About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 527201, 12 pages
http://dx.doi.org/10.1155/2011/527201
Review Article

A Novel Animal Model of Hippocampal Cognitive Deficits, Slow Neurodegeneration, and Neuroregeneration

1Department of Psychology, University of Calgary, 2500 University Drive NW, Calgary, AB, Canada T2N 1N4
2Department of Psychology, Trent University, 1600 West Bank Drive, Peterborough, ON, Canada K9J 7B8
3Department of Neuroscience, University of Lethbridge, 4401 University Drive, Lethbridge, AB, Canada T1K 3M4

Received 16 September 2010; Accepted 19 January 2011

Academic Editor: Oreste Gualillo

Copyright © 2011 Simon C. Spanswick 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. J. Götz and L. M. Ittner, “Animal models of Alzheimer's disease and frontotemporal dementia,” Nature Reviews Neuroscience, vol. 9, no. 7, pp. 532–544, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. M. E. Smith, “Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies,” Hippocampus, vol. 15, no. 6, pp. 798–807, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Brück, T. Kurki, V. Kaasinen, T. Vahlberg, and J. O. Rinne, “Hippocampal and prefrontal atrophy in patients with early non-demented Parkinson's disease is related to cognitive impairment,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 75, no. 10, pp. 1467–1469, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. W. H. Theodore, S. Bhatia, J. Hatta et al., “Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures,” Neurology, vol. 52, no. 1, pp. 132–136, 1999. View at Scopus
  5. A. C. DeVries, R. J. Nelson, R. J. Traystman, and P. D. Hurn, “Cognitive and behavioral assessment in experimental stroke research: will it prove useful?” Neuroscience and Biobehavioral Reviews, vol. 25, no. 4, pp. 325–342, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. O. Lindvall and P. Hagell, “Role of cell therapy in Parkinson disease,” Neurosurgical Focus, vol. 13, no. 5, p. e2, 2002. View at Scopus
  7. O. Lindvall and Z. Kokaia, “Prospects of stem cell therapy for replacing dopamine neurons in Parkinson's disease,” Trends in Pharmacological Sciences, vol. 30, no. 5, pp. 260–267, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Jeltsch, J. Yee, E. Aloy, et al., “Transplantation of neurospheres after granule cell lesions in rats: cognitive improvements despite no long-term immunodetection of grafted cells,” Behavioural Brain Research, vol. 143, no. 2, pp. 177–191, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. A. K. Shetty and D. A. Turner, “Development of fetal hippocampal grafts in intact and lesioned hippocampus,” Progress in Neurobiology, vol. 50, no. 5-6, pp. 597–653, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. D. A. Turner, A. K. Shetty, B. Jacobs et al., “Clinical prospects for neural grafting therapy for hippocampal lesions and epilepsy,” Neurosurgery, vol. 52, no. 3, pp. 632–644, 2003. View at Scopus
  11. B. Will, C. Kelche, and J. C. Cassel, “Intracerebral transplants and memory dysfunction: circuitry repair or functional level setting?” Neural Plasticity, vol. 7, no. 1-2, pp. 93–108, 2000. View at Scopus
  12. A. K. Shetty and B. Hattiangady, “Restoration of calbindin after fetal hippocampal CA3 cell grafting into the injured hippocampus in a rat model of temporal lobe epilepsy,” Hippocampus, vol. 17, no. 10, pp. 943–956, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Rüschenschmidt, P. G. Koch, O. Brüstle, and H. Beck, “Functional properties of ES cell-derived neurons engrafted into the hippocampus of adult normal and chronically epileptic rats,” Epilepsia, vol. 46, no. 5, pp. 174–183, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. P. S. Eriksson, E. Perfilieva, T. Björk-Eriksson et al., “Neurogenesis in the adult human hippocampus,” Nature Medicine, vol. 4, no. 11, pp. 1313–1317, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. R. S. Sloviter, G. Valiquette, G. M. Abrams et al., “Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy,” Science, vol. 243, no. 4890, pp. 535–538, 1989. View at Scopus
  16. R. S. Sloviter, E. Dean, and S. Neubort, “Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system,” Journal of Comparative Neurology, vol. 330, no. 3, pp. 337–351, 1993. View at Scopus
  17. E. Gould, C. S. Woolley, and B. S. McEwen, “Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus,” Neuroscience, vol. 37, no. 2, pp. 367–375, 1990. View at Publisher · View at Google Scholar · View at Scopus
  18. C. S. Woolley, E. Gould, R. R. Sakai, R. L. Spencer, and B. S. McEwen, “Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat,” Brain Research, vol. 554, no. 1-2, pp. 312–315, 1991. View at Scopus
  19. D. Jaarsma, F. Postema, and J. Korf, “Time course and distribution of neuronal degeneration in the dentate gyrus of rat after adrenalectomy: a silver impregnation study,” Hippocampus, vol. 2, no. 2, pp. 143–150, 1992. View at Scopus
  20. C. Park, M. Kang, Y. Kim-Kwon, J. Kim, H. Ahn, and Y. Huh, “Inhibition of neuronal nitric oxide synthase increases adrenalectomy-induced granule cell death in the rat dentate gyrus,” Brain Research, vol. 933, no. 1, pp. 81–84, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Andrés, S. Cárdenas, C. Parra et al., “Effects of long-term adrenalectomy on apoptosis and neuroprotection in the rat hippocampus,” Endocrine, vol. 29, no. 2, pp. 299–307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Greiner, S. Cárdenas, C. Parra et al., “Adrenalectomy regulates apoptotic-associated genes in rat hippocampus,” Endocrine, vol. 15, no. 3, pp. 323–333, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. L. C. Schmued and K. J. Hopkins, “Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration,” Brain Research, vol. 874, no. 2, pp. 123–130, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Walker, D. Chan, and M. Thom, “Hippocampus and human disease,” in The Hippocampus Book, P. Anderson, R. Morris, D. Amaral, T. Bliss, and J. O'Keefe, Eds., pp. 769–812, Oxford University Press, New York, NY, USA, 2007.
  25. C. K. Petito, E. Feldmann, W. A. Pulsinelli, and F. Plum, “Delayed hippocampal damage in humans following cardiorespiratory arrest,” Neurology, vol. 37, no. 8, pp. 1281–1286, 1987. View at Scopus
  26. R. R. Hicks, D. H. Smith, D. H. Lowenstein, R. Saint Marie, and T. K. McIntosh, “Mild experimental brain injury in the rat induces cognitive deficits associated with regional neuronal loss in the hippocampus,” Journal of Neurotrauma, vol. 10, no. 4, pp. 405–414, 1993. View at Scopus
  27. P. Kumar, H. Kalonia, and A. Kumar, “Huntington's disease: pathogenesis to animal models,” Pharmacological Reports, vol. 62, no. 1, pp. 1–14, 2010. View at Scopus
  28. A. J. Lees, J. Hardy, and T. Revesz, “Parkinson's disease,” The Lancet, vol. 373, no. 9680, pp. 2055–2066, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. S. C. Spanswick and R. J. Sutherland, “Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats,” Learning & Memory, vol. 17, no. 5, pp. 241–245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. J. West, G. Danscher, and H. Gydesen, “A determination of the volumes of the layers of the rat hippocampal region,” Cell and Tissue Research, vol. 188, no. 3, pp. 345–359, 1978. View at Scopus
  31. M. J. West, L. Slomianka, and H. J. G. Gundersen, “Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator,” Anatomical Record, vol. 231, no. 4, pp. 482–497, 1991. View at Scopus
  32. P. R. Mouton, Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists, The Johns Hopkins University Press, Baltimore, Md, USA, 2002.
  33. C. Schmitz and P. R. Hof, “Design-based stereology in neuroscience,” Neuroscience, vol. 130, no. 4, pp. 813–831, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. J. N. Armstrong, D. C. McIntyre, S. Neubort, and R. S. Sloviter, “Learning and memory after adrenalectomy-induced hippocampal dentate granule cell degeneration in the rat,” Hippocampus, vol. 3, no. 3, pp. 359–371, 1993. View at Scopus
  35. B. Roozendaal, R. M. Sapolsky, and J. L. McGaugh, “Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory,” Neuroscience, vol. 84, no. 2, pp. 453–465, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. S. C. Spanswick, J. R. Epp, J. R. Keith, and R. J. Sutherland, “Adrenalectomy-induced granule cell degeneration in the hippocampus causes spatial memory deficits that are not reversed by chronic treatment with corticosterone or fluoxetine,” Hippocampus, vol. 17, no. 2, pp. 137–146, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. C. M. Stienstra, F. van der Graaf, A. Bosma, Y. J. G. Karten, W. Hesen, and M. Joëls, “Synaptic transmission in the rat dentate gyrus after adrenalectomy,” Neuroscience, vol. 85, no. 4, pp. 1061–1071, 1998. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Wossink, H. Karst, O. Mayboroda, and M. Joëls, “Morphological and functional properties of rat dentate granule cells after adrenalectomy,” Neuroscience, vol. 108, no. 2, pp. 263–272, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. H. J. Krugers, S. van der Linden, E. van Olst et al., “Dissociation between apoptosis, neurogenesis, and synaptic potentiation in the dentate gyrus of adrenalectomized rats,” Synapse, vol. 61, no. 4, pp. 221–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. D. G. Margineanu, A. J. Gower, J. Gobert, and E. Wulfert, “Long-term adrenalectomy reduces hippocampal granule cell excitability in vivo,” Brain Research Bulletin, vol. 33, no. 1, pp. 93–98, 1993. View at Publisher · View at Google Scholar · View at Scopus
  41. R. J. Sutherland, I. Q. Whishaw, and B. Kolb, “A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat,” Behavioural Brain Research, vol. 7, no. 2, pp. 133–153, 1983. View at Publisher · View at Google Scholar
  42. G. F. Xavier, F. J. B. Oliveira-Filho, and A. M. G. Santos, “Dentate gyrus-selective colchicine lesion and disruption of performance in spatial tasks: difficulties in 'place strategy' because of a lack of flexibility in the use of environmental cues?” Hippocampus, vol. 9, no. 6, pp. 668–681, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. C. M. McCormick, M. McNamara, S. Mukhopadhyay, and J. E. Kelsey, “Acute corticosterone replacement reinstates performance on spatial and nonspatial memory tasks 3 months after adrenalectomy despite degeneration in the dentate gyrus,” Behavioral Neuroscience, vol. 111, no. 3, pp. 518–531, 1997. View at Publisher · View at Google Scholar
  44. N. O'Brien, H. Lehmann, V. Lecluse, and D. G. Mumby, “Enhanced context-dependency of object recognition in rats with hippocampal lesions,” Behavioural Brain Research, vol. 170, no. 1, pp. 156–162, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. D. G. Mumby, S. Gaskin, M. J. Glenn, T. E. Schramek, and H. Lehmann, “Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts,” Learning & Memory, vol. 9, no. 2, pp. 49–57, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. L. de Toledo-Morrell, B. Dickerson, M. P. Sullivan, C. Spanovic, R. Wilson, and D. A. Bennett, “Hemispheric differences in hippocampal volume predict verbal and spatial memory performance in patients with Alzheimer's disease,” Hippocampus, vol. 10, no. 2, pp. 136–142, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. R. S. Astur, L. B. Taylor, A. N. Mamelak, L. Philpott, and R. J. Sutherland, “Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task,” Behavioural Brain Research, vol. 132, no. 1, pp. 77–84, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Marschner, R. Kalisch, B. Vervliet, D. Vansteenwegen, and C. Büchel, “Dissociable roles for the hippocampus and the amygdala in human cued versus context fear conditioning,” Journal of Neuroscience, vol. 28, no. 36, pp. 9030–9036, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. O. Pascalis, N. M. Hunkin, J. Bachevalier, and A. R. Mayes, “Change in background context disrupts performance on visual paired comparison following hippocampal damage,” Neuropsychologia, vol. 47, no. 10, pp. 2107–2113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Laczó, R. Andel, M. Vyhnalek et al., “Human analogue of the morris water maze for testing subjects at risk of Alzheimer's Disease,” Neurodegenerative Diseases, vol. 7, no. 1–3, pp. 148–152, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Kempermann, S. Jessberger, B. Steiner, and G. Kronenberg, “Milestones of neuronal development in the adult hippocampus,” Trends in Neurosciences, vol. 27, no. 8, pp. 447–452, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Alvarez-Buylla and J. M. García-Verdugo, “Neurogenesis in adult subventricular zone,” Journal of Neuroscience, vol. 22, no. 3, pp. 629–634, 2002. View at Scopus
  53. J. E. Malberg, A. J. Eisch, E. J. Nestler, and R. S. Duman, “Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus,” Journal of Neuroscience, vol. 20, no. 24, pp. 9104–9110, 2000. View at Scopus
  54. L. Santarelli, M. Saxe, C. Gross et al., “Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants,” Science, vol. 301, no. 5634, pp. 805–809, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. H. G. Kuhn, J. Winkler, G. Kempermann, L. J. Thal, and F. H. Gage, “Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain,” Journal of Neuroscience, vol. 17, no. 15, pp. 5820–5829, 1997. View at Scopus
  56. G. Kempermann, H. G. Kuhn, and F. H. Gage, “More hippocampal neurons in adult mice living in an enriched environment,” Nature, vol. 386, no. 6624, pp. 493–495, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. A. K. Olson, B. D. Eadie, C. Ernst, and B. R. Christie, “Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways,” Hippocampus, vol. 16, no. 3, pp. 250–260, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Brown, C. M. Cooper-Kuhn, G. Kempermann et al., “Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis,” European Journal of Neuroscience, vol. 17, no. 10, pp. 2042–2046, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Gould, H. A. Cameron, D. C. Daniels, C. S. Woolley, and B. S. McEwen, “Adrenal hormones suppress cell division in the adult rat dentate gyrus,” Journal of Neuroscience, vol. 12, no. 9, pp. 3642–3650, 1992. View at Scopus
  60. H. A. Cameron, “Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus,” Neuroscience, vol. 61, no. 2, pp. 203–209, 1994. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Tanapat, N. B. Hastings, T. A. Rydel, L. A. M. Galea, and E. Gould, “Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism,” Journal of Comparative Neurology, vol. 437, no. 4, pp. 496–504, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. M. F. Montaron, K. G. Petry, J. J. Rodriguez, et al., “Adrenalectomy increases neurogenesis but not PSA-NCAM expression in aged dentate gyrus,” European Journal of Neuroscience, vol. 11, no. 4, pp. 1479–1485, 1999. View at Publisher · View at Google Scholar
  63. E. Y. H. Wong and J. Herbert, “Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus,” European Journal of Neuroscience, vol. 22, no. 4, pp. 785–792, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Tashiro, H. Makino, and F. H. Gage, “Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage,” Journal of Neuroscience, vol. 27, no. 12, pp. 3252–3259, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Auvergne, C. Leré, B. El Bahh et al., “Delayed kindling epileptogenesis and increased neurogenesis in adult rats housed in an enriched environment,” Brain Research, vol. 954, no. 2, pp. 277–285, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. H. van Praag, B. R. Christie, T. J. Sejnowski, and F. H. Gage, “Running enhances neurogenesis, learning, and long-term potentiation in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 23, pp. 13427–13431, 1999. View at Publisher · View at Google Scholar · View at Scopus
  67. J. S. Rhodes, S. Jeffrey, I. Girard et al., “Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running,” Behavioral Neuroscience, vol. 117, no. 5, pp. 1006–1016, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. A. S. Naylor, A. I. Persson, P. S. Eriksson, I. H. Jonsdottir, and T. Thorlin, “Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat,” Journal of Neurophysiology, vol. 93, no. 5, pp. 2406–2414, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Kempermann and F. H. Gage, “Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal,” Hippocampus, vol. 9, no. 3, pp. 321–332, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. G. Lai, H. Lehmann, S. C. Spanswick, H. Yamazaki, and R. J. Sutherland, “Behavior deficit and functional recovery after granule cell death in the hippocampus,” Society for Neuroscience Abstracts, p. 779.8, 2007.
  71. K. S. Rai, B. Hattiangady, and A. K. Shetty, “Enhanced production and dendritic growth of new dentate granule cells in the middle-aged hippocampus following intracerebroventricular FGF-2 infusions,” European Journal of Neuroscience, vol. 26, no. 7, pp. 1765–1779, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Ahn and A. L. Joyner, “In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog,” Nature, vol. 437, no. 7060, pp. 894–897, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. V. Palam, D. A. Lim, N. Dahmane et al., “Sonic hedgehog controls stem cells behavior in the postnatal and adult brain,” Development, vol. 132, no. 2, pp. 335–344, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. R. R. Hicks, D. H. Smith, D. H. Lowenstein, R. Saint Marie, and T. K. McIntosh, “Mild experimental brain injury in the rat induces cognitive deficits associated with regional neuronal loss in the hippocampus,” Journal of Neurotrauma, vol. 10, no. 4, pp. 405–414, 1993. View at Scopus
  75. T. Yamaki, N. Murakami, Y. Iwamoto et al., “Cognitive dysfunction and histological findings in rats with chronic- stage contusion and diffuse axonal injury,” Brain Research Protocols, vol. 3, no. 1, pp. 100–106, 1998. View at Publisher · View at Google Scholar · View at Scopus
  76. J. W. Huh and R. Raghupathi, “Chronic cognitive deficits and long-term histopathological alterations following contusive brain injury in the immature rat,” Journal of Neurotrauma, vol. 24, no. 9, pp. 1460–1474, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. K. D. Langdon, S. Granter-Button, and D. Corbett, “Persistent behavioral impairments and neuroinflammation following global ischemia in the rat,” European Journal of Neuroscience, vol. 28, no. 11, pp. 2310–2318, 2008. View at Publisher · View at Google Scholar · View at Scopus