Skip to main content
NCBI home page
Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 1993 Aug;13(4):457–482. doi: 10.1007/BF00711583

Adrenal steroids and plasticity of hippocampal neurons: Toward an understanding of underlying cellular and molecular mechanisms

Bruce S McEwen 1,✉, Heather Cameron 1, Helen M Chao 1, Elizabeth Gould 1, Ana Maria Magarinos 1, Yoshifumi Watanabe 1, Catherine S Woolley 1
PMCID: PMC11566985  PMID: 8252613

The content is available as a PDF (1.7 MB).

References

  1. Aloe, L. (1989). Adrenalectomy decreases nerve growth factor in young adult rat hippocampus.Proc. Natl. Acad. Sci. USA865636–5640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alzheimer, C., Rohrenbeck, J., and Bruggencate, G. (1991). Adenosine depresses induction of LTP at the mossy fiber-CA3 synapse in vitro.Brain Res.534163–165. [DOI] [PubMed] [Google Scholar]
  3. Andrade, J., Cadete-leite, A., Madeira, M., and Paula-Barbosa, M. (1991). Long-term low-protein diet reduces the number of hippocampal mossy fiber synapses.Exp. Neurol.112119–124. [DOI] [PubMed] [Google Scholar]
  4. Armanini, M., Hutchins, C., Stein, B., and Sapolsky, R. (1990). Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent.Brain Res.5327–12. [DOI] [PubMed] [Google Scholar]
  5. Arnold, A., and Breedlove, S. (1985). Organizational and activational effects of sex steroids on brain and behavior: A reanalysis.Horm. Behav.19469–498. [DOI] [PubMed] [Google Scholar]
  6. Arriza, J., Weinberger, C., Cerelli, G., Glaser, T., Handelin, B., Housman, D., and Evans, R. (1987). Cloning of human mineralocorticoid receptor complementary DNA: Structural and functional kinship with the glucocorticoid receptor.Science237268–275. [DOI] [PubMed] [Google Scholar]
  7. Arriza, J., Simerly, R., Swanson, L., and Evans, R. (1988). The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response.Neuron1887–900. [DOI] [PubMed] [Google Scholar]
  8. aus der Muhlen, K., and Ockenfels, H. (1969). Morphologische veranderungen im diencephalon und telencephalon: Storungen des regelkreises adenohypophysenenbennierenrinde.Z. Zellforsch. Mikrosck. Anat.93126–141. [Google Scholar]
  9. Ballarin, M., Ernfors, P., Lindefors, N., and Persson, H. (1991). Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain.Exp. Neurol.11435–43. [DOI] [PubMed] [Google Scholar]
  10. Barbany, G., and Persson, H. (1992). Regulation of neurotrophin mRNA expression in the rat brain by glucocorticoids.Eur. J. Neurosci.4396–403. [DOI] [PubMed] [Google Scholar]
  11. Barton, A., Harrison, P., Najlerahim, A., Jeffernan, J., McDonald, B., Robinson, J., Davies, D., Harrison, W., Mitra, P., Hardy, J., and Pearson, R. (1990). Increased Tau messenger RNA in Alzheimer's disease hippocampus.Am. J. Pathol.137497–502. [PMC free article] [PubMed] [Google Scholar]
  12. Bayer, S. (1985). The hippocampus. InThe Rat Nervous System (G. Paxinos, Ed.), Academic, Sydney, pp. 335–352. [Google Scholar]
  13. Bear, M., Kleinschmidt, A., Gu, Q., and Singer, W. (1990). Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist.J. Neurosci.10909–925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bennett, E., Diamond, M., Krech, D., and Rosenzweig, M. (1964). Chemical and anatomical plasticity of brain.Science146610–618. [DOI] [PubMed] [Google Scholar]
  15. Benshalom, G., and White, E. (1988). Dendritic spines are susceptible to structural alterations induced by degeneration of their presynaptic afferents.Brain Res.443377–382. [DOI] [PubMed] [Google Scholar]
  16. Bielenberg, G., and Brukhardt, M. (1990). 5-Hydroxytryptamine-1A agonists. A new therapeutic principle for stroke treatment.Stroke Suppl.IV(21):IV-161–IV-163. [PubMed] [Google Scholar]
  17. Bindu, P., and Desiraju, T. (1990). Increase of dendritic branching of CA3 neurons of hippocampus and self-stimulation areas in subjects experiencing self-stimulation of lateral hypothalamus and substantia nigra-ventral tegmental area.Brain Res.527171–175. [DOI] [PubMed] [Google Scholar]
  18. Bode-Greuel, K., Klisch, J., Horvath, E., Glaser, T., and Traber, J. (1990). Effects of 5-hydroxytryptamine 1A-receptor agonists on hippocampal damage after transient forebrain ischemia in the Mongolian gerbil.Stroke Suppl.IV (21):IV-164–IV-166. [PubMed] [Google Scholar]
  19. Boxer, P., Cordon, J., Mann, M., Rodolosi, L., Vartanina, M., Rock, D., Taylor, C., and Marcoux, F. (1990). Comparison of phenytoin with noncompetitive N-methyl-D-aspartate antagonists in a model of focal brain ischemia in rat.Stroke21III-47–III-51. [PubMed] [Google Scholar]
  20. Caceres, A., Payne, M., Binder, L., and Steward, O. (1983). Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines.Proc. Natl. Acad. Sci. USA801738–1742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Chao, H. M., Spencer, R. L., Sakai, R. R., and McEwen, B. S. (1992). The expression of growth-associated protein GAP-43 mRNA in the rat hippocampus in response to adrenalectomy and aging.Mol. Cell. Neurosci.3529–535. [DOI] [PubMed] [Google Scholar]
  22. Chem, S., and Hillman, D. (1992). Transient c-fos expression and dendritic spine plasticity in hippocampal granule cells.Brain Res.577169–174. [DOI] [PubMed] [Google Scholar]
  23. Choi, D. (1990). Cerebral hypoxia: some new approaches and unanswered questions.J. Neurosci.102493–2501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Cline, H., and Constantine-Paton, M. (1989). NMDA receptor antagonists disrupt the retinotectal topographic map.Neuron3413–426. [DOI] [PubMed] [Google Scholar]
  25. Cline, H., Debski, E., and Constantine-Paton, M. (1987). N-Methyl-D-asparate receptor antagonist desegregates eye-specific stripes.Proc. Natl. Acad. Sci.844342–4345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Cole, A., Saffen, D., Baraban, J., and Worley, P. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation.Nature340474–476. [DOI] [PubMed] [Google Scholar]
  27. Collins, F., and Crutcher, K. (1989). Sustained elevation in hippocampal NGF-like biological activity following medial septal lesions in the rat.Brain Res.490355–360. [DOI] [PubMed] [Google Scholar]
  28. Coss, R., and Globus, A. (1978). Spine stems on tectal interneurons in jewel fish are shortened by social stimulation.Science200788–789. [DOI] [PubMed] [Google Scholar]
  29. Crowder, J., and Bradford, H. (1987). Common anticonvulsants inhibit Ca2+ uptake and amino acid neurotransmitter release in vitro.Epilepsia28378–382. [DOI] [PubMed] [Google Scholar]
  30. Crusio, W., and Schwegler, H. (1991). Early postnatal hyperthyroidism improves both working and reference memory in a spatial radial-maze task in adult mice.Physiol. Behav.50259–261. [DOI] [PubMed] [Google Scholar]
  31. Crusio, W., Schwegler, H., and van Abeelen, J. H. (1991). Behavioral and neuroanatomical divergence between two sublines of C57BL/6J inbred mice.Behav. Brain Res.4293–97. [DOI] [PubMed] [Google Scholar]
  32. Davis, L., Burger, B., Banker, B., and Steward, O. (1990). Dendritic transport: Quantitative analysis of the time course of somatodendritic transport of recently synthesized RNA.J. Neurosci.103056–3068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Deitch, J., and Rubel, E. (1989). Rapid changes in ultrastructure during deafferentation-induced dendritic atrophy.J. Comp. Neurol.281234–258. [DOI] [PubMed] [Google Scholar]
  34. Dugich-Djordjevic, M., Tocco, G., Lapchak, P., Pasinetti, G., Najm, I., Baudry, M., and Hefti, F. (1992). Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid.Neuroscience47303–315. [DOI] [PubMed] [Google Scholar]
  35. Eichenbaum, H., and Otto, T. (1992). The hippocampus—what does it do?Behav. Neur. Biol.572–36. [Google Scholar]
  36. Fabrazzo, M., Costa, E., and Mocchetti, I. (1991). Stimulation of nerve growth factor biosynthesis in developing rat brain by reserpine: steroids as potential mediators.Mol. Pharmacol.39144–149. [PubMed] [Google Scholar]
  37. Fattaccini, C., Bolonos-Jimenez, H., Gozlan, H., and Hamon, M. (1990). Tianeptine stimulates uptake of 5-hydroxytryptamine in vivo in the rat brain.Neuropharmacology291–8. [DOI] [PubMed] [Google Scholar]
  38. Ferreira, A., and Caceres, A. (1991). Estrogen-enhanced neurite growth: Evidence for a selective induction of tau and stable microtubule.J. Neurosci.11392–400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ferreira, A., Busciglio, J., and Caceres, A. (1989). Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: Evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau.Dev. Brain Res.49215–228. [DOI] [PubMed] [Google Scholar]
  40. Fifkova, E., and van Harreveld, A. (1977). Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area.J. Neurocytol.6211–230. [DOI] [PubMed] [Google Scholar]
  41. Frankfurt, M., Gould, E., Woolley, C., and McEwen, B. S. (1990). Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a golgi study in the adult rat.Neuroendocrinology51530–535. [DOI] [PubMed] [Google Scholar]
  42. Fujikura, H., Kato, H., Nakano, S., and Kogure, K. (1989). A serotonin S2 antagonist, naftidrofuryl, exhibited a protective effect on ischemic neuronal damage in the gerbil.Brain Res.494387–390. [DOI] [PubMed] [Google Scholar]
  43. Gall, C., and Isackson, P. (1989). Limbic seizures increase neuronal production of messenger RNA for nerve growth factor.Science245758–761. [DOI] [PubMed] [Google Scholar]
  44. Garner, C., Tucker, R., and Matus, A. (1988). Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites.Nature336674–677. [DOI] [PubMed] [Google Scholar]
  45. Geinisman, Y., deToledo-Morrell, L., and Morrell, F. (1990). The brain's record experience: Kindling-induced enlargement of the active zone in hippocampal perforated synapses.Brian Res.513175–179. [DOI] [PubMed] [Google Scholar]
  46. Gerlach, J., and McEwen, B. S. (1972). Rat brain binds adrenal steroid hormone: Radioautography of hippocampus with corticosterone.Science1751133–1136. [DOI] [PubMed] [Google Scholar]
  47. Gilad, G., Gilad, V., Wyatt, R., and Tizabi, Y. (1990). Region-selective stress-induced increase of glutamate uptake and release in rat forebrain.Brain Res.525335–338. [DOI] [PubMed] [Google Scholar]
  48. Gomez-Pinilla, F., Lee, J. W.-K., and Cotman, C. (1992). Basic FGF in adult rat brain: Cellular distribution and response to entorhinal lesion and fimbria-fornix transection.J. Neurosci.12345–355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Gould, E., Woolley, C. S., and McEwen, B. S. (1990a). Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus.Neuroscience37367–375. [DOI] [PubMed] [Google Scholar]
  50. Gould, E., Woolley, C. S., Frankfurt, M., and McEwen, B. S. (1990b). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood.J. Neurosci.101286–1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Gould, E., Woolley, C. S., and McEwen, B. S. (1991a). The hippocampal formation: Morphological changes induced by thyroid, gonadal and adrenal hormones.Psychoneuroendocrinology1667–84. [DOI] [PubMed] [Google Scholar]
  52. Gould, E., Woolley, C. S., and McEwen, B. S. (1991b). Adrenal steroids regulate postnatal development of the rat dentate gyrus. I. Effects of glucocorticoids on cell death.J. Comp. Neurol.313479–485. [DOI] [PubMed] [Google Scholar]
  53. Gould, E., Woolley, C. S., Cameron, H. A., Daniels, D. C., and McEwen, B. S. (1991c). Adrenal steroids regulate postnatal development of the rat dentate gyrus. II. Effects of glucocorticoids and mineralocorticoids on cell birth.J. Comp. Neurol.313486–493. [DOI] [PubMed] [Google Scholar]
  54. Gould, E., Cameron, H. A., Daniels, D. C., Woolley, C. S., and McEwen, B. S., (1992). Adrenal hormones suppress cell division in the adult rat dentate gyrus.J. Neurosci.123642–3650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Greenough, W., and Bailey, C. (1988). The anatomy of a memory: convergence of results across a diversity of tests.TINS11142–147. [Google Scholar]
  56. Greenough, W., Juraska, J., and Volkmar, F. (1979. Maze training effects on dendritic branching in occipital cortex of adult rats.Behav. Neur. Biol.26287–297. [DOI] [PubMed] [Google Scholar]
  57. Griffith, W., and Taylor, L. (1988). Phenytoin reduces excitatory synaptic transmission and post-tetanic potentiation in the in virto hippocampus.J. Pharmacol. Exp. Ther.246851–858. [PubMed] [Google Scholar]
  58. Gustafsson, J.-A., Carlstedt-Duke, J., Poellinger, L.,et al. (1987). Biochemistry, molecular biology and physiology of the glucocorticoid receptor.Endocr. Rev.8185–234. [DOI] [PubMed] [Google Scholar]
  59. Hahm, J.-O., Langdon, R., and Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors.Nature351568–570. [DOI] [PubMed] [Google Scholar]
  60. Hahn, J., Aizenman, E., and Lipton, S. (1988). Central mammalian neurons normally resistant to glutamate toxicity are made sensitive by elevated extracellular CA2+: Toxicity is blocked by the N-methyl-D-asparate antagonist MK-801.Proc. Natl. Acad. Sci.856556–6560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Halpain, S., and Greengard, P. (1990). Activation of NMDA receptors induces rapid dephosphorylation of the cytoskeletal protein MAP2.Neuron5237–246. [DOI] [PubMed] [Google Scholar]
  62. Haydon, P., McCobb, D., and Kater, S. (1984). Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons.Science226561–564. [DOI] [PubMed] [Google Scholar]
  63. Herman, J. P., Patel, P. D., Akil, H., and Watson, S. J. (1989). Localization and regulation of glucocorticoid and mineralocorticoid receptor mRNAs in the hippocampal formation of the rat.Mol. Endocrinol.31886–1894. [DOI] [PubMed] [Google Scholar]
  64. Hirokawa, N., Hisanaga, S.-I., and Shiomura, Y. (1988). MAP2 is a component of crossbridges between microtubules and neurofilaments in the neuronal cytoskeleton: Quick-freeze, deep-etch immunoelectron microscopy and reconstitution studies.J. Neurosci.82769–2779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Horn, G., Bradley, P., and McCabe, B. (1985). Changes in the structure of synapses associated with learning.J. Neurosci.53161–3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Horner, H., Packan, D., and Sapolsky, R. (1990). Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia.Neuroendocrinology5257–64. [DOI] [PubMed] [Google Scholar]
  67. Hunt, S., Pini, A., and Evan, G. (1987). Induction of c-fos-like protein in spinal cord neurons following sensory stimulation.Nature328632–634. [DOI] [PubMed] [Google Scholar]
  68. Jacobs, L., and Spencer, W. (1991). Patterns of natural spatial behavior predict hippocampal size in kangeroo rats.Abstr. Soc. Neurosci.1754.7. [Google Scholar]
  69. Jacobson, L., and Sapolsky, R. (1991). The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis.Endocr. Rev.12118–134. [DOI] [PubMed] [Google Scholar]
  70. Joseph, R., Tsering, C., Grunfeld, S., and Welch, K. (1992). Serotonin may have neurotoxic properties.Neurosci. Lett.13615–18. [DOI] [PubMed] [Google Scholar]
  71. Kawarabayashi, T., Shoji, M., Harigaya, Y., Yamaguchi, H., and Hirai, S. (1991). Expression of APP in the early stage of brain damage.Brain Res.563334–338. [DOI] [PubMed] [Google Scholar]
  72. Kennet, G., Dickinson, S., and Curzon, G. (1985). Enhancement of some 5-HT dependent behavioral responses following repeated immobilization in rats.Brain Res.330253–263. [DOI] [PubMed] [Google Scholar]
  73. Kerr, S., Sqampbell, L., Applegate, M., Brodish, A., and Landfield, P. (1991). Chronic stressinduced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging.J. Neurosci.11316–1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Kiyota, Y., Takami, K., Iwane, M., Shino, A., Miyamoto, M., Tsukuda, R., and Nagakoa, A. (1991). Increase in basic fibroblast growth factor-like immunoreactivity in rat brain after forebrain ischemia.Brain Res.545322–328. [DOI] [PubMed] [Google Scholar]
  75. Kleiman, R., Banker, G., and Steward, O. (1990). Differential subcellular localization of particular mRNAs in hippocampal neurons in culture.Neuron5821–830. [DOI] [PubMed] [Google Scholar]
  76. Kleinschmidt, A., Bear, M., and Singer, W. (1987). Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex.Science238355–358. [DOI] [PubMed] [Google Scholar]
  77. Klisch, J., and Bode-Greuel, K. (1992). Ketanserin reduces neuronal calcium accumulation and cell death in the hippocampus of the mongolian gerbil after transient forebrain ischemia.Brain Res.5781–7. [DOI] [PubMed] [Google Scholar]
  78. Koh, J.-Y., Goldberg, M., Hartley, D., and Choi, D. (1990). Non-NMDA receptor-mediated neurotoxicity in cortical culture.J. Neurosci.10693–705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Koide, T., Wieloch, T., and Siesjo, B. (1986). Chronic dexamethasone pretreatment aggravates ischemic neuronal necrosis.J. Cereb. Blood Flow Metab.6395–404. [DOI] [PubMed] [Google Scholar]
  80. Kolasa, K., Song, L., and Jope, R. (1992). Adrenalectomy increases phosphoinositide hydrolysis induced by norepinephrine or excitatory amino acids in rat hippocampal slices.Brain Res.579128–134. [DOI] [PubMed] [Google Scholar]
  81. Krebs, J., Sherry, D., Healy, S., Perry, H., and Vaccarino, A. (1989). Hippocampal specialization of food-storing birds.Proc. Natl. Acad. Sci.861388–1392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Landfield, P. (1987). Modulation of brain aging correlates by long-term alterations of adrenal steroids and neurally-active peptides.Prog. Brain Res.72279–300. [DOI] [PubMed] [Google Scholar]
  83. Landfield, P., Baskin, R., and Pitter, T. (1981). Brain-aging correlates: Retardation by hormonalpharmacological treatments.Science214581–584. [DOI] [PubMed] [Google Scholar]
  84. Lauder, J. (1983). Hormonal and humoral influences on brain development.Psychoneuroendocrinology8121–155. [DOI] [PubMed] [Google Scholar]
  85. Lee, K., Schottler, F., Oliver, M., and Lynch, G. (1980). Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus.J. Neurophysiol.44247–258. [DOI] [PubMed] [Google Scholar]
  86. Lee, K., Frank, S., Vanderklish, P., Arai, A., and Lynch, G. (1991). Inhibition of proteolysis protects hippocampal neurons from ischemia.Proc. Natl. Acad. Sci. USA887233–7237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Lindholm, D., Hengerer, B., Heurmann, R., Carroll, P., and Thoenen, H. (1990). Glucocorticoid hormones negatively regulate nerve growth factor expression in vivo and in cultured rat fibroblasts.Eur. J. Neurosci.2795–801. [DOI] [PubMed] [Google Scholar]
  88. Lindholm, D., Castren, E., Hengerer, B., Zafra, F., Berninger, B., and Thoenen, H. (1992). Differential regulation of nerve growth factor (NGF) synthesis in neurons and astrocytes by glucocorticoid hormones.Eur. J. Neurosci.4404–410. [DOI] [PubMed] [Google Scholar]
  89. Lindvall, O., Ernfors, P., Bengzon, J., Kokaia, Z., Smith, M.-L., Siesjo, B., and Persson, H. (1992). Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma.Proc. Natl. Acad. Sci. USA89648–652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Lipton, D., and Kater, S. (1989). Plasticity and survival.TINS12265–270.2475939 [Google Scholar]
  91. Lorez, H., Keller, F., Ruess, G., and Otten, U. (1989). Nerve growth factor increases in adult rat brain after hypoxic injury.Neurosci. Lett.98339–344. [DOI] [PubMed] [Google Scholar]
  92. Madeira, M. D., Sousa, N., Lima-Andrade, M. T., Calheiros, F., Cadette, A., and Paula-Barbosa, M. M. (1992). Selective vulnerability of the hippocampal pyramidal neurons to hypothyroidism in male and female rats.J. Comp. Neurol.332501–518. [DOI] [PubMed] [Google Scholar]
  93. Maggi, A., Bettini, S., Mantero, G., and Zucchi, I. (1989). Hippocampus: A target for estrogen action in mammalian brain.Mol. Endo.31165–1170. [DOI] [PubMed] [Google Scholar]
  94. Martin, D., McNamara, J., and Nadler, J. (1992). Kindling enhances sensitivity of CA3 hippocampal pyramidal cells to NMDA.J. Neurosci.121928–1935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Mattson, M., Dou, P., and Kater, S. (1988). Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons.H. Neurosci.82087–2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Mattson, M., Cheng, B., Davis, D., Byrant, K., Lieberburg, I., and Rydel, R. (1992). Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity.J. Neurosci.12376–389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. McEwen, B. S. (1992). Re-examination of the glucocorticoid cascade hypothesis of stress and aging.Prog. Brain Res.93365–383. [DOI] [PubMed] [Google Scholar]
  98. Mendelson, S., and McEwen, B. S. (1990). Adrenalectomy increases the density of 5-HT(1A) receptors in rat hippocampus.Neuroendo. Lett.12353. [Google Scholar]
  99. Mendelson, S., and McEwen, B. S. (1991). Autoradiographic analyses of the effects of restraintinduced stress on 5-HT1A, 5-HT1C and 5-HT2 receptors in the dorsal hippocampus of male and female rats.Neuorendocrinology54454–461. [DOI] [PubMed] [Google Scholar]
  100. Mendelson, S., and McEwen, B. S. (1992a). Autoradiographic analyses of the effects of adrenalectomy and corticosterone on 5-HT1A and 5-HT1B receptors in the dorsal hippocampus and cortex of the rat.Neuroendocrinology55444–450. [DOI] [PubMed] [Google Scholar]
  101. Mendelson, S., and McEwen, B. S. (1992b). Quantitative autoradiographic analyses of the time course and reversibility of corticosterone-induced decreases in binding at 5-HT1A receptors in rat forebrain.Neuroendocrinology56881–888. [DOI] [PubMed] [Google Scholar]
  102. Mennini, T., and Miari, A. (1991). Modulation of 3H glutamate binding by serotonin in rat hippocampus: An autoradiographic study.Life Sci.49283–292. [DOI] [PubMed] [Google Scholar]
  103. Mennini, T., Mocaer, E., and Gerratini, S. (1987). Tianeptine, a selective enhancer of serotonin uptake in rate brain.Nauyn-Schmied. Arch. Pharm.336478–482. [DOI] [PubMed] [Google Scholar]
  104. Milward, E., Papadopoulos, R., Fuller, S., Moir, R., Small, D., Beyreuther, K., and Masters, C. (1992). The amyloid protein precursors of Alzheimer's disease is a mediator of the effects of nerve growth factor on neurite outgrowth.Neuron9129–137. [DOI] [PubMed] [Google Scholar]
  105. Mizoguchi, K., Kunishita, T., Chui, D.-H., and Tabira, T. (1992). Stress induced neuronal death in the hippocampus of castrated rats.Neurosci. Lett.138157–160. [DOI] [PubMed] [Google Scholar]
  106. Modney, B., and Hatton, G. (1989). Multiple synapse formation: A possible compensatory mechanism for increased cell size in rat supraoptic nucleus.J. Neuroendocrinol.121–27. [DOI] [PubMed] [Google Scholar]
  107. Morgan, J., and Curran, T. (1989). Stimulus-transcription coupling in neurons: role of cellular immediate-early genes.TINS12459–461. [DOI] [PubMed] [Google Scholar]
  108. Nadler, J., and Cuthbertson, G. (1980). Kainic acid neurotoxicity toward hippocampal formation: Dependence on specific excitatory pathways.Brain Res.19547–56. [DOI] [PubMed] [Google Scholar]
  109. Nakamura, Y., Takeda, M., Niigawa, H., Hariguchi, S., and Nishimura, T. (1992). Amyloid beta-protein precursor deposition in rat hippocampus lesioned by ibotenic acid injection.Neurosci. Lett.13695–98. [DOI] [PubMed] [Google Scholar]
  110. Nedergaard, S., Engber, T., and Flatman, J. (1987). The modulation of excitatory amino acid responses by serotonin in the cat neocortex in vitro.Cell. Mol. Neurol.7367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Nichols, N., and Finch, C. (1991). Transforming growth factor-beta1 mRNA decreases in brain in response to glucocorticoid treatment of adrenalectomized rats.Mol. Cell. Neurosci.2221–227. [DOI] [PubMed] [Google Scholar]
  112. Nitsch, R., and Frotscher, M. (1991). Maintenance of peripheral dendrites of GABAergic neurons requires specific input.Brain Res.554304–307. [DOI] [PubMed] [Google Scholar]
  113. Nitsch, R., and Frotscher, M. (1992). Reduction of posttraumatic transneuronal “early gene” activation and dendritic atrophy by the N-methyl-D-aspartate receptor antagonist MK-801.Proc. Natl. Acad. Sci.895197–5200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Ohi, K., Mikuni, M., and Takahashi, K. (1989). Stress adaptation and hypersensitivity in 5-HT neuronal systems after repeated foot shock.Pharm. Biochem. Behav.34603–608. [DOI] [PubMed] [Google Scholar]
  115. Ohno, M., Yamamoto, T., and Watanabe, S. (1991). Blockade of 5-HT2 receptors protects against impairment of working memory following transient forebrain ischemia in the rat.Neurosci. Lett.129185–188. [DOI] [PubMed] [Google Scholar]
  116. O'Keefe, J., and Handa, R. (1990). Transient elevation of estrogen receptors in the neonatal rat hippocampus.Dev. Brain Res.57119–127. [DOI] [PubMed] [Google Scholar]
  117. Olmos, G., Naftolin, F., Perez, J. Tranque, P., and Garcia-Segura, L. (1989). Synaptic remodeling in the rat arcuate nucleus during the estrous cycle.Neuroscience32663–667. [DOI] [PubMed] [Google Scholar]
  118. Packan, D., and Sapolsky, R. (1990). Glucocorticoid endangerment of the hippocampus: tissue, steroid and receptor specificity.Neuroendocrinology51613–618. [DOI] [PubMed] [Google Scholar]
  119. Paula-Barbosa, M., Andrade, J., Castedo, J., Azevedo, F., Camoes, I., Volk, B., and Tavares, M. (1989). Cell loss in cerebellum and hippocampal formation of adult rats after long-term low-protein diet.Exp. Neurol.103186–193. [DOI] [PubMed] [Google Scholar]
  120. Pearce, I., Cambray-Deakin, M., and Burgoyne, R. (1987). Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells.FEBS Let.223143–147. [DOI] [PubMed] [Google Scholar]
  121. Phillips, L., and Steward, O. (1990). Increases in mRNA for cytoskeletal proteins in the denervated neuropil of the dentate gyrus: An in situ hybridization study using riboprobes for beta-actin and beta-tubulin.Mol. Brain Res.8239–257. [DOI] [PubMed] [Google Scholar]
  122. Phillips, H., Hains, J., Laramee, G., Rosenthal, A., and Winslow, J. (1990). Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons.Science250290–293. [DOI] [PubMed] [Google Scholar]
  123. Popov, V., and Bocharova, L. (1992). Hibernation-induced structural changes in synaptic contacts between mossy fibers and hippocampal pyramidal neurons.Neuroscience4853–62. [DOI] [PubMed] [Google Scholar]
  124. Popov, V., Bocharova, L., and Bragin, A. (1992). Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation.Neuroscience4845–51. [DOI] [PubMed] [Google Scholar]
  125. Prehn, J., Backhaub, C., Karkoutly, C., Nuglisch, J., Peruche, B., Robberg, C., and Kreiglstein, J. (1991). Neuroprotective properties of 5-HT1A receptor agonists in rodent models of focal and global cerebral ischemia.Eur. J. Pharm.203213–222. [DOI] [PubMed] [Google Scholar]
  126. Rabacchi, S., Bailly, Y., Delhaye-Bouchaud, N., and Mariani, J. (1992). Involvement of the N-methyl-D-aspartate (NMDA) receptor in synapse elimination during cerebellar development.Science2561823–1825. [DOI] [PubMed] [Google Scholar]
  127. Reul, J., and Dekolet, E. R. (1985). Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation.Endocrinology1172505–2511. [DOI] [PubMed] [Google Scholar]
  128. Richter-Leven, G., and Segal, M. (1988). Serotonin releasers modulate reactivity of the rat hippocampus to afferent stimulation.94:173-176. [DOI] [PubMed]
  129. Rocamora, N., Palacios, J., and Mengod, G. (1992). Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in the rat hippocampus.Mol. Brain Res.1327–33. [DOI] [PubMed] [Google Scholar]
  130. Sanchez-Toscano, F., Sancez, M-del-M. and Garzon, J. (1991). Changes in the number of dendritic spines in the medial preoptic area during a premature long-term social isolation in rats.Neurosci. Letts.1221–3. [DOI] [PubMed] [Google Scholar]
  131. Sapolsky, R. (1986). Glucocorticoid toxicity in the hippocampus: Reversal by supplementation with brain fuels.J. Neurosci.62240–2244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Sapolsky, R. (1990). Glucocorticoids, hippocampal damage and the glutamatergic synapse.Prog. Brain Res.8613–23. [DOI] [PubMed] [Google Scholar]
  133. Sapolsky, R., and Pulsinelli, W. (1985). Glucocorticoids potentiate ischemic injury to neurons: Therapeutic implications.Science2291397–1399. [DOI] [PubMed] [Google Scholar]
  134. Sapolsky, R., Krey, L., and McEwen, B. S. (1985). Prolonged glucocorticoic exposure reduces hippocampal neuron number: Implications for aging.J. Neurosci.51222–1227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Sapolsky, R., Krey, L., and McEwen, B. S. (1986). The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis.Endocr. Rev.7284–301. [DOI] [PubMed] [Google Scholar]
  136. Sapolsky, R., Packan, D., and Vale, W. (1988). Glucocorticoid toxicity in the hippocampus: In vitro demonstration.Brain Res.453367–371. [DOI] [PubMed] [Google Scholar]
  137. Schaasfoort, E. M. C., DeBruin, L. A., and Korf, J. (1988). Mild stress stimulates rat hippocampal glucose utilization transiently via NMDA receptors, as assessed by lactography.Brain Res.45758–63. [DOI] [PubMed] [Google Scholar]
  138. Seil, F., Eckenstein, F., and Reiser, P. (1992). Induction of dendritic spine proliferation by an astrocyte secreted factor.Exp. Neurol.11785–89. [DOI] [PubMed] [Google Scholar]
  139. Seubert, P., Lee, K., and Lynch, G. (1989). Ischemia triggers NMDA receptor-linked cytoskeletal proteolysis in hippocampus.Brain Res.492366–370. [DOI] [PubMed] [Google Scholar]
  140. Sharp, F., Gonzalez, M., Hisanaga, K., Mobley, W., and Sagar, S. (1989). Induction of the c-fos gene product in rat forebrain following cortical lesions and NGF injections.Neurosci. Lett.100117–122. [DOI] [PubMed] [Google Scholar]
  141. Sheng, M., and Greenberg, M. (1990). The regulation and function of c-fos and other immediate early genes in the nervous system.Neuron4477–485. [DOI] [PubMed] [Google Scholar]
  142. Sherry, D., Vaccarino, A., Buckenham, K., and Herz, R. (1989). The hippocampal complex of food-storing birds.Brain Behav. Evol.34308–317. [DOI] [PubMed] [Google Scholar]
  143. Sherry, D., Jacobs, L., and Gaulin, S. (1992). Spatial memory and adaptive specialization of the hippocampus.TINS15299–303. [DOI] [PubMed] [Google Scholar]
  144. Siesjo, B., and Bengtsson, F. (1989). Calcium fluxes, calcium antagonists and calcium-related pathology in brain ischemia, hypoglycemia and spreading depression: A unifying hypothesis.J. Cerebr. Blood Flow Metab.9127–140. [DOI] [PubMed] [Google Scholar]
  145. Sikich, L., Hickok, J., and Todd, R. (1990). 5-HT1A receptors contro neurite branching during development.Dev. Brain Res.56269–274. [DOI] [PubMed] [Google Scholar]
  146. Skerritt, J., and Johnston, G. (1983). Inhibition of amino acid transmitter release from rat brain slices by phenytoin and related anticonvulsants.Clin. Exp. Pharm. Physiol.10527–533. [DOI] [PubMed] [Google Scholar]
  147. Sloviter, R. (1983). “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies.Brain Res. Bull.10675–697. [DOI] [PubMed] [Google Scholar]
  148. Sohn, R., and Ferrendelli, J. (1973). Inhibition of Ca++ transport into rat brain synaptosomes by diphenylhydantoin (DPH).J. Pharmacol. Exp. Ther.185272–275. [PubMed] [Google Scholar]
  149. Sonnenberg, J., Mitchelmore, C., Macgregor-Leon, P., Hempstead, J., Morgan, J., and Curran, T. (1989). Glutamate receptor agonists increase the expression of Fos, Fra, and AP-1 DNA binding activity in the mammalian brain.J. Neurosci. Res.2472–80. [DOI] [PubMed] [Google Scholar]
  150. Stanton, P., and Moskal, R. (1991). Diphenylhydantoin protects against hypoxia-induced impairment of hippocampal synaptic transmission.Brain Res.546351–354. [DOI] [PubMed] [Google Scholar]
  151. Stein, B., and Sapolsky, R. (1988). Chemical adrenalectomy reduces hippocampal damage induced by kainic acid.Brain Res.473175–180. [DOI] [PubMed] [Google Scholar]
  152. Steward, O., Davis, L., Dotti, C., Phillips, L., Rao, A., and Banker, G. (1988). Protein synthesis and processing in cytoplasmic microdomains beneath postsynaptic sites on CNS neurons. A mechanism for establishing and maintaining a mosaic postsynaptic receptive surface.Mol. Neurobiol.2227–261. [DOI] [PubMed] [Google Scholar]
  153. Sutula, T., Xiao-Xian, H., Cavazos, J., and Grayson, S. (1988). Synaptic reorganization in the hippocampus induced by abnormal functional activity.Science2391147–1150. [DOI] [PubMed] [Google Scholar]
  154. Taft, W., Clifton, G., Blair, R., and DeLorenzo, R. (1989). Phenytoin protects against ischemiaproduced neuronal cell death.Brain Res.483143–148. [DOI] [PubMed] [Google Scholar]
  155. Takeda, A., Onodera, H., Yamasaki, Y., Furukawa, K., Kogure, K., Obinata, M., and Shibahara, S. (1992). Decreased expression of neurotrophin-3 mRNA in the rat hippocampus following transient forebrain ischemia.Brain Res.569177–180. [DOI] [PubMed] [Google Scholar]
  156. Theodosis, D., and Poulain, D. (1989). Neuronal-glial and synaptic plasticity in the adult rat paraventricular nucleus.Brain Res.484361–366. [DOI] [PubMed] [Google Scholar]
  157. Torre, E., and Steward, O. (1992). Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies.J. Neurosci.12762–772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  158. Tweedle, C., and Hatton, G. (1984). Synapse formation and disappearance in adult rat supraoptic nucleus during different hydration states.Brain Res.309373–376. [DOI] [PubMed] [Google Scholar]
  159. Uno, H., Tarara, R. Else, J., Suleman, M., and Sapolsky, R. (1989). Hippocampal damage associated with prolonged and fatal stress in primates.J. Neurosci.91705–1711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. Vaccarino, F., Hayward, M., Nestler, E., Duman, R., and Tallman, J. (1992). Differential induction of immediate early genes by excitatory amino acid receptor types in primary cultures of cortical and striatal neurons.Mol. Brain Res.12233–241. [DOI] [PubMed] [Google Scholar]
  161. Virgin, C., Ha, T., Packan, D., Tombaugh, G. Yang, S., Horner, H., and Sapolsky, R. (1991). Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: Implications for glucocorticoid neurotoxicity.J. Neurochem.571422–1428. [DOI] [PubMed] [Google Scholar]
  162. Visvader, J., Sassone-Corsi, P., and Verma, I. (1988). Two adjacent promoter elements mediate nerve growth factor activation of the c-fos gene and bind distinct nuclear complexes.Proc. Natl. Acad. Sci. USA859474–9478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. Watanabe, Y., Gould, E., and McEwen, B. S. (1992a). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons.Brain Res.588341–345. [DOI] [PubMed] [Google Scholar]
  164. Watanabe, Y., Gould, E., Cameron, H., Daniels, D., and McEwen, B. S. (1992b). Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons.Hippocampus2431–435. [DOI] [PubMed] [Google Scholar]
  165. Watanabe, Y., Gould, E., Daniels, D., Cameron, H., and McEwen, B. S. (1992c). Tianeptine attenuates stress-induced morphological changes in the hippocampus.Eur. J. Pharm.588341–345. [DOI] [PubMed] [Google Scholar]
  166. Weiland, N. (1992a). Estradiol selectively regulates agonist binding sites on the N-methyl-D-aspartate receptor complex in the CA1 region of the hippocampus.Endocrinology131662–668. [DOI] [PubMed] [Google Scholar]
  167. Weiland, N. (1992b). Glutamic acid decarboxylase messenger ribonucleic acid is regulated by estradiol and progesterone in the hippocampus.Endocrinology1312697–2702. [DOI] [PubMed] [Google Scholar]
  168. Whitton, P., Sarna, G., O'Connell, M., and Curzon, G. (1991). The effect of the novel antidepressant tianeptine on the concentration of 5-hydroxytryptamine in rat hippocampal dialysates in vivo.Psychopharmacology10481–85. [DOI] [PubMed] [Google Scholar]
  169. Williams, C., and Meck, W. (1991). The organizational effects of gonadal steroids on sexually dimorphic spatial ability.Psychoneuroendocrinology16155–176. [DOI] [PubMed] [Google Scholar]
  170. Withers, G., and Greenough, W. (1989). Reach training selectively alters dendritic branching in subpopulations of layer II–III pyramids in rat motor-somatosensory forelimb cortex.Neuropsychologia2761–69. [DOI] [PubMed] [Google Scholar]
  171. Wong, M., and Moss, R. (1992). Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons.J. Neurosci.123217–3255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  172. Wong, M.-L., Weiss, S., Gold, P., Doi, S., Banerjee, S., Licinio, J., Lad, R., Post, R., and Smith, M. (1992). Induction of constitutive heat shock protein 73 mRNA in the dentate gyrus by seizures.Mol. Brain Res.1319–25. [DOI] [PubMed] [Google Scholar]
  173. Woolley, C., and McEwen, B. S. (1992). Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat.J. Neurosci.122549–2554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  174. Woolley, C., Gould, E., Frankfurt, M., and McEwen, B. S. (1990a). Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons.J. Neurosci.104035–4039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  175. Woolley, C., Gould, E., and McEwen, B. S. (1990b). Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons.Brain Res.531225–231. [DOI] [PubMed] [Google Scholar]
  176. Yaari, Y., Hamon, B., and Lux, H. (1987). Development of two types of calcium channels in cultured mammalian hippocampal neurons.Science235680–682. [DOI] [PubMed] [Google Scholar]
  177. Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., and Lindholm, D. (1990). Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors.EMBO J.93545–3550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  178. Zafra, F., Castren, E., Thoenen, H., and Lindholm, D. (1991). Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve-growth factor synthesis in hippocampal neurons.Proc. Natl. Acad. Sci. USA8810037–10041. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Cellular and Molecular Neurobiology are provided here courtesy of Springer

RESOURCES