Adrenalectomy-induced granule cell degeneration in the hippocampus causes spatial memory deficits that are not reversed by chronic treatment with corticosterone or fluoxetine

Hippocampus

Volumn 17, Issue 2, 2007, Pages 137-146

  Spanswick, Simon C ^a   Epp, Jonathan R ^a   Keith, Julian R ^b   Sutherland, Robert J ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Adult neurogenesis; Antidepressant; Dentate gyrus; Doublecortin; Ki67; Regeneration

Indexed keywords

APOTEX; CORTICOSTERONE; DOUBLECORTIN; FLUOXETINE; KI 67 ANTIGEN; UNCLASSIFIED DRUG;

ADRENALECTOMY; AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL DEGENERATION; CONTROLLED STUDY; DRUG MECHANISM; GRANULE CELL; HIPPOCAMPUS; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; SPATIAL MEMORY;

ADRENALECTOMY; ANIMALS; BIOLOGICAL MARKERS; CELL COUNT; CORTICOSTERONE; CYTOPLASMIC GRANULES; FLUOXETINE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MALE; MAZE LEARNING; MEMORY DISORDERS; MICROTUBULE-ASSOCIATED PROTEINS; NERVE DEGENERATION; NEUROPEPTIDES; RATS; RATS, LONG-EVANS; SEROTONIN UPTAKE INHIBITORS; SPACE PERCEPTION;

EID: 33847666058     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20252     Document Type: Article

References (44)

1. Ambrogini P, Orsini L, Mancini C, Ferri P, Ciaroni S, Cuppini R. 2004. Learning may reduce neurogenesis in adult rat dentate gyrus. Neurosci Lett 359:13-16.
2. Amrein I, Slomianka L, Poletaeva II, Bologova NV, Lipp HP. 2004. Marked species and age-dependent differences in cell proliferation and neurogenesis in the hippocampus of wild-living rodents. Hippocampus 14:1000-1010.
3. Armstrong JN, McIntyre DC, Neubort S, Sloviter RS. 1993. Learning and memory after adrenalectomy-induced hippocampal dentate granule cell degeneration in the rat. Hippocampus 3:359-371.
4. Atkinson HC, Wood SA, Kershaw YM, Bate E, Lightman SL. 2006. Diurnal variation in the responsiveness of the hypothalamic-pituitary-adrenal axis of the male rat to noise stress. J Neuroendocrinol 18:526-533.
5. Banasr M, Hery M, Printemps R, Daszuta A. 2004. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 29:450-460.
6. Barnea A, Nottebohm F. 1994. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217-11221.
7. Bizon JL, Lee HJ, Gallagher M. 2004. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 3:227-234.
8. Brown JP, Couillard-Depres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
9. Carlén M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisén J. 2002. Functional integration of adult-born neurons. Curr Biol 12:606-608.
10. Conrad CD, Roy EJ. 1993. Selective loss of hippocampal granule cells following adrenalectomy: Implications for spatial memory. J Neurosci 13:2582-2590.
11. Conrad CD, Roy EJ. 1995. Dentate gyrus destruction and spatial learning impairment after corticosteroid removal in young and middle-aged rats. Hippocampus 5:1-15.
12. Czurko A, Czeh B, Seress L, Nadel L, Bures J. 1997. Severe spatial navigation deficit in the Morris water maze after single high dose of neonatal X-ray irradiation in the rat. Proc Natl Acad Sci USA 94:2766-2771.
13. Dudchenko PA, Wood ER, Eichenbaum H. 2000. Neurotoxic hippocampal lesions have no effect on odor span and little effect on odor recognition memory but produce significant impairments on spatial span recognition, and alternation. J Neurosci 20:2964-2977.
14. Encinas JM, Vahtokari, Enikolopov G. 2006. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 103:8233-8238.
15. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
16. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
17. Huang GJ, Herbert J. 2006. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 59:619-624.
18. Islam A, Henriksson B, Mohammed A, Winbald B, Adem A. 1995. Behavioral deficits in adult rats following long-term adrenalectomy. Neurosci Lett 194:49-52.
19. Jarrad LE. 2002. Use of excitotoxins to lesion the hippocampus: Update. Hippocampus 12:405-414.
20. Jeltsch H, Bertrand F, Lazarus C, Cassel JC. 2001. Cognitive performances and locomotor activity following dentate granule cell damage in rats: Role of lesion extent and type of memory tested. Neurobiol Learn Mem 76:81-105.
21. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs. Science 197:1092-1094.
22. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM. 2002. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105.
23. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
24. Kempermann G, Jessberger S, Steiner B, Kronenberg G. 2004. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
25. Kodama M, Fujioka T, Duman RS. 2004. Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry 56:570-580.
26. Malberg J, Eisch AJ, Nestler EJ, Duman RS. 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110.
27. McCormick CM, McNamara M, Mukhopadhyay S, Kelsey JE. 1997. Acute corticosterone replacement reinstates performance on spatial and nonspatial memory tasks 3 months after adrenalectomy despite degeneration in the dentate gyrus. Behav Neurosci 1111:518-531.
28. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ. 1989. Hippocampal granule cells are necessary for normal spatial-learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76:485-496.
29. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
30. Rao MS, Shetty AK. 2004. Efficacy of doublecortin as a marker to analyse the absolute number and dendrite growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19:234-246.
31. Roozendaal B, Sapolsky RM, McGaugh JL. 1998. Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neuroscience 84:453-465.
32. Roozendaal B, Phillips RG, Power AE, Brooke SM, Sapolsky RM, McGaugh JL. 2001. Memory retrieval impairment induced by hippocampal CA3 lesions is blocked by adrenocortical suppression. Nat Neurosci 4:1169-1171.
33. Rudy JW, Barrientos RM, O'Reilly RC. 2002. The hippocampal formation supports conditioning to memory of a context. Behav Neurosci 116:530-538.
34. Scholzen T, Gerdes J. 2000. The Ki-67 protein: From the known and unknown. J Cell Physiol 182:311-322.
35. Sloviter RS, Valiquette G, Abrams GM, Ronk EC, Sollas AL, Paul LA, Neubort S. 1989. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 243:535-538.
36. Sloviter RS, Dean E, Neubort S. 1993a. Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: Apoptosis in the adult central nervous system. J Comp Neurol 330:337-351.
37. Sloviter RS, Sollas AL, Dean E, Neubort S. 1993b. Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: Characterization of an in vivo model of controlled neuronal death. J Comp Neurol 330:324-336.
38. Sousa N, Madeira MD, Paula-Barbosa MM. 1999. Corticosterone replacement restores normal morphological features to the hippocampal dendrites, axons and synapses of adrenalectomized rats. J Neurocytol 28:541-558.
39. Sutherland RJ, Kolb B, Whishaw IQ. 1982. Spatial mapping: Definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neurosci Lett 31:271-276.
40. Sutherland RJ, Whishaw IQ, Kolb B. 1983. A behavioral analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behav Brain Res 7:133-153.
41. Vaher P, Luine VN, Gould E, McEwan BS. 1994. Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology. Brain Res 656:71-78.
42. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
43. Woolley CS, Gould E, Sakai RR, Spencer RL, McEwen BS. 1991. Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res 554:312-315.
44. Xavier GF, Oliveira-Filho JB, Santos AMG. 1999. 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 9:668-681.