Long-Term Effects of Brief Acute Stress on Cellular Signaling and Hippocampal LTP
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In a previous study, we reported that a brief exposure to swim stress transforms an electrically induced, protein synthesis-independent early long-term potentiation (early LTP) into a protein synthesis-dependent late LTP [“reinforcement of LTP” in the hippocampal dentate gyrus (DG)] (Korz and Frey, 2003). This transformation depends on activation of mineralocorticoid receptors (MRs) by corticosterone, and on intact basolateral amygdala (BLA) function. Here, we demonstrate that a brief swim experience results in lasting changes in levels of hippocampal cellular signaling molecules that are known to be involved in the induction of late LTP. Within the DG, MRs were rapidly upregulated, whereas glucocorticoid receptor (GR) levels were elevated with a 3 h delay. Levels of phosphorylated mitogen-activated protein kinase 2 (pMAPK2) and p38 MAPK, as well as phosphorylated calcium/calmodulin-dependent protein kinase II (pCaMKII) were enhanced shortly after swim stress and remained elevated until 24 h, whereas levels of phosphorylated cAMP response element-binding protein (pCREB) remained unchanged. MR and GR were upregulated with a longer delay within the CA1 region, whereas levels of pMAPK2 and p38MAPK were rapidly increased, but the former returned to basal levels after 3 h. Levels of pCREB and pCaMKII were maintained in an enhanced state after swim stress. DG-LTP reinforcement requires a serotonergic but not dopaminergic heterosynaptic receptor activation that probably mediates the BLA-dependent modulation of LTP under stress. Thus, molecular alterations induced by specific stress resemble late LTP-related molecular changes. These changes, in interaction with stress-specific heterosynaptic processes, may support the transformation of early LTP into late LTP. The results contribute to the understanding of the rapid consolidation of cellular and possibly systemic memories triggered by stress.
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Brief stress transforms protein synthesis-independent LTP into a long-lasting protein synthesis-dependent form of LTP, via activation of mineralocorticoid (MR) receptors.
“Ahmed et al. [209] demonstrated that brief stress transforms protein synthesis-independent LTP into a long-lasting protein synthesis-dependent form of LTP, via activation of mineralocorticoid (MR) receptors.”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Ahmed et al. [209]
The onset of an emotional experience activates endogenous forms of neuroplasticity in the hippocampus for a period of seconds to minutes, which is revealed as an enhancement of LTP when tetanizing stimulation occurs in this narrow-time window.
“According to the temporal dynamics model, the onset of an emotional experience activates endogenous forms of neuroplasticity in the hippocampus for a period of seconds to minutes, which is revealed as an enhancement of LTP when tetanizing stimulation occurs in this narrow-time window (Ahmed et al. [209]; Reymann and Frey [242]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Ahmed et al. [209]
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Stress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621 · see citing works
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860 · see citing works
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · see citing works
Sweatt, J. D. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00054.x · Cited by 1,131 · see citing works
Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory
Kelleher, R. J., Govindarajan, A., Jung, H.-Y., Kang, H., & Tonegawa, S. (2004) · Cell · doi:10.1016/s0092-8674(04)00115-1 · Cited by 845 · see citing works
Brain corticosteroid receptor balance and homeostatic control
de Kloet, E. R. (1991) · Frontiers in Neuroendocrinology · Cited by 842 · see citing works
Translational Regulatory Mechanisms in Persistent Forms of Synaptic Plasticity
Kelleher, R. J., Govindarajan, A., & Tonegawa, S. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.013 · Cited by 592 · see citing works
The neuronal mineralocorticoid eeceptor as a mediator of glucocorticoid response
Arriza, J. L., Simerly, R. B., Swanson, L. W., & Evans, R. M. (1988) · Neuron · doi:10.1016/0896-6273(88)90136-5 · Cited by 591 · see citing works
Persistent protein kinase activity underlying long-term potentiation
Malinow, R., Madison, D. V., & Tsien, R. W. (1988) · Nature · doi:10.1038/335820a0 · Cited by 552 · see citing works
Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus
Shors, T. J., Seib, T. B., Levine, S., & Thompson, R. F. (1989) · Science · doi:10.1126/science.2704997 · Cited by 458 · see citing works
Goldstein, L. E., Rasmusson, A. M., Bunney, B. S., & Roth, R. H. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-15-04787.1996 · Cited by 387 · see citing works
Dopaminergic innervation of the rat prefrontal cortex: A fluorescence histochemical study
Berger, B., Thierry, A. M., Tassin, J., & Doyennette‐Moyne, M. (1976) · Brain Research · doi:10.1016/0006-8993(76)90078-0 · Cited by 375 · see citing works
Roozendaal, B., McReynolds, J. R., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4664-03.2004 · Cited by 327 · see citing works
Serotonin, stress and corticoids
Chaouloff, F. (2000) · Journal of Psychopharmacology · doi:10.1177/026988110001400203 · Cited by 315 · see citing works
Dopaminergic Innervation of the Amygdala Is Highly Responsive to Stress
Inglis, F., & Moghaddam, B. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0721088.x · Cited by 310 · see citing works
Kato, A., Ozawa, F., Saitoh, Y., Hirai, K., & Inokuchi, K. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00775-8 · Cited by 298 · see citing works
Trapp, T., Rupprecht, R., Castrén, M. L., Reul, J. M. H. M., & Holsboer, F. (1994) · Neuron · doi:10.1016/0896-6273(94)90431-6 · Cited by 291 · see citing works
de Kloet, E. R., Meijer, O. C., Nicola, A. F. D., Rijk, R. H. D., & Joëls, M. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.02.003 · Cited by 279 · see citing works
Frey, S., Bergado, J. A., Seidenbecher, T., Pape, H., & Frey, J. U. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-03697.2001 · Cited by 266 · see citing works
Self-citationInoue, T., Tsuchiya, K., & Koyama, T. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90243-7 · Cited by 262 · see citing works
The role of immediate early genes in the stabilization of long-term potentiation
Abraham, W. C., Dragunow, M., & Tate, W. P. (1991) · Molecular Neurobiology · doi:10.1007/bf02935553 · Cited by 254 · see citing works
Rosenkranz, J. A., & Grace, A. A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-11027.1999 · Cited by 253 · see citing works
The MAPK pathway and Egr-1 mediate stress-related behavioral effects of glucocorticoids
Revest, J., Blasi, F. D., Kitchener, P., Rougé‐Pont, F., Desmedt, A., Turiault, M., Tronche, F., & Piazza, P. V. (2005) · Nature Neuroscience · doi:10.1038/nn1441 · Cited by 236 · see citing works
Gesing, A., Bilang‐Bleuel, A., Droste, S. K., Linthorst, A. C. E., Holsboer, F., & Reul, J. M. H. M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-13-04822.2001 · Cited by 211 · see citing works
Kirby, L. G., Chou-Green, J. M., Davis, K., & Lucki, I. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00287-4 · Cited by 201 · see citing works
Acute Stress Rapidly and Persistently Enhances Memory Formation in the Male Rat
Shors, T. J. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3956 · Cited by 182 · see citing works
Properties and Mechanisms of LTP Maintenance
Abraham, W. C., & Williams, J. M. (2003) · The Neuroscientist · doi:10.1177/1073858403259119 · Cited by 178 · see citing works
Corticosteroid actions in hippocampus require DNA binding of glucocorticoid receptor homodimers
Karst, H., Karten, Y. J. G., Reichardt, H. M., de Kloet, E. R., Schütz, G., & Joëls, M. (2000) · Nature Neuroscience · doi:10.1038/79910 · Cited by 171 · see citing works
Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms
Hevroni, D., Rattner, A., Bundman, M. C., Lederfein, D., Gabarah, A., Mangelus, M., Silverman, M. A., Kedar, H., Naor, C., Kornuc, M., et al. (1998) · Journal of Molecular Neuroscience · doi:10.1007/bf02737120 · Cited by 170 · see citing works
Yang, C., Huang, C., & Hsu, K. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3968-04.2004 · Cited by 166 · see citing works
Retana‐Márquez, S., Bonilla‐Jaime, H., Vázquez-Palacios, G., Domı́nguez-Salazar, E., Martínez-García, R., & Velázquez‐Moctezuma, J. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00017-3 · Cited by 164 · see citing works
Activation of Erk and JNK MAPK pathways by acute swim stress in rat brain regions
Shen, C., Tsimberg, Y., Salvadore, C., & Meller, E. (2004) · BMC Neuroscience · doi:10.1186/1471-2202-5-36 · Cited by 161 · see citing works
Korz, V., & Frey, J. U. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-19-07281.2003 · Cited by 155 · see citing works
Self-citationSeidenbecher, T., Reymann, K. G., & Balschun, D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1494 · Cited by 154 · see citing works
Straube, T., Korz, V., Balschun, D., & Frey, J. U. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049452 · Cited by 152 · see citing works
Self-citationLinthorst, A. C. E., Peñalva, R. G., Flachskamm, C., Holsboer, F., & Reul, J. M. H. M. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02400.x · Cited by 142 · see citing works
Garza, R. D. L., & Mahoney, J. J. (2004) · Brain Research · doi:10.1016/j.brainres.2004.06.052 · Cited by 131 · see citing works
Bilang‐Bleuel, A., Rech, J., Carli, S. D., Holsboer, F., & Reul, J. M. H. M. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01934.x · Cited by 130 · see citing works
Yokoyama, M., Suzuki, E., Sato, T., Maruta, S., Watanabe, S., & Miyaoka, H. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2004.12.047 · Cited by 128 · see citing works
Rodríguez, J. J., Davies, H. A., Silva, A. T., De Souza, I. E. J., Peddie, C. J., Colyer, F. M., Lancashire, C. L., Fine, A., Errington, M. L., Bliss, T. V. P., et al. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04068.x · Cited by 113 · see citing works
Shors, T. J., & Dryver, E. T. (1994) · Brain Research · doi:10.1016/0006-8993(94)90777-3 · Cited by 111 · see citing works
Ahmed, T., & FREY, J. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.04.018 · Cited by 110 · see citing works
Self-citationBudziszewska, B., Jaworska-Feil, L., Kajta, M., & Lasoń, W. (2000) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703445 · Cited by 108 · see citing works
French, P. J., O'Connor, V. M., Jones, M. W., Davis, S., Errington, M. L., Voss, K. L., Truchet, B., Wotjak, C. T., Stean, T., Doyère, V., et al. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01467.x · Cited by 103 · see citing works
Sananbenesi, F., Fischer, A., Schrick, C., Spiess, J., & Radulović, J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-36-11436.2003 · Cited by 94 · see citing works
Varying responses to the rat forced-swim test under diurnal and nocturnal conditions
Kelliher, P., Connor, T. J., Harkin, A., Sánchez, C., Kelly, J. P., & Leonard, B. E. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00213-4 · Cited by 91 · see citing works
Lai, M., McCormick, J. A., Chapman, K. E., Kelly, P. A. T., Seckl, J. R., & Yau, J. L. W. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00038-1 · Cited by 74 · see citing works
Navakkode, S., Sajikumar, S., & Frey, J. U. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2443-05.2005 · Cited by 68 · see citing works
Self-citationLégrádi, G., Holzer, D., Kapcala, L. P., & Lechan, R. M. (2008) · Neuroendocrinology · doi:10.1159/000127224 · Cited by 68 · see citing works
Regulated expression of an actin‐associated protein, synaptopodin, during long‐term potentiation
Yamazaki, M., Matsuo, R., Fukazawa, Y., Ozawa, F., & Inokuchi, K. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00552.x · Cited by 67 · see citing works
Popoli, M., Vocaturo, C., Pérez, J., Smeraldi, E., & Racagni, G. (1995) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)10514-2 · Cited by 59 · see citing works
Reboxetine attenuates forced swim test-induced behavioural and neurochemical alterations in the rat
Connor, T. J., Kelliher, P., Harkin, A., Kelly, J. P., & Leonard, B. E. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00492-6 · Cited by 58 · see citing works
Korz, V., & Frey, J. U. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0910-05.2005 · Cited by 58 · see citing works
Self-citationIgaz, L. M., Bekinschtein, P., Izquierdo, I., & Medina, J. H. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.08.016 · Cited by 55 · see citing works
Hügin-Flores, M. E., Steimer, T., Aubert, M., & Schulz, P. (2004) · Neuroendocrinology · doi:10.1159/000078099 · Cited by 55 · see citing works
Schiapparelli, L., Rı́o, J. D., & Frechilla, D. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03193.x · Cited by 47 · see citing works
Role of Hippocampal CaMKII in Serotonin 5-HT1A Receptor-Mediated Learning Deficit in Rats
Moyano, S., Rı́o, J. D., & Frechilla, D. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300504 · Cited by 46 · see citing works
Davis, S., Salin, H., Helme-Guizon, A., Dumas, S., Stéphan, A., Corbex, M. A., Mallet, J. J., & Laroche, S. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00193.x · Cited by 39 · see citing works
Leal, A. M. O., & Moreira, A. C. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1321 · Cited by 38 · see citing works
Racca, S., Spaccamiglio, A., Esculapio, P., Abbadessa, G., Cangemi, L., DiCarlo, F., & Portaleone, P. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.06.014 · Cited by 37 · see citing works
Hypothalamic and Hippocampal Release of Serotonin in Rats Bred for Hyper- or Hypo-anxiety
Umriukhin, A., Wigger, A., Singewald, N., & Landgraf, R. (2002) · Stress · doi:10.1080/1025389021000061200 · Cited by 34 · see citing works
Ishikawa, M., Ohdo, S., Watanabe, H., Hara, C., & Ogawa, N. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00192-8 · Cited by 31 · see citing works
Bergado, J. A., Almaguer‐Melian, W., Kostenko, S., Frey, S., & Frey, J. U. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00943-1 · Cited by 27 · see citing works
Self-citationRichter‐Levin, G., Greenberger, V., & Segal, M. (1994) · Brain Research · doi:10.1016/0006-8993(94)90911-3 · Cited by 25 · see citing works
de Macedo, C. E. A., Martinez, R. C. R., Silva, M. A. D. S., & Brandão, M. L. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03939.x · Cited by 23 · see citing works
Ahmed, T., Frey, S., & Frey, J. U. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.01.005 · Cited by 23 · see citing works
Self-citationTranscriptional induction of rat mineralocorticoid receptor gene in neurones by corticosteroids
Castrén, M. L., Trapp, T., Berninger, B., Ċastrén, E., & Holsboer, F. (1995) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0140285 · Cited by 22 · see citing works
Zandieh‐Doulabi, B., Schiphorst, M. P.-T., Kalsbeek, A., Fliers, E., Bakker, O., & Wiersinga, W. M. (2003) · Endocrinology · doi:10.1210/en.2003-0791 · Cited by 21 · see citing works
Corticosteroid Effects on Serotonin Responses in Granule Cells of the Rat Dentate Gyrus
Karten, Y. J. G., Stienstra, C. M., & Joëls, M. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00616.x · Cited by 18 · see citing works
Budziszewska, B., Siwanowicz, J., & Przegaliński, E. (1996) · PubMed · Cited by 4 · see citing works
Flagged first, then by citations
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Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795 · see citing works
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“[209]; Lemon and Manahan-Vaughan [249]), and norepinephrine (Gray and Johnston [250]; Hopkins and Johnston [251]; Katsuki et al.”
BackgroundDynorphin, stress, and depression
Knoll, A. T., & Carlezon, W. A. (2010) · Brain Research · doi:10.1016/j.brainres.2009.09.074 · Cited by 465 · see citing works
Joëls, M., Sarabdjitsingh, R. A., & Karst, H. (2012) · Pharmacological Reviews · doi:10.1124/pr.112.005892 · Cited by 425 · see citing works
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381 · see citing works
Calcium homeostasis and modulation of synaptic plasticity in the aged brain
Foster, T. C. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00283.x · Cited by 303 · see citing works
Stress-Induced p38 Mitogen-Activated Protein Kinase Activation Mediates κ-Opioid-Dependent Dysphoria
Bruchas, M. R., Land, B. B., Aita, M., Xu, M., Barot, S. K., Li, S., & Chavkin, C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3769-07.2007 · Cited by 282 · see citing works
Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memoryPreprint
O’Carroll, C., Martin, S. J., Sandin, J., Frenguelli, B. G., & Morris, R. G. M. (2006) · Learning & Memory · doi:10.1101/lm.321006 · Cited by 237 · see citing works
Neuroactive steroids: State of the art and new perspectives
Melcangi, R. C., García‐Segura, L. M., & Mensah‐Nyagan, A. G. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7403-5 · Cited by 232 · see citing works
Maggio, N., & Segal, M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0155-07.2007 · Cited by 230 · see citing works
Stress, the hippocampus, and epilepsy
Joëls, M. (2008) · Epilepsia · doi:10.1111/j.1528-1167.2008.01902.x · Cited by 221 · see citing works
Chandramohan, Y., Droste, S. K., Arthur, J. S. C., & Reul, J. M. H. M. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06230.x · Cited by 180 · see citing works
Glucocorticoids act on glutamatergic pathways to affect memory processes
Sandi, C. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.01.006 · Cited by 162 · see citing works
Antistress Effect of TRPV1 Channel on Synaptic Plasticity and Spatial Memory
Li, H.-B., Mao, R., Zhang, J., Yang, Y., Cao, J., & Xu, L. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.02.020 · Cited by 160 · see citing works
Hagena, H., Hansen, N., & Manahan‐Vaughan, D. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv330 · Cited by 163 · see citing works
Synaptic Plasticity, Metaplasticity and Depression
Vose, L. R., & Stanton, P. K. (2016) · Current Neuropharmacology · doi:10.2174/1570159x14666160202121111 · Cited by 127 · see citing works
Stress exacerbates neuropathic pain via glucocorticoid and NMDA receptor activation
Alexander, J., DeVries, A. C., Kigerl, K. A., Dahlman, J. M., & Popovich, P. G. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.04.001 · Cited by 135 · see citing works
New aspects of rapid aldosterone signaling
Großmann, C., & Gekle, M. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.02.005 · Cited by 124 · see citing works
Adamec, R. E., Muir, C. A., Grimes, M. T., & Pearcey, K. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.001 · Cited by 114 · see citing works
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Palagini, L., Biber, K. P. H., & Riemann, D. W. (2013) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2013.05.002 · Cited by 113 · see citing works
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Joëls, M., Krugers, H. J., & Karst, H. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)67001-0 · Cited by 109 · see citing works
Zoladz, P. R., Clark, B., Warnecke, A., Smith, L., Tabar, J., & Talbot, J. N. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.01.016 · Cited by 102 · see citing works
Bruchas, M. R., Xu, M., & Chavkin, C. (2008) · Neuroreport · doi:10.1097/wnr.0b013e32830dd655 · Cited by 83 · see citing works
Mannironi, C., Camon, J., Vito, F. D., Biundo, A., Stefano, M. E. D., Persiconi, I., Bozzoni, I., Fragapane, P., Mele, A., & Presutti, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073385 · Cited by 77 · see citing works
Barco, Á., de Armentia, M. L., & Alarcón, J. M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.01.002 · Cited by 77 · see citing works
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Multiomic profiling of the acute stress response in the mouse hippocampus
von Ziegler, L., Floriou‐Servou, A., Waag, R., Gupta, R. R. D., Sturman, O., Gapp, K., Maat, C. A., Kockmann, T., Lin, H.-Y., Duss, S. N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29367-5 · Cited by 66 · see citing works
Abrari, K., Rashidy‐Pour, A., Semnanian, S., & Fathollahi, Y. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.10.008 · Cited by 68 · see citing works
Role of corticosteroid hormones in the dentate gyrus
Joëls, M. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63021-0 · Cited by 67 · see citing works
Hypothesized mechanisms through which acute exercise influences episodic memory
Loprinzi, P. D., Ponce, P., & Frith, E. (2018) · Physiology International · doi:10.1556/2060.105.2018.4.28 · Cited by 67 · see citing works
Gruss, M., Braun, K., Frey, J. U., & Korz, V. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2007.12.033 · Cited by 64 · see citing works
Self-citationRiedemann, T., Patchev, A. V., Cho, K., & Almeida, O. F. X. (2010) · Molecular Brain · doi:10.1186/1756-6606-3-2 · Cited by 62 · see citing works
Wang, C., & Wang, S. (2009) · Synapse · doi:10.1002/syn.20654 · Cited by 59 · see citing works
Tse, Y. C., Bagot, R. C., Hutter, J. A., Wong, A. S., & Wong, T. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027215 · Cited by 57 · see citing works
Hagena, H., & Manahan‐Vaughan, D. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0229 · Cited by 54 · see citing works
Chewing ameliorates stress-induced suppression of hippocampal long-term potentiation
Ono, Y., Kataoka, T., Miyake, S., Cheng, S., Tachibana, A., Sasaguri, K., & Onozuka, M. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.057 · Cited by 53 · see citing works
Ferguson, D., & Sapolsky, R. M. (2008) · Hippocampus · doi:10.1002/hipo.20467 · Cited by 51 · see citing works
The dose makes the poison: From glutamate-mediated neurogenesis to neuronal atrophy and depression
Rubio-Casillas, A., & Fernández-Guasti, A. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0066 · Cited by 49 · see citing works
Lerch, J. K., Alexander, J., Madalena, K. M., Motti, D., Quach, T., Dhamija, A., Zha, A. M., Gensel, J. C., Marketon, J. I. W., Lemmon, V., et al. (2017) · eNeuro · doi:10.1523/eneuro.0246-17.2017 · Cited by 49 · see citing works
Modulating role of serotonergic signaling in sleep and memory
Vaseghi, S., Arjmandi-Rad, S., Eskandari, M., Ebrahimnejad, M., Kholghi, G., & Zarrindast, M. (2021) · Pharmacological Reports · doi:10.1007/s43440-021-00339-8 · Cited by 49 · see citing works
Chen, C., Yang, C., Huang, C., & Hsu, K. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.33 · Cited by 49 · see citing works
Enhancing Cognition after Stress with Gene Therapy
Nicholas, A. C., Munhoz, C. D., Ferguson, D., Chappell-Campbell, L., & Sapolsky, R. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3122-06.2006 · Cited by 45 · see citing works
Martel, G., Blanchard, J., Mons, N. E., Gastambide, F., Micheau, J., & Guillou, J.-L. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.004 · Cited by 44 · see citing works
Role of Stress, Depression, and Aging in Cognitive Decline and Alzheimer’s Disease
Daulatzai, M. A. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_350 · Cited by 42 · see citing works
Sarabdjitsingh, R. A., Kofink, D., Karst, H., de Kloet, E. R., & Joëls, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042143 · Cited by 39 · see citing works
Active place avoidance is no more stressful than unreinforced exploration of a familiar environment
Lesburguères, E., Sparks, F. T., O’Reilly, K. C., & Fenton, A. A. (2016) · Hippocampus · doi:10.1002/hipo.22666 · Cited by 38 · see citing works
Zoladz, P. R., & Diamond, D. M. (2008) · Dose-Response · doi:10.2203/dose-response.08-015.zoladz · Cited by 37 · see citing works
Korz, V., & Frey, J. U. (2007) · Learning & Memory · doi:10.1101/lm.459807 · Cited by 37 · see citing works
Self-citationLlorens-Martı́n, M., & Trejo, J. L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028376 · Cited by 36 · see citing works
Fasting induces a form of autonomic synaptic plasticity that prevents hypoglycemia
Wang, M., Wang, Q., & Whim, M. D. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517275113 · Cited by 36 · see citing works
Temporal modulation of hippocampal excitatory transmission by corticosteroids and stress
Chaouloff, F., & Groc, L. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.004 · Cited by 36 · see citing works
Li, Z., & Richter‐Levin, G. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00021 · Cited by 35 · see citing works
Cellular mechanisms of long-term depression induced by noradrenaline in rat prefrontal neurons
Marzo, A., Bai, J., Caboche, J., Vanhoutte, P., & Otani, S. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.046 · Cited by 34 · see citing works
Boxelaere, M. V., Clements, J., Callaerts, P., D’Hooge, R., & Callaerts‐Vegh, Z. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188537 · Cited by 31 · see citing works
Wang, H., Meyer, K., & Korz, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.06.004 · Cited by 28 · see citing works
Self-citationLoprinzi, P. D. (2019) · OBM Neurobiology · doi:10.21926/obm.neurobiol.1902026 · Cited by 26 · see citing works
Effects of single swim stress on changes in TRPV1-mediated plasticity in the amygdala
Kulisch, C., & Albrecht, D. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.09.003 · Cited by 24 · see citing works
Epinephrine converts long‐term potentiation from transient to durable form in awake rats
Korol, D. L., & Gold, P. E. (2007) · Hippocampus · doi:10.1002/hipo.20372 · Cited by 23 · see citing works
Gill, D. A., Perry, M. A., McGuire, E. P., Pérez‐Gómez, A., & Tasker, R. A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.02.036 · Cited by 23 · see citing works
Wang, M., Ramasamy, V. S., Samidurai, M., & Jo, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-47452-6 · Cited by 22 · see citing works
Gold, P. E. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00162-5 · Cited by 21 · see citing works
Learning-Related Hippocampal Long-Term Potentiation and Long-Term Depression
Manahan‐Vaughan, D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21104-8 · Cited by 21 · see citing works
Basolateral amygdala GABA-A receptors mediate stress-induced memory retrieval impairment in rats
Sardari, M., Rezayof, A., Khodagholi, F., & Zarrindast, M. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713001363 · Cited by 20 · see citing works
Sardari, M., Rezayof, A., & Zarrindast, M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.031 · Cited by 20 · see citing works
Harada, A., Shiosaka, S., Ishikawa, Y., & Komai, S. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.03.042 · Cited by 16 · see citing works
Dopamine type 1- and 2-like signaling in the modulation of spatial reference learning and memory
Feyissa, D. D., Sialana, F. J., Keimpema, E., Kalaba, P., Paunkov, A., Engidawork, E., Höger, H., Lübec, G., & Korz, V. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.01.028 · Cited by 17 · see citing works
Self-citationSpeksnijder, N., Christensen, K. V., Didriksen, M., de Kloet, E. R., & Datson, N. A. (2012) · Journal of Molecular Neuroscience · doi:10.1007/s12031-012-9809-2 · Cited by 16 · see citing works
Maćkowiak, M., Grzegorzewska, M., Budziszewska, B., Chocyk, A., Hess, G., & Wędzony, K. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06255.x · Cited by 16 · see citing works
The effects of prenatal stress on expression of p38 MAPK in offspring hippocampus
Cai, Q., Huang, S., Zhu, Z., Li, H., Li, Q., Jia, N., & Liu, J. (2008) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2008.06.001 · Cited by 16 · see citing works
Neurobiological Basis of the Complex Effects of Stress on Memory and Synaptic Plasticity
Zoladz, P. R., Park, C. R., & Diamond, D. M. (2011) · Wiley eBooks · doi:10.1002/9781118083222.ch8 · Cited by 16 · see citing works
Sucrose-induced plasticity in the basolateral amygdala in a ‘comfort’ feeding paradigm
Packard, A. E. B., Di, S., Egan, A. E., Fourman, S. M., Tasker, J. G., & Ulrich‐Lai, Y. M. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1454-7 · Cited by 15 · see citing works
Effects of Acute Exercise and Learning Strategy Implementation on Memory Function
Loprinzi, P. D., Harris, F., McRaney, K., Chism, M., Deming, R., Jones, T. W., Zou, L., & Tan, M. (2019) · Medicina · doi:10.3390/medicina55090568 · Cited by 15 · see citing works
Li, Z., & Richter‐Levin, G. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.059 · Cited by 15 · see citing works
Tabassum, H., & Frey, J. U. (2013) · Hippocampus · doi:10.1002/hipo.22166 · Cited by 13 · see citing works
Self-citationAntidepressant behavior in thyroidectomized Wistar rats is induced by hippocampal hypothyroidism
da Conceição, R. R., Laureano‐Melo, R., Oliveira, K. C., Melo, M. C. D. C., Kasamatsu, T. S., Maciel, R. M. B., de Souza, J. S., & Giannocco, G. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.02.005 · Cited by 12 · see citing works
Frey, S., & Frey, J. U. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.07.024 · Cited by 12 · see citing works
Self-citationSchulz, K., & Korz, V. (2010) · Learning & Memory · doi:10.1101/lm.1855610 · Cited by 11 · see citing works
Self-citationLi, S., Feig, L. A., & Hartley, D. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05760.x · Cited by 9 · see citing works
Thacker, J. S., & Mielke, J. G. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105233 · Cited by 8 · see citing works
NAN-190 potentiates the impairment of retention produced by swim stress
Schneider, A. M., & Simson, P. E. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2007.04.002 · Cited by 8 · see citing works
de Vargas, L. D. S., Gonçalves, R., de Lara, M. V. S., Costa‐Ferro, Z. S. M., Salamoni, S. D., Domingues, M. F., Piovesan, A. R., de Assis, D. R., Vinadé, L., Corrado, A. P., et al. (2017) · Brain Research · doi:10.1016/j.brainres.2017.06.007 · Cited by 8 · see citing works
Enhanced brain performance in mice following postnatal stress
Loizzo, A., Spampinato, S. M., Campana, G., Vella, S., Fortuna, A., Costa, L., Capasso, A., Monteleone, P., Renzi, P., & Loizzo, S. (2012) · Journal of Endocrinology · doi:10.1530/joe-12-0369 · Cited by 7 · see citing works
Gorbunova, A. A., Kudryashova, I. V., Манолова, А. О., Novikova, M. R., Stepanichev, M. Y., & Gulyaeva, N. V. (2017) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2017-058 · Cited by 7 · see citing works
“Unpredictable Stress”: Ambiguity of Stress Reactivity in Studies of Long-Term Plasticity
Kudryashova, I. V., & Gulyaeva, N. V. (2017) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-017-0496-x · Cited by 5 · see citing works
Leite, A. K. O., Farias, C. P., Schmidt, B. E., Teixeira, L., Rieder, A. S., Furini, C. R. G., & Wyse, Â. T. D. S. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.10.016 · Cited by 5 · see citing works
“Information”—from an Evolutionary Point of View
Kofler, W. W. (2014) · Information · doi:10.3390/info5020272 · Cited by 5 · see citing works
Effects of Exercise on Long-Term Potentiation in Neuropsychiatric Disorders
Loprinzi, P. D. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-1792-1_30 · Cited by 4 · see citing works
The effects of prenatal stress on expression of CaMK-II and L-Ca2+ channel in offspring hippocampus
Cai, Q., Zhang, B., Huang, S., Wang, T., & Zhou, T. (2011) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmr057 · Cited by 5 · see citing works
Rensel, M. A., & Schlinger, B. A. (2021) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2021.113734 · Cited by 4 · see citing works
Zoladz, P. R., & Diamond, D. M. (2008) · American Journal of Pharmacology and Toxicology · doi:10.3844/ajptsp.2008.111.124 · Cited by 4 · see citing works
Valipour, H., Jahromi, G. P., Mohammadi, A., & Meftahi, G. H. (2023) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-023-02790-1 · Cited by 3 · see citing works
El‐Kadi, R. A., Sedeek, M. S., Abdelkader, N. F., Zaki, H. F., & Kamel, A. S. E. D. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04911-8 · Cited by 4 · see citing works
Chang, S., Chen, H., Shaw, F.-Z., & Shyu, B. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100554 · Cited by 4 · see citing works
Molecular roadmap of the healthy stress response in the mouse hippocampusPreprint
von Ziegler, L., Floriou‐Servou, A., Waag, R., Gupta, R. R. D., Sturman, O., Gapp, K., Maat, C. A., Kockmann, T., Lin, H.-Y., Duss, S. N., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.26.436970 · Cited by 3 · see citing works
Autar, K., Guo, X., Powell, H., Patel, A., Malik, M., Grillo, M., Akanda, N., Narasimhan, N. S., Bogen, W., Long, C. J., et al. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.118556 · Cited by 2 · see citing works
Farmer, G. E., Park, C. R., Bullard, L. A., & Diamond, D. M. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1056-4_10 · Cited by 2 · see citing works
Kudryashova, I. V. (2013) · Neurochemical Journal · doi:10.1134/s1819712413030070 · Cited by 2 · see citing works
- Authors
- Ahmed, T., Frey, J. U., & Korz, V.
- Affiliations
- Leibniz Institute for Neurobiology (DE)
- University of Bayreuth (DE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-04-12
- Volume
- 26
- Issue
- 15
- Pages
- 3951-3958
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673904
- OpenAlex
- W2013192604
- Cited by
- 111
- References
- 71
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 3 · 2020: 1 · 2019: 5 · 2018: 2 · 2017: 8 · 2016: 7 · 2015: 1 · 2014: 4 · 2013: 6 · 2012: 8
- FWCI
- 6.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, public-domain)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- acute stress, swim stress, long-term potentiation, dentate gyrus, hippocampus, mineralocorticoid receptor, glucocorticoid receptor, p38 MAPK, CaMKII, CREB, basolateral amygdala, memory consolidation, corticosterone
- MeSH terms
- Animals, Benzazepines, Disease Models, Animal, Electrophysiology, Hippocampus, Male, Stress, Psychological, Swimming, Time Factors, Signal Transduction, Rats, Wistar, Dopamine Antagonists, Rats
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