Neurochemical changes in the hippocampus of the brown Norway rat during aging

Neurobiology of Aging

Volumn 18, Issue 3, 1997, Pages 319-327

  Bhatnagari, M ^a   Cintra, A ^a   Chadi, G ^a   Lindberg, J ^a   Oitzl, M ^b   De Kloet, E R ^b   Moller A ^c   Agnati, L F ^d   Fuxe, K ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LEIDEN UNIVERSITY   (Netherlands)

^c NEUROSEARCH A S   (Denmark)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Basic fibroblast growth factor; Brown Norway rat; Glucocorticoid receptors; Hippocampus; Immunocytochemistry; Mineralocorticoid receptors; Stereology

Indexed keywords

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CORTICOSTERONE RELEASE; DRUG RECEPTOR BINDING; GLIA CELL; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; NERVE DEGENERATION; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; STEREOLOGY; STRESS;

EID: 0030742529     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-4580(97)80314-4     Document Type: Article

References (60)

1. Agnati L. F., Fuxe K., Zoli M., Ferraguti F., Benfenati F., Ouimet C., Walaas I., Golstein M., Greengard P. Morphometrical analysis of tyrosine hydroxylase, enkephalin and DARPP-32-like immunoreactive profiles and their codistribution at three rostrocaudal levels of the striatum. Neuroscience. 27:1988;785-797.
2. Ahima R. S., Harlan R. E. Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience. 39:1990;579-604.
3. Ahima R. S., Krozowski Z., Harlan R. E. Type I corticosteroid receptor-like immunoreactivity in the rat CNS: Distribution and regulation by corticosteroids. J. Comp. Neurol. 313:1991;522-538.
4. Barbany G., Persson H. Regulation of neurotrophin mRNA expression in the rat brain by glucocorticoids. Eur. J. Neurosci. 4:1992;396-403.
5. Barbany G., Persson H. Adrenalectomy attenuates kainic acid-elicited increases of messenger RNAs for neurotrophins and their receptors in the rat brain. Neuroscience. 54:1993;909-922.
6. Bardgett M. E., Taylor G. T., Csernansky J. G., Newcomer J. W., Nock B. Chronic corticosterone impairs spontaneous alternation in rats. Behav. Neural Biol. 61:1994;186-190.
7. Bronson R. T., Lipman R. D., Harrison D. E. Age-related gliosis in the white matter of mice. Brain Res. 609:1993;124-128.
8. Chao H. M., McEwen B. S. Glucocorticoids and the expression of mRNAs for neurotrophins, their receptors and GAP-43 in the rat hippocampus. Mol. Brain Res. 26:1994;271-276.
9. Cintra A., Lindberg J., Chadi G., Tinner B., Möller A., Gustafsson J.-Å., de Kloet E. R., Oitzl M., Agnati L. F., Fuxe K. Basic fibroblast growth factor and steroid receptors in the aging hipocampus of the Brown Norway rat: Immunocytochemical analysis in combination with stereology. Neurochem. Int. 25:1994;39-45.
10. Cintra A., Zoli M., Rosén L., Agnati L. F., Okret S., Wikström A.-C., Gustafsson J.-Å., Fuxe K. Mapping and computer assisted morphometry and microdensitometry of glucocorticoid receptor immunoreactive neurons and glial cells in the rat central nervous system. Neuroscience. 62:1994;843-897.
11. Coleman P. D., Flood D. G. Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol. Aging. 8:1987;521-545.
12. DeKloet E. R., Sutanto W., Rots N., van Haarst A., van den Berg D., Oitzl M., van Eekelen J. A., Voorhuis D. Plasticity and function of brain corticosteroid receptors during aging. Acta Endocrinol. 125:(Suppl 1):1991;65-72.
13. Dember W. N. The search for cues and motives. Dember W. N., Richman L. L. Spontaneous alternation behavior. 1990;19-39 Springer Verlag, New York.
14. Douglas R. J. Spontaneous alternation behavior and the brain. Dember W. N., Richman L. L. Spontaneous alternation behavior. 1990;73-109 Springer Verlag, New York.
15. Eldridge J. C., Kute T., Brodish A., Landfield P. W. Apparent age-dependent resistance of hippocampal type II corticoid receptors to down-regulation by chronic scape training. J. Neurosci. 9:1989;3237-3242.
16. Fuxe K., Diaz R., Cintra A., Bhatnagar M., Tinner B., Gustafsson J.-Å., Ögren S.-O., Agnati L. F. On the role of glucocorticoid receptors in brain plasticity. Cell. Mol. Neurobiol. 16:1996;239-258.
17. Fuxe K., Wikström A.-C., Okret S., Agnati L. F., Härfstrand A., Yu Z.-Y., Granholm L., Zoli M., Vale W., Gustafsson J.-Å.-. Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel-and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor. Endocrinology. 177:1985;1803-1812.
18. Geinisman Y., de Toledo-Morrell L., Morrell F. Aged rats need a preserved complement of perforated axospinous synapses per hippocampal neuron to maintain good spatial memory. Brain Res. 398:1986;266-275.
19. Gerlai R., Marks A., Roder J. T-maze spontaneous alternation rate is decreased in S100ß transgenic mice. Behav. Neurosci. 108:1994;100-106.
20. Goss J. R., Morgan D. G. Enhanced glial fibrillary acidic protein RNA response to fornix transection in aged mice. J. Neurochem. 64:1995;1351-1360.
21. Gundersen H. J. G., Jensen E. B. The efficiency of systematic sampling in stereology and its predication. J. Microsc. 147:1987;229-263.
22. Hsu S.-M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:1981;577.
23. Hughes R. N. Phylogenetic comparisons. Dember W. N., Richman L. L. Spontaneous alternation behavior. 1990;39-59 Springer Verlag, New York.
24. Issa A. M., Rowe W., Gauthier S., Meaney M. J. Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J. Neurosci. 10:1990;3247-3254.
25. Kohama S. G., Goss J. R., Finch C. E., McNeill T. H. Increases of glial fibrillary acidic protein in the aging female mouse brain. Neurobiol. Aging. 16:1995;59-67.
26. Krozowski Z., Rundle S. E., Wallace C., Castell M. J., Shen J.-H., Dowling J., Funder J. W., Smith A. I. Immunolocalization of renal mineralocorticoid receptors with an antiserum against a peptide deduced from the complimentary deoxyribonucleic acid sequence. Endocrinology. 125:1989;192-198.
27. Landfield P. W., Baskin R. K., Pitler T. A. Brain aging correlates: Retardation by hormonal-pharmacological treatments. Science. 214:1981;581-584.
28. Landfield P. W., Eldridge J. C. Evolving aspects of the glucocorticoid hypothesis of brain aging: Hormonal modulation of neuronal calcium homeostasis. Neurobiol. Aging. 15:1994;579-588.
29. Landfield P. W., Waymire J. L., Lynch G. S. Hippocampal aging and adrenocorticoids: Quantitative correlations. Science. 202:1978;1098-1102.
30. Lorens S. A., Hata N., Handa R. J., van de Kar L. D., Guschwan M., Goral J., Lee J. M., Hamilton M. E., Bethea C. L., Clancy J. Jr. Neurochemical, endocrine and immunological responses to stress in young and old Fischer 344 male rats. Neurobiol. Aging. 11:1990;139-150.
31. Matsuzaki K., Yoshitake Y., Matuo Y., Sasaki H., Nishikawa K. Monoclonal antibodies against heparin-binding growth factor II/basic fibroblast growth factor that block its biological activity: Invalidity of the antibodies for tumor angiogenesis. Proc. Natl. Acad. Sci. USA. 86:1989;9911-9915.
32. McEwen B. S., Weiss J. M., Schwartz L. S. Selective retention of corticosterone by limbic structures in rat brain. Nature. 220:1968;911-912.
33. Meaney M. J., Aitken D. H., van Berkel C., Bhatnagar S., Sapolsky R. M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science. 239:1988;766-768.
34. Newcomer J. W., Craft S., Hershey T., Askins K., Bardgett M. E. Glucocorticoid-induced impairments in declarative memory performance in adult humans. J. Neurosci. 14:1994;2047-2053.
35. Oitzl M. S., de Kloet E. R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106:1992;62-71.
36. Oitzl M. S., Fluttert M., de Kloet E. R. The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur. J. Neurosci. 6:1994;1072-1079.
37. Okret S., Wikström A.-C., Wrange Ö., Andersson B., Gustafsson J.-Å. Monoclonal antibodies against the rat liver glucocorticoid receptor. Proc. Natl. Acad. Sci. USA. 81:1984;1609-1613.
38. Patacchioli F. R., Casolini P., Puglisi-Allegra S., Sadile A. G., Angelucci L. Hippocampal glucocorticoid receptor and behavior: A correlative study in rats and mice. J. Steroid Biochem. Mol. Biol. 37:1990;405-409.
39. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1986;Harcourt Brace Jovanovich, San Diego.
40. Peterson D. A., Lucidi-Phillipi C. A., Murphy D. P., Ray J., Gage F. H. Fibroblast growth factor-2 protects entorhinal layer II glutamatergic neurons from axotomy-induced death. J. Neurosci. 16:1996;886-898.
41. Rapp P. R., Amaral D. G. Individual differences in the cognitive and neurobiological consequences of normal aging. Trends Neurosci. 15:1992;340-344.
42. Rapp P. R., Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. USA. 93:1996;9926-9930.
43. Rasmussen T., Schliemann T., Sörensen J. C., Zimmer J., West M. J. Memory impaired rats: No loss of principal hippocampal and subicular neurons. Neurobiol. Aging. 17:1996;143-147.
44. Reul J. M. H. M., deKloet E. R. Two receptor systems for corticosterone in rat brain: Microdistribution and diferential occupation. Endocrinology. 117:1985;2505-2511.
45. Reul J. M. H. M., Tonnaer H. A. D. M., de Kloet E. R. Neurotrophic ACTH analogue promotes plasticity of type I corticosteroid receptor in brain of senescent rats. Neurobiol. Aging. 8:1988;253-261.
46. Sapolsky R. M., Krey L. C., McEwen B. S. Corticosterone receptors decline in a site-specific manner in the aged rat brain. Brain Res. 289:1983;235-240.
47. Sapolsky R. M., Krey L. C., McEwen B. S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. J. Neurosci. 5:1985;1222-1227.
48. Sapolsky R. M., Krey L. C., McEwen B. S. The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis. Endocr. Rev. 7:1986;284-301.
49. Sapolsky R. M., Packan D. R., Vale W. W. Glucocorticoid toxicity in the hippocampus: In vitro demonstration. Brain Res. 453:1988;367-371.
50. Spruijt B. M., Hol T., Rouseau J. Approach, avoidance and contact behavior of individually recognized animals automatically quantified with an image analysis technique. Physiol. Behav. 51:1992;747-752.
51. Uno H., Tarara R., Else J. G., Suleman M. S., Sapolsky R. M. Hippocampal damage associated with prolonged and fatal stress in primates. J. Neurosci. 9:1989;1705-1711.
52. van Eekelen J. A., de Kloet E. R. Co-localization of brain corticosterone receptors in the rat hippocampus. Prog. Histochem. Cytochem. 26:1992;250-258.
53. van Eekelen J. A. M., Oitzl M. S., de Kloet E. R. Adrenocortical deficiency and glucocorticoid feedback resistance on old male Brown Norway rats. J. Geront. 50:1995;B83-B89.
54. van Eekelen J. A. M., Rots N. Y., Sutanto W., de Kloet E. R. The effect of aging on stress responsiveness and central corticosteroid receptors in the Brown Norway rat. Neurobiol. Aging. 13:1992;159-170.
55. West M. J., Slomianka L., Gundersen H. J. G. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231:1991;482-497.
56. Woodward W. R., Nishi R., Meshul C. K., Williams T. E., Coulombe M., Eckenstein F. P. Nuclear and cytoplasmic localization of basic fibroblast growth factor in astrocytes and CA2 hippocampal neurons. J. Neurosci. 12:1992;142-152.
57. Zamboni I., de Martino C. Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy. J. Cell. Biol. 35:1967;148A.
58. Zoli M., Agnati L. F., Fuxe K., Ferraguti F., Biagini G., Cintra A., Gustafsson J.-Å. Long-lasting reduction of glucocorticoid receptor immunoreactivity in the hippocampal field CA1 but not in the dentate gyrus after neonatal treatment with corticosterone in the rat. Acta Physiol. Scand. 138:1990;577-579.
59. Zoli M., Ferraguti F., Gustafsson J.-Å, Toffano G., Fuxe K., Agnati L. F. Selective reduction of glucocorticoid receptor immunoreactivity in the hippocampal formation and central amygdaloid nucleus of the aged rat. Brain Res. 545:1991;199-207.
60. Zoli M., Zini I., Agnati L. F., Guidolin D., Ferraguti F., Fuxe K. Aspects of neuronal plasticity in the central nervous system. Computer-assisted image analysis methods. Neurochem. Int. 16:1990;383-418.