinska, “GAD67-positive puncta: Contributors to learning-dependent plasticity in the barrel cortex of adult mice,” Brain Research, vol. 1106, no. 1, pp. 52–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. M. L. Tappaz, M. Wassef, and W. H. Oertel, “Light- and electron-microscopic immunocytochemistry of glutamic acid decarboxylase (GAD) in the basal hypothalamus: morphological evidence for neuroendocrine γ-aminobutyrate (GABA),” Neuroscience, vol. 9, no. 2, pp. 271–287, 1983. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Frotscher, B. Heimrich, and H. Schwegler, “Plasticity of identified neurons in slice cultures of hippocampus: a combined Golgi/electron microscopic and immunocytochemical study,” Progress in Brain Research, vol. 83, pp. 323–339, 1990. View at Google Scholar · View at Scopus
  36. T. F. Freund, K. A. C. Martin, A. D. Smith, and P. Somogyi, “Glutamate decarboxylase-immunoreactive terminals of Golgi-impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex,” Journal of Comparative Neurology, vol. 221, no. 3, pp. 263–278, 1983. View at Google Scholar · View at Scopus
  37. M. Frotscher and J. Zimmer, “GABAergic nonpyramidal neurons in intracerebral transplants of the rat hippocampus and fascia dentata: a combined light and electron microscopic immunocytochemical study,” Journal of Comparative Neurology, vol. 259, no. 2, pp. 266–276, 1987. View at Google Scholar · View at Scopus
  38. S. A. Jenkins and D. D. Simmons, “GABAergic neurons in the lateral superior olive of the hamster are distinguished by differential expression of gad isoforms during development,” Brain Research, vol. 1111, no. 1, pp. 12–25, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. L. E. Eiden, “The vesicular neurotransmitter transporters: current perspectives and future prospects,” FASEB Journal, vol. 14, no. 15, pp. 2396–2400, 2000. View at Google Scholar · View at Scopus
  40. R. Vemuganti, “Decreased expression of vesicular GABA transporter, but not vesicular glutamate, acetylcholine and monoamine transporters in rat brain following focal ischemia,” Neurochemistry International, vol. 47, no. 1-2, pp. 136–142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Jin, H. Wu, G. Osterhaus et al., “Demonstration of functional coupling between γ-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 4293–4298, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. B. I. Kanner, “Sodium-coupled GABA and glutamate transporters,” in Neurotransmitter Transporters: Structure, Function and Regulation, M. E. A. Reith, Ed., pp. 151–169, Human Press, Totowa, NJ, USA, 1997. View at Google Scholar
  43. A. Shuaib, S. Ijaz, H. Miyashita, T. Mainprize, and R. Kanthan, “Progressive decrease in extracellular GABA concentrations in the post-ischemic period in the striatum: a microdialysis study,” Brain Research, vol. 666, no. 1, pp. 99–103, 1994. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Nemoto, T. Hida, and R. Arai, “Calretinin and calbindin-D28k in dopaminergic neurons of the rat midbrain: a triple-labeling immunohistochemical study,” Brain Research, vol. 846, no. 1, pp. 129–136, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. B. G. Kim, D. H. Shin, G. S. Jeon et al., “Relative sparing of calretinin containing neurons in the substantia nigra of 6-OHDA treated rat Parkinsonian model,” Brain Research, vol. 855, no. 1, pp. 162–165, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. W. R. G. Gibb, “Neuropathology of Parkinson's disease and related syndromes,” Neurologic Clinics, vol. 10, no. 2, pp. 361–376, 1992. View at Google Scholar · View at Scopus
  47. J. P. Bolam and Y. Smith, “The GABA and substance P input to dopaminergic neurones in the substantia nigra of the rat,” Brain Research, vol. 529, no. 1-2, pp. 57–78, 1990. View at Google Scholar · View at Scopus
  48. M. S. Reid, M. Herrera-Marschitz, T. Hokfelt, N. Lindefors, H. Persson, and U. Ungerstedt, “Striatonigral GABA, dynorphin, substance P and neurokinin A modulation of nigrostriatal dopamine release: evidence for direct regulatory mechanisms,” Experimental Brain Research, vol. 82, no. 2, pp. 293–303, 1990. View at Google Scholar · View at Scopus
  49. J. M. Tepper and C. R. Lee, “GABAergic control of substantia nigra dopaminergic neurons,” in Progress in Brain Research, J. M. Tepper, E. D. Abercrombie, and J. P. Bolam, Eds., vol. 160, chapter 11, pp. 189–208, 2007. View at Google Scholar
  50. C. R. Gerfen, J. F. McGinty, and W. S. Young III, “Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis,” Journal of Neuroscience, vol. 11, no. 4, pp. 1016–1031, 1991. View at Google Scholar · View at Scopus
  51. W. Hauber, “Involvement of basal ganglia transmitter systems in movement initiation,” Progress in Neurobiology, vol. 56, no. 5, pp. 507–540, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Wichmann, M. A. Kliem, and M. R. DeLong, “Antiparkinsonian and behavioral effects of inactivation of the substantia nigra pars reticulata in hemiparkinsonian primates,” Experimental Neurology, vol. 167, no. 2, pp. 410–424, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Nakane, A. Teraoka, R. Asato, and A. Tamura, “Degeneration of the ipsilateral substantia nigra following cerebral infarction in the striatum,” Stroke, vol. 23, no. 3, pp. 328–332, 1992. View at Google Scholar · View at Scopus
  54. T. Ogawa, T. Okudera, A. Inugami et al., “Degeneration of the ipsilateral substantia nigra after striatal infarction: evaluation with MR imaging,” Radiology, vol. 204, no. 3, pp. 847–851, 1997. View at Google Scholar · View at Scopus
  55. F. M. Benes, B. Lim, D. Matzilevich, J. P. Walsh, S. Subburaju, and M. Minns, “Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 24, pp. 10164–10169, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. K. Hawker and A. E. Lang, “Hypoxic-ischemic damage of the basal ganglia: case reports and a review of the literature,” Movement Disorders, vol. 5, no. 3, pp. 219–224, 1990. View at Google Scholar · View at Scopus
  57. A. P. Fève, G. Fenelon, C. Wallays, P. Remy, and A. Guillard, “Axial motor disturbances after hypoxic lesions of the globus pallidus,” Movement Disorders, vol. 8, no. 3, pp. 321–326, 1993. View at Google Scholar · View at Scopus
  58. C. Lim, M. P. Alexander, G. LaFleche, D. M. Schnyer, and M. Verfaellie, “The neurological and cognitive sequelae of cardiac arrest,” Neurology, vol. 63, no. 10, pp. 1774–1778, 2004. View at Google Scholar · View at Scopus
  59. S. Khot and D. L. Tirschwell, “Long-term neurological complications after hypoxic-ischemic encephalopathy,” Seminars in Neurology, vol. 26, no. 4, pp. 422–431, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Lu-Emerson and S. Khot, “Neurological sequelae of hypoxic-ischemic brain injury,” NeuroRehabilitation, vol. 26, no. 1, pp. 35–45, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. I. S. Choi, “Parkinsonism after carbon monoxide poisoning,” European Neurology, vol. 48, no. 1, pp. 30–33, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. I. S. Choi, “Carbon monoxide poisoning: systemic manifestations and complications,” Journal of Korean Medical Science, vol. 16, no. 3, pp. 253–261, 2001. View at Google Scholar · View at Scopus
  63. F. Yoshii, R. Kozuma, W. Takahashi, M. Haida, S. Takagi, and Y. Shinohara, “Magnetic resonance imaging and 11C-N-methylspiperone/positron emission tomography studies in a patient with the interval form of carbon monoxide poisoning,” Journal of the Neurological Sciences, vol. 160, no. 1, pp. 87–91, 1998. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. H. Sohn, Y. Jeong, H. S. Kim, J. H. Im, and J.-S. Kim, “The brain lesion responsible for parkinsonism after carbon monoxide poisoning,” Archives of Neurology, vol. 57, no. 8, pp. 1214–1218, 2000. View at Google Scholar · View at Scopus
  65. O. Y. Kwon, S. P. Chung, Y. R. Ha, I. S. Yoo, and S. W. Kim, “Delayed postanoxic encephalopathy after carbon monoxide poisoning,” Emergency Medicine Journal, vol. 21, no. 2, pp. 250–251, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. L. D. Prockop and R. I. Chichkova, “Carbon monoxide intoxication: an updated review,” Journal of the Neurological Sciences, vol. 262, no. 1-2, pp. 122–130, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Rissanen, T. Paavilainen, J. Virta, R. J. Marttila, J. O. Rinne, and L. Airas, “Carbon monoxide poisoning-induced migrostriatal dopaminergic dysfunction detected using positron emission tomography (PET),” NeuroToxicology, vol. 31, pp. 403–407, 2010. View at Google Scholar · View at Scopus
  68. M. H. Bhatt, J. A. Obeso, and C. D. Marsden, “Time course of postanoxic akinetic-rigid and dystonic syndromes,” Neurology, vol. 43, no. 2, pp. 314–317, 1993. View at Google Scholar · View at Scopus
  69. K. B. Boylan, J. H. Chin, and S. J. DeArmond, “Progressive dystonia following resuscitation from cardiac arrest,” Neurology, vol. 40, no. 9, pp. 1458–1461, 1990. View at Google Scholar · View at Scopus
  70. T. Kinoshita, S. Sugihara, E. Matsusue, S. Fujii, M. Ametani, and T. Ogawa, “Pallidoreticular damage in acute carbon monoxide poisoning: diffusion-weighted MR imaging findings,” American Journal of Neuroradiology, vol. 26, no. 7, pp. 1845–1848, 2005. View at Google Scholar · View at Scopus
  71. T. Kawanami, T. Kato, K. Kurita, and H. Sasaki, “The pallidoreticular pattern of brain damage on MRI in a patient with carbon monoxide poisoning,” Journal of Neurology Neurosurgery and Psychiatry, vol. 64, no. 2, p. 282, 1998. View at Google Scholar · View at Scopus
  72. K. P. Bhatia and C. D. Marsden, “The behavioural and motor consequences of focal lesions of the basal ganglia in man,” Brain, vol. 117, no. 4, pp. 859–876, 1994. View at Google Scholar · View at Scopus
  73. S. F. Bucher, K. C. Seelos, R. C. Dodel, W. Paulus, M. Reiser, and W. H. Oertel, “Pallidal lesions: structural and functional magnetic resonance imaging,” Archives of Neurology, vol. 53, no. 7, pp. 682–686, 1996. View at Google Scholar · View at Scopus