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Structural plasticity and tianeptine: cellular and molecular targets

Published online by Cambridge University Press:  16 April 2020

B.S. McEwen ,
A.M. Magarinos  and
L.P. Reagan
B.S. McEwen*
Affiliation:
Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, New York, NY 10021, USA
A.M. Magarinos
Affiliation:
Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, New York, NY 10021, USA
L.P. Reagan
Affiliation:
Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, New York, NY 10021, USA
*
*Corresponding author: The Rockefeller University, Box 165, 1230 York Avenue, New York, NY 10021, USA. E-mail address: [email protected] (B.S. McEwen).
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Summary

The hippocampal formation, a structure involved in declarative, spatial and contextual memory, undergoes atrophy in depressive illness along with impairment in cognitive function. Animal model studies have shown that the hippocampus is a particularly sensitive and vulnerable brain region that responds to stress and stress hormones. Studies on models of stress and glucocorticoid actions reveal that the hippocampus shows a considerable degree of structural plasticity in the adult brain. Stress suppresses neurogenesis of dentate gyrus granule neurons, and repeated stress causes remodeling of dendrites in the CA3 region, a region that is particularly important in memory processing. Both forms of structural remodeling of the hippocampus are mediated by adrenal steroids working in concert with excitatory amino acids (EAA) and N-methyl-D-aspartate (NMDA) receptors. EAA and NMDA receptors are also involved in neuronal death that is caused in pyramidal neurons by seizures, head trauma, and ischemia, and alterations of calcium homeostasis that accompany age-related cognitive impairment. Tianeptine (tianeptine) is an effective antidepressant that prevents and even reverses the actions of stress and glucocorticoids on dendritic remodeling in an animal model of chronic stress. Multiple neurotransmitter systems contribute to dendritic remodeling, including EAA, serotonin, and gamma-aminobutyric acid (GABA), working synergistically with glucocorticoids. This review summarizes findings on neurochemical targets of adrenal steroid actions that may explain their role in the remodeling process. In studying these actions, we hope to better understand the molecular and cellular targets of action of tianeptine in relation to its role in influencing structural plasticity of the hippocampus.

Keywords

Excitatory amino acidDepressionHippocampusSerotoninStressTianeptine
Type
Research Article
Information
European Psychiatry , Volume 17 , Issue S3: A new pharmacology of depression: the concept of synaptic plasticity , July 2002 , pp. 318s - 330s
Copyright
Copyright Éditions scientifiques et médicales Elsevier SAS 2002

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Footnotes

To be presented at ECNP Barcelona, 5-9 October 2002, during the symposium “A new pharmacology of depression: the concept of synaptic plasticity.”

References

Aberg, MAIAberg, NDHedbacker, HOscarsson, JEriksson, PSPeripheral infusion of IGF-1 selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 2000;20:2896–2903.CrossRefGoogle ScholarPubMed
Barnes, CMcNaughton, BGoddard, GDouglas, RAdamec, RCircadian rhythm of synaptic excitability in rat and monkey central nervous system. Science 1977;197:91–92.CrossRefGoogle ScholarPubMed
Bartanusz, VAubry, JMPagliusi, SJezova, DBaffi, JKiss, JZStress-induced changes in messenger RNA levels of N-methyl-D-aspartate and AMPA receptor subunits in selected regions of the rat hippocampus and hypothalamus. Neuroscience 1995;66:247–252.CrossRefGoogle ScholarPubMed
Bengzon, JKokaia, ZElmer, ENanobashvili, AKokaia, MLindvall, OApoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 1997;94:10432–10437.Google ScholarPubMed
Bogerts, BLieberman, JAAshtair, MBilder, RMDe Greef, GLerner, Get al. Hippocampus-amygdala volumes and psychopathology in chronic schizophrenia. Biol Psychiatry 1993;33:236–246.CrossRefGoogle ScholarPubMed
Brezun, JMDaszuta, ADepletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 1999;89:999–1002.CrossRefGoogle ScholarPubMed
Cameron, HAGould, EThe control of neuronal birth and survival. In: Shaw, CA editors. Receptor dynamics in neural development, first edition. New York, NY: CRC Press 1996. p. 141–157Google Scholar
Cameron, HAGould, EDistinct populations of cells in the adult dentate gyrus undergo mitosis or apoptosis in response to adrenalectomy. J Comp Neurol 1996;369:56–63.Google ScholarPubMed
Cameron, HAMcEwen, BSGould, ERegulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995;15:4687–4692.Google ScholarPubMed
Carro, ENunez, ABusiguina, STorres-Aleman, ICirculating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000;20:2926–2933.CrossRefGoogle Scholar
Chan, PHRole of oxidants in ischemic brain damage. Stroke 1996;27:1124–1129.CrossRefGoogle ScholarPubMed
Chittajallu, RVignes, MDev, KKBarnes, JMCollingridge, GLHenley, JMRegulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 1996;379:78–81.CrossRefGoogle ScholarPubMed
Conrad, CDMagarinos, AMLeDoux, JEMcEwen, BSRepeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 1999;113:902–913.CrossRefGoogle ScholarPubMed
Dana, RCMartinez, JLEffect of adrenalectomy on the circadian rhythm of LTP. Brain Res 1984;308:392–395.CrossRefGoogle ScholarPubMed
De Kloet, ERAzmitia, ECLandfield, PWBrain corticosteroid receptors: studies on the mechanism, function, and neurotoxicity of corticosteroid action. Ann New York Acad Sci 1994;746:499.Google Scholar
DeKloet, ERVreugdenhil, EOitzl, MSJoels, MBrain corticosteroid receptor balance in health and disease. Endocr Rev 1998;19:269–301.Google Scholar
Diamond, DMBennett, MCFleshner, MRose, GMInverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 1992;2:421–430.CrossRefGoogle ScholarPubMed
Diamond, DMFleshner, MIngersoll, NRose, GMPsychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 1996;110:661–672.CrossRefGoogle ScholarPubMed
Diamond, DMFleshner, MRose, GMPsychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav Brain Res 1994;62:1–9.CrossRefGoogle ScholarPubMed
Diamond, DMFleshner, MRose, GMPsychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 1996;110:661–672.CrossRefGoogle ScholarPubMed
Dore, SKar, SQuirion, RInsulin-like growth factor I protects and rescues hippocampal neurons against β-amyloid and human amylin-induced toxicity. Proc Natl Acad Sci USA 1997;94:4772–4777.CrossRefGoogle ScholarPubMed
Dore, SKar, SRowe, WQuirion, RDistribution and levels of 〚125I〛IGF-I, 〚125I〛IGF-II and 〚125I〛insulin receptor binding sites in the hippocampus of aged memory-unimpaired and -impaired rats. Neuroscience 1997;80:1033–1040.Google Scholar
Drevets, WCOngur, DPrice, JLNeuroimaging abnormalities in the subgenual prefrontal cortex: implications for the pathophysiology of familial mood disorders. Mol Psychiatry 1998;3:220–226.Google ScholarPubMed
Drevets, WCPrice, JLSimpson, JR JrTodd, RDReich, TVannier, Met al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997;386:824–827.CrossRefGoogle ScholarPubMed
Eichenbaum, HOtto, TThe hippocampus - what does it do?. Behav Neural Biol 1992;57:2–36.Google Scholar
Flugge, GDynamics of central nervous 5-HT1A-receptors under psychosocial stress. J Neurosci 1995;15:7132–7140.CrossRefGoogle ScholarPubMed
Freund, TFBuzsaki, GInterneurons of the hippocampus. Hippocampus 1996;6:345–470.Google ScholarPubMed
Fukuzako, HFukuzako, THashiguchi, THokazono, YTakeuchi, KHirakawa, Ket al. Reduction in hippocampal formation volume is caused mainly by its shortening in chronic schizophrenia: assessment by MRI. Biol Psychiatry 1996;39:938–945.Google ScholarPubMed
Galea, LAMTanapat, PGould, EExposure to predator odor suppresses cell proliferation in the dentate gyrus of adult rats via a cholinergic mechanism. Abstr Soc Neurosci 1996;22:1196–1196 No. 474.8.1196.Google Scholar
Gleichmann, MWeller, MSchulz, JBInsulin-like growth factor-1 mediated protection from neuronal apoptosis is linked to phosphorylation of the pro-apoptotic protein BAD but not to inhibition of cytochrome c translocation in rat cerebellar neurons. Neurosci Lett 2000;282:69–72.CrossRefGoogle Scholar
Gould, ESerotonin and hippocampal neurogenesis. Neuropsychopharmacology 1999;21:465–515.CrossRefGoogle ScholarPubMed
Gould, EMcEwen, BSTanapat, PGalea, LAMFuchs, ENeurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997;17:2492–2498.CrossRefGoogle ScholarPubMed
Gould, ETanapat, PLesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 1997;80:427–436.CrossRefGoogle ScholarPubMed
Gould, ETanapat, PCameron, HAAdrenal steroids suppress granule cell death in the developing dentate gyrus through an NMDA receptor-dependent mechanism. Dev Brain Res 1997;103:91–93.CrossRefGoogle ScholarPubMed
Gould, ETanapat, PMcEwen, BSFlugge, GFuchs, EProliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 1998;95:3168–3171.Google ScholarPubMed
Gurvits, TVShenton, MEHokama, HOhta, HLasko, NBGilbertson, MWet al. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatry 1996;40:1091–1099.Google ScholarPubMed
Hayashi, YShi S-, HEsteban, JAPiccini, APoncer, J-CMalinow, RDriving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 2000;287:2262–2267.Google ScholarPubMed
Ikegaya, YSaito, HAbe, KThe basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo. Eur J Neurosci 1997;8:1833–1839.CrossRefGoogle Scholar
Islam, AAyer-LeLievre, CHeigenskold, CBogdanovic, NWinblad, BAdem, AChanges in IGF-1 receptors in the hippocampus of adult rats after long-term adrenalectomy: receptor autoradiography and in situ hybridization histochemistry. Brain Res 1998;797:342–346.CrossRefGoogle ScholarPubMed
Jacobs, BLvan Praag, HGage, FHDepression and the birth and death of brain cells. Am Sci 2000;88:340–345.Google Scholar
Jacobson, LSapolsky, RThe role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 1991;12:118–134.CrossRefGoogle ScholarPubMed
Joels, MSteroid hormones and excitability in the mammalian brain. Front Neuroendocrinol 1997;18:2–48.CrossRefGoogle ScholarPubMed
Kerr, DSHuggett, AMAbraham, WCModulation of hippocampal long-term potentiation and long-term depression by corticosteroid receptor activation. Psychobiology 1994;22:123–133.Google Scholar
Kerr, SCampbell, LApplegate, MBrodish, ALandfield, PChronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J Neurosci 1991;11:1316–1324.CrossRefGoogle ScholarPubMed
Lai, MHibberd, CJGluckman, PDSeckl, JRReduced expression of insulin-like growth factor 1 messenger RNA in the hippocampus of aged rats. Neurosci Lett 2000;288:66–70.CrossRefGoogle ScholarPubMed
Landfield, PWEldridge, JCEvolving aspects of the glucocorticoid hypothesis of brain aging: hormonal modulation of neuronal calcium homeostasis. Neurobiol Aging 1994;15:579–588.CrossRefGoogle ScholarPubMed
LeDoux, JEIn search of an emotional system in the brain: leaping from fear to emotion and consciousness. In: Gazzaniga, M editors. The cognitive neurosciences Cambridge, Mass: MIT Press; 1995. p. 1049–1061.Google Scholar
Lin, JWang, XShigenaga, MKYeo, HCMori, AAmes, BNImmobilization stress causes oxidative damage of lipid, protein, and DNA in the brain of rats. FASEB J 1996;10:1532–1538.Google Scholar
Lowy, MTGault, LYamamoto, BKAdrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J Neurochem 1993;61:1957–1960.CrossRefGoogle ScholarPubMed
Lowy, MTGault, LYamamoto, BKAdrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J Neurochem 1993;61:1957–1960.CrossRefGoogle ScholarPubMed
Lowy, MTWittenberg, LYamamoto, BKEffect of acute stress on hippocampal glutamate levels and spectrin proteolysis in young and aged rats. J Neurochem 1995;65:268–274.CrossRefGoogle Scholar
Lynch, CDLyons, DKhan, ABennett, SASonntag, WEInsulin-like growth factor-1 selectively increases glucose utilization in brains of aged animals. Endocrinology 2001;142:506–509.CrossRefGoogle ScholarPubMed
Magarinos, AMDeslandes, AMcEwen, BSEffects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 1999;371:113–122.Google ScholarPubMed
Magarinos, AMMcEwen, BSStress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995;69:83–88.CrossRefGoogle ScholarPubMed
Magarinos, AMMcEwen, BSStress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995;69:89–98.CrossRefGoogle ScholarPubMed
Magarinos, AMMcEwen, BSExperimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress. Proc Natl Acad Sci USA 2000;97:11056–11061.CrossRefGoogle ScholarPubMed
Magarinos, AMMcEwen, BSFlugge, GFuchs, EChronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 1996;16:3534–3540.CrossRefGoogle ScholarPubMed
Magarinos, AMOrchinik, MMcEwen, BSMorphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res 1998;809:314–318.CrossRefGoogle ScholarPubMed
Magarinos, AMVerdugo Garcia, JMMcEwen, BSChronic restraint stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci USA 1997;94:14002–14008.CrossRefGoogle ScholarPubMed
Maren, SProperties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory. Neurobiol Learn Mem 1995;63:1–18.CrossRefGoogle ScholarPubMed
Markowska, ALMooney, MSonntag, WEInsulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 1998;87:559–569.CrossRefGoogle ScholarPubMed
Mason, JLSuzuki, KChaplin, DDMatsushima, GKInterleukin-1 promotes repair of the CNS. J Neurosci 2001;21:7046–7052.CrossRefGoogle ScholarPubMed
McCord, JOxygen-derived free radicals in postischemic tissue injury. N Engl J M 1985;312:159–163.Google ScholarPubMed
McEwen, BSAlbeck, DCameron, HChao, HMGould, EHastings, Net al. Stress and the Brain: A paradoxical role for adrenal steroids. In: Litwack, GD editors. Vitamins and hormones, vol. 51. San Diego, Calif: Academic Press Inc 1995. p. 371–402.Google Scholar
McEwen, BSWeiss, JSchwartz, LSelective retention of corticosterone by limbic structures in rat brain. Nature 1968;220:911–912.CrossRefGoogle ScholarPubMed
McKittrick, CRMagarinos, AMBlanchard, DCBlanchard, RJMcEwen, BSSakai, RRChronic social stress decreases binding to 5-HT transporter sites and reduces dendritic arbors in CA3 of hippocampus. Abstr Soc Neurosci 1996;22:809–809 18.2060.Google Scholar
McKittrick, CRMagarinos, AMBlanchard, DCBlanchard, RJMcEwen, BSSakai, RRChronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000;36:85–94.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
McKittrick, CRMcEwen, BSRegulation of serotonergic function in the CNS by steroid hormones and stress. In: Stone, TW editors. CNS neurotransmitters and neuromodulators neuroactive steroids. New York, NY: CRC Press; 1996. p. 37–76.Google Scholar
Mennini, TMiari, AModulation of 3H-glutamate binding by serotonin in rat hippocampus: an autoradiographic study. Life Sci 1991;49:283–292.CrossRefGoogle Scholar
Moghaddam, BBoliano, MLStein-Behrens, BSapolsky, RGlucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res 1994;655:251–254.Google ScholarPubMed
Noguchi, SHigashi, KKawamura, MA posssible role of the β-subunit of (Na,K)-ATPase in facilitating correct assembly of the β-subunit into the membrane. J Biol Chem 1990;265:5991–5995.Google Scholar
Norris, CMHalpain, SFoster, TCReversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. J Neurosci 1998;18:3171–3179.Google ScholarPubMed
OˈKusky, JRYe, PDˈErcole, AJInsulin-like growth factor-1 promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J Neurosci 2000;20:8435–8442.CrossRefGoogle ScholarPubMed
Ongur, DDrevets, WCPrice, JLGlial loss in the subgenual prefrontal cortex in familial mood disorders. Abstr Soc Neurosci 1998;24:386–386 13.990.Google Scholar
Orchinik, MCarroll, SSLi Y-, HMcEwen, BSWeiland, NGHeterogeneity of hippocampal GABAA receptors: regulation by corticosterone. J Neurosci 2001;21:330–339.CrossRefGoogle Scholar
Orchinik, MWeiland, NGMcEwen, BSAdrenalectomy selectively regulates GABAa receptor subunit expression in the hippocampus. Mol Cell Neurosci 1994;5:451–458.CrossRefGoogle ScholarPubMed
Parent, JMYu, TWLeibowitz, RTGeschwind, DHSloviter, RSLowenstein, DHDentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997;17:3727–3738.CrossRefGoogle ScholarPubMed
Pavlides, CKimura, AMagarinos, AMMcEwen, BSType I adrenal steroid receptors prolong hippocampal long-term potentiation. NeuroReport 1994;5:2673–2677.CrossRefGoogle ScholarPubMed
Pavlides, CKimura, AMagarinos, AMMcEwen, BSHippocampal homosynaptic long-term depression/depotentiation induced by adrenal steroids. Neuroscience 1995;68:379–385.CrossRefGoogle ScholarPubMed
Pavlides, COgawa, SKimura, AMcEwen, BSRole of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices. Brain Res 1996;738:229–235.CrossRefGoogle ScholarPubMed
Pavlides, CWatanabe, YMagarinos, AMMcEwen, BSOpposing role of adrenal steroid type I and type II receptors in hippocampal long-term potentiation. Neuroscience 1995;68:387–394.CrossRefGoogle Scholar
Phillips, RGLeDoux, JEDifferential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992;106:274–285.CrossRefGoogle ScholarPubMed
Porter, NMThibault, OThibault, VChen K-, CLandfield, PWCalcium channel density and hippocampal cell death with age in long-term culture. J Neurosci 1997;17:5629–5639.CrossRefGoogle ScholarPubMed
Pulford, BEIshii, DNUptake of circulating insulin-like growth factors (IGFs) into cerebrospinal fluid appears to be independent of the IGF receptors as well as IGF-binding proteins. Endocrinology 2001;142:213–220.CrossRefGoogle ScholarPubMed
Radley, JJJacobs, BLTanapat, PGould, EBlockade of 5-HT1A receptors prevents hippocampal granule cell genesis during and after pilocarpine-induced status epilepticus. Abstr Soc Neurosci 1998;24:796–796 5.1992.Google Scholar
Raghavendra Rao, VLDogan, ATodd, KGBowen, KKKim, B-TRothstein, JDet al. Antisense knockdown of the glial glutamate transporter GLT-1, but not the neuronal glutamate transporter EAAC1, exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J Neurosci 2001;21:1876–1883.Google Scholar
Rahmann, SNeumann, RSActivation of 5-HT2 receptors facilitates depolarization of neocortical neurons by N-methyl-D-aspartate. Eur J Pharmacol 1993;231:347–354.CrossRefGoogle Scholar
Rajkowska, GPostmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol Psychiatry 2000;48:766–777.CrossRefGoogle ScholarPubMed
Rajkowska, GMiguel-Hidalgo, JJWei, JDilley, GPittman, SDMeltzer, HYet al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999;45:1085–1098.CrossRefGoogle ScholarPubMed
Rapp, PRGallagher, MPreserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci USA 1996;93:9926–9930.CrossRefGoogle ScholarPubMed
Rasmussen, TSchliemann, TSorensen, JCZimmer, JWest, MJMemory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol Aging 1996;14:143–147.Google Scholar
Sanchez, MMYoung, LJPlotsky, PMInsel, TRDistribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J Neurosci 2000;20:4657–4668.Google ScholarPubMed
Sapolsky, RStress, the aging brain and the mechanisms of neuron death. Cambridge, Mass: MIT Press; 1992. p. 1–423Google Scholar
Sheline, YIGado, MHPrice, JLAmygdala core nuclei volumes are decreased in recurrent major depression. NeuroReport 1998;9:2023–2028.CrossRefGoogle ScholarPubMed
Sheline, YISanghavi, MMintun, MAGado, MHDepression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 1999;19:5034–5043.Google Scholar
Sheline, YIWang, PWGado, MHCsernansky, JCVannier, MWHippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 1996;93:3908–3913.CrossRefGoogle ScholarPubMed
Sousa, NLukoyanov, NVMadeira, MDAlmeida, OFXPaula-Barbosa, MMReorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 2000;97:253–266.CrossRefGoogle ScholarPubMed
Starkman, MGebarski, SBerent, SSchteingart, DHippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol Psychiatry 1992;32:756–765.CrossRefGoogle ScholarPubMed
Starkman, MNGiordani, BGebrski, SSBerent, SSchork, MASchteingart, DEDecrease in cortisol reverses human hippocampal atrophy following treatment of Cushingˈs disease. Biol Psychiatry 1999;46:1595–1602.CrossRefGoogle ScholarPubMed
Sugaya, KChouinard, MGreene, RRobbins, MPersonett, DKent, Cet al. Molecular indices of neuronal and glial plasticity in the hippocampal formation in a rodent model of age-induced spatial learning impairment. J Neurosci 1996;16:3427–3443.CrossRefGoogle Scholar
Takadera, TMatsuda, IOhyashiki, TApoptotic cell death and caspase-3 activation induced by N-methyl-D-aspartate receptor antagonists and their prevention by insulin-like growth factor I. J Neurochem 1999;73:548–556.CrossRefGoogle ScholarPubMed
Tanaka, KWatase, KManabe, TYamada, KWatanabe, MTakahashi, Ket al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 1997;276:1699–1702.CrossRefGoogle ScholarPubMed
Thorlin, TRoginski, RSChoudhury, KNilsson, MRonnback, LHansson, Eet al. Regulation of the glial glutamate transporter GLT-1 by glutamate and δ-opioid receptor stimulation. FEBS Lett 1998;425:453–459.CrossRefGoogle ScholarPubMed
Trejo, JLCarro, ETorres-Aleman, ICirculating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001;21:1628–1634.CrossRefGoogle ScholarPubMed
van Praag, HKempermann, GGage, FHRunning increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neurosci 1999;2:266–270.CrossRefGoogle ScholarPubMed
Wagstaff, AJOrmrod, DSpencer, CMTianeptine. A review of its use in depressive disorders. CNS Drugs 2001;15:231–259.CrossRefGoogle ScholarPubMed
Watanabe, YGould, ECameron, HDaniels, DMcEwen, BSStress and antidepressant effects on hippocampus. Eur J Pharmacol 1992;222:157–162.CrossRefGoogle ScholarPubMed
Watanabe, YGould, ECameron, HADaniels, DCMcEwen, BSPhenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 1992;2:431–436.CrossRefGoogle ScholarPubMed
Watanabe, YGould, EDaniels, DCameron, HMcEwen, BSTianeptine attenuates stress-induced morphological changes in the hippocampus. Eur J Pharmacol 1992;222:157–162.CrossRefGoogle ScholarPubMed
Watanabe, YGould, EMcEwen, BSStress induces atrophy of apical dendrites of hippocampus CA3 pyramidal neurons. Brain Res 1992;588:341–344.CrossRefGoogle Scholar
Watanabe, YWeiland, NGMcEwen, BSEffects of adrenal steroid manipulations and repeated restraint stress on dynorphin mRNA levels and excitatory amino acid receptor binding in hippocampus. Brain Res 1995;680:217–225.CrossRefGoogle ScholarPubMed
Weiland, NGOrchinik, MMcEwen, BSCorticosterone regulates mRNA levels of specific subunits of the NMDA receptor in the hippocampus but not in cortex of rats. Abstr Soc Neurosci 1995;21:502–502 No.207.12.Google Scholar
Weiland, NGOrchinik, MTanapat, PChronic corticosterone treatment induces parallel changes in N-methyl-D-aspartate receptor subunit messenger RNA levels and antagonist binding sites in the hippocampus. Neuroscience 1997;78:653–662.CrossRefGoogle ScholarPubMed
Woolley, CSGould, EMcEwen, BSExposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990;531:225–231.CrossRefGoogle ScholarPubMed
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