Stress effects on memory: An update and integration
Abstract
It is well known that stressful experiences may affect learning and memory processes. Less clear is the exact nature of these stress effects on memory: both enhancing and impairing effects have been reported. These opposite effects may be explained if the different time courses of stress hormone, in particular catecholamine and glucocorticoid, actions are taken into account. Integrating two popular models, we argue here that rapid catecholamine and non-genomic glucocorticoid actions interact in the basolateral amygdala to shift the organism into a 'memory formation mode' that facilitates the consolidation of stressful experiences into long-term memory. The undisturbed consolidation of these experiences is then promoted by genomic glucocorticoid actions that induce a 'memory storage mode', which suppresses competing cognitive processes and thus reduces interference by unrelated material. Highlighting some current trends in the field, we further argue that stress affects learning and memory processes beyond the basolateral amygdala and hippocampus and that stress may pre-program subsequent memory performance when it is experienced during critical periods of brain development.
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Studies investigating the subtleties of stress prior to encoding generally suggest that stress immediately before or during encoding enhances memory recognition and recall performance, whereas stress induced before (25 min or more) encoding typically impairs memory performance.
“Studies that investigated the subtleties of stress prior to encoding generally suggest that stress immediately before or during encoding enhances memory recognition and recall performance, whereas stress induced before (i.e., 25 min or more) encoding typically impairs memory performance (Joëls et al., 2011; Schwabe et al., 2012; Zoladz et al., 2011, 2018).”
From The effects of acute stress on eyewitness memory: An integrative review for eyewitness researchers (2021) · cites this paper as Schwabe et al., 2012
Neurobiology research indicates that stress and stress hormones are critically involved in forming enduring memories.
“This assumption is in contrast with findings from the neurobiology field of learning and memory, showing that stress and stress hormones are critically involved in forming enduring memories.”
From Stress, stress-induced cortisol responses, and eyewitness identification performance (2016) · cites this paper as Schwabe et al., 2012
The impairing effects of stress on memory retrieval may offset the known beneficial effects of stress and stress hormones on memory formation in single-session eyewitness studies.
“so the impairing effects of stress on memory retrieval may offset the known beneficial effects of stress and stress hormones on memory formation (Schwabe et al., 2012; Wolf, 2009).”
From Stress, stress-induced cortisol responses, and eyewitness identification performance (2016) · cites this paper as Schwabe et al., 2012
Cites
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · 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
Self-citationMemory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
(1996) · Cited by 3,692 · see citing works
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640 · see citing works
Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation
REUL, J. M. H. M., & KLOET, E. R. D. (1985) · Endocrinology · doi:10.1210/endo-117-6-2505 · Cited by 2,580 · see citing works
Memory systems of the brain: A brief history and current perspective
Squire, L. R. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.06.005 · Cited by 2,269 · see citing works
The neurobiology of stress and development.
Gunnar, M., & Quevedo, K. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085605 · Cited by 2,011 · cited 2× · see citing works
“In the face of these findings and other findings that relate early life or prenatal stress to an increased vulnerability to psychopathology (for reviews see Cottrell and Seckl, 2009; Gunnar and Quevedo, 2007; Loman and Gunnar, 2010), studying the influence of early life or prenatal stress on brain and cognition appear…”
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Self-citationLearning and Memory Functions of the Basal Ganglia
Packard, M. G., & Knowlton, B. J. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142937 · Cited by 1,717 · see citing works
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543 · see citing works
Goal-directed instrumental action: contingency and incentive learning and their cortical substrates
Balleine, B. W., & Dickinson, A. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00033-1 · Cited by 1,541 · see citing works
Joëls, M., & Baram, T. Z. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2632 · Cited by 1,521 · see citing works
Self-citationStress and cognition: are corticosteroids good or bad guys?
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01438-1 · Cited by 1,258 · see citing works
Self-citationActions and habits: The development of behavioural autonomy
Dickinson, A. (1985) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1985.0010 · Cited by 1,217 · see citing works
Stress and glucocorticoids impair retrieval of long-term spatial memory
de Quervain, D. J.-F., Roozendaal, B., & McGaugh, J. L. (1998) · Nature · doi:10.1038/29542 · Cited by 1,182 · see citing works
Self-citationThe long-term behavioural consequences of prenatal stress
Weinstock, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.002 · Cited by 1,045 · see citing works
Learning under stress: how does it work?
Joëls, M., Pu, Z., Wiegert, O., Oitzl, M. S., & Krugers, H. J. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.02.002 · Cited by 947 · see citing works
Self-citationCompetition among multiple memory systems: converging evidence from animal and human brain studies
Poldrack, R. A., & Packard, M. G. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00157-4 · Cited by 880 · see citing works
Chronic Stress Causes Frontostriatal Reorganization and Affects Decision-Making
Dias-Ferreira, E., Sousa, J. C., Melo, I., Morgado, P., Mesquita, A. R., Cerqueira, J. J., Costa, R. M., & Sousa, N. (2009) · Science · doi:10.1126/science.1171203 · Cited by 858 · see citing works
Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval
Roozendaal, B. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4080 · Cited by 838 · see citing works
Self-citationKirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00118-x · Cited by 815 · see citing works
Self-citationKarst, H., Berger, S., Turiault, M., Tronche, F., Schütz, G., & Joëls, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507572102 · Cited by 774 · see citing works
Self-citationDiamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · cited 7× · see citing works
“…mediator of catecholamine and glucocorticoid actions on memory processes (Roozendaal et al., 2009a), these stress hormones exert also direct effects on brain regions such as the prefrontal cortex and hippocampus which contribute to the initiation of the memory formation mode (Diamond et al., 2007).”
InfluentialEnhanced memory for emotional material following stress-level cortisol treatment in humans
Buchanan, T. W., & Lovallo, W. R. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(00)00058-5 · Cited by 762 · see citing works
Acute cortisone administration impairs retrieval of long-term declarative memory in humans
de Quervain, D. J.-F., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000) · Nature Neuroscience · doi:10.1038/73873 · Cited by 745 · see citing works
Self-citationImpaired Memory Retrieval after Psychosocial Stress in Healthy Young Men
Kuhlmann, S., Piel, M., & Wolf, O. T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5139-04.2005 · Cited by 680 · see citing works
Self-citationChampagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661 · see citing works
Cahill, L., Gorski, L., & Le, K. (2003) · Learning & Memory · doi:10.1101/lm.62403 · Cited by 660 · see citing works
Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning.
Oitzl, M. S., & de Kloet, E. R. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.62 · Cited by 641 · see citing works
Self-citationPrenatal stress, glucocorticoids and the programming of adult disease
Cottrell, E. C. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.019.2009 · Cited by 640 · see citing works
Stress prompts habit behavior in humans
Schwabe, L., & Wolf, O. T. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0979-09.2009 · Cited by 606 · see citing works
Self-citationKim, J. J., Lee, H. J., Han, J.-S., & Packard, M. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05222.2001 · Cited by 537 · see citing works
Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning.
Oitzl, M. S., & de Kloet, E. R. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.1.62 · Cited by 525 · see citing works
Self-citationStress, memory, and the hippocampus: can't live with it, can't live without it
LUPIEN, S. J., & Lepage, M. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00361-8 · Cited by 515 · see citing works
Roozendaal, B., Okuda, S., van der Zee, E. A., & McGaugh, J. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601874103 · Cited by 499 · see citing works
Self-citationEarly experience and the development of stress reactivity and regulation in children
Loman, M. M., & Gunnar, M. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.007 · Cited by 489 · see citing works
Mechanisms of late-onset cognitive decline after early-life stress
Brunson, K. L., Kramár, E., Lin, B., Chen, Y., Colgin, L. L., Yanagihara, T. K., Lynch, G., & Baram, T. Z. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2281-05.2005 · Cited by 479 · see citing works
Morimoto, M., Morita, N., Ozawa, H., Yokoyama, K., & Kawata, M. (1996) · Neuroscience Research · doi:10.1016/s0168-0102(96)01105-4 · Cited by 475 · see citing works
A trans-dimensional approach to the behavioral aspects of depression
Bessa, J. M. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.001.2009 · Cited by 469 · see citing works
Sandi, C., Loscertales, M., & Guaza, C. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01412.x · Cited by 447 · see citing works
Laplante, D. P., Brunet, A., Schmitz, N., Ciampi, A., & King, S. (2008) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e31817eec80 · Cited by 424 · see citing works
Rapid non-genomic effects of corticosteroids and their role in the central stress response
Groeneweg, F. L., Karst, H., de Kloet, E. R., & Joëls, M. (2011) · Journal of Endocrinology · doi:10.1530/joe-10-0472 · Cited by 414 · see citing works
Self-citationCorticosteroid effects in the brain: U-shape it
Joëls, M. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.03.007 · Cited by 408 · see citing works
Self-citationGlucocorticoid effects on object recognition memory require training-associated emotional arousal
Okuda, S., Roozendaal, B., & McGaugh, J. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307803100 · Cited by 402 · see citing works
Self-citationQuirarte, G. L., Roozendaal, B., & McGaugh, J. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.14048 · Cited by 385 · see citing works
Self-citationRoozendaal, B., Okuda, S., de Quervain, D. J.-F., & McGaugh, J. L. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.049 · Cited by 382 · see citing works
Self-citationStress and emotional memory: a matter of timing
Joëls, M., Fernández, G., & Roozendaal, B. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.04.004 · Cited by 372 · see citing works
Self-citationBrain development under stress: Hypotheses of glucocorticoid actions revisited
Oitzl, M. S., Champagne, D. L., van der Veen, R., & de Kloet, E. R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.07.006 · Cited by 358 · see citing works
Self-citationReconsolidation: the advantage of being refocused
Dudai, Y. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.03.010 · Cited by 357 · see citing works
The modulatory effects of corticosteroids on cognition: studies in young human populations
Lupien, S. J., Wilkinson, C. W., Brière, S., Ménard, C., Ng Ying Kin, N. M. K., & Nair, N. P. V. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00061-0 · Cited by 353 · see citing works
Oomen, C. A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F. N., Manders, E. M. M., Joëls, M., Lucassen, P. J., & Krugers, H. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0247-10.2010 · Cited by 352 · see citing works
Self-citationMetaplasticity of amygdalar responses to the stress hormone corticosterone
Karst, H., Berger, S., Erdmann, G., Schütz, G., & Joëls, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914381107 · Cited by 342 · see citing works
Self-citationRoozendaal, 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
Self-citationRoozendaal, B., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0001 · Cited by 317 · see citing works
Self-citationSmeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.07.009 · Cited by 316 · see citing works
Self-citationRoozendaal, B., & McGaugh, J. L. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01355.x · Cited by 306 · see citing works
Self-citationStress modulates the use of spatial versus stimulus-response learning strategies in humansPreprint
Schwabe, L., Oitzl, M. S., Philippsen, C., Richter, S., Böhringer, A., Wippich, W., & Schächinger, H. (2007) · Learning & Memory · doi:10.1101/lm.435807 · Cited by 303 · see citing works
Self-citationLearning under stress impairs memory formation
Schwabe, L., & Wolf, O. T. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.09.009 · Cited by 297 · see citing works
Self-citationStressed Memories: How Acute Stress Affects Memory Formation in Humans
Henckens, M. J. A. G., Hermans, E. J., Pu, Z., Joëls, M., & Fernández, G. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1184-09.2009 · Cited by 295 · see citing works
Self-citationRoozendaal, B., Nguyen, B. T., Power, A. E., & McGaugh, J. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11642 · Cited by 293 · see citing works
Self-citationBuchanan, T. W., Tranel, D., & Adolphs, R. (2006) · Learning & Memory · doi:10.1101/lm.206306 · Cited by 293 · see citing works
Roozendaal, B., Griffith, Q. K., Buranday, J., de Quervain, D. J.-F., & McGaugh, J. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337480100 · Cited by 291 · see citing works
Self-citationAmygdala Modulation of Multiple Memory Systems: Hippocampus and Caudate-Putamen
Packard, M. G., & Teather, L. A. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3815 · Cited by 287 · see citing works
Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory
Oitzl, M. S., Reichardt, H. M., Joëls, M., & de Kloet, E. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.231313998 · Cited by 286 · see citing works
Self-citationRoozendaal, B., & McGaugh, J. L. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.3765 · Cited by 282 · see citing works
Self-citationLearning under stress: The inverted-U-shape function revisitedPreprint
Salehi, B., Cordero, M. I., & Sandi, C. (2010) · Learning & Memory · doi:10.1101/lm.1914110 · Cited by 272 · see citing works
Glucocorticoid Release and Memory Consolidation in Men and Women
Andreano, J. M., & Cahill, L. (2006) · Psychological Science · doi:10.1111/j.1467-9280.2006.01729.x · Cited by 270 · see citing works
Memory formation under stress: Quantity and quality
Schwabe, L., Wolf, O. T., & Oitzl, M. S. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.11.015 · Cited by 268 · see citing works
Self-citationBarsegyan, A., Mackenzie, S. M., Kurose, B. D., McGaugh, J. L., & Roozendaal, B. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011975107 · Cited by 262 · see citing works
Self-citationRoozendaal, B., Quirarte, G. L., & McGaugh, J. L. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01876.x · Cited by 260 · see citing works
Self-citationFrequency-Dependent Noradrenergic Modulation of Long-Term Potentiation in the Hippocampus
Hopkins, W. F., & Johnston, D. (1984) · Science · doi:10.1126/science.6091272 · Cited by 256 · see citing works
Payne, J. D., Jackson, E. D., Hoscheidt, S., Ryan, L., Jacobs, W. J., & Nadel, L. (2007) · Learning & Memory · doi:10.1101/lm.743507 · Cited by 248 · see citing works
Interaction between the Human Hippocampus and the Caudate Nucleus during Route Recognition
Voermans, N. C., Petersson, K. M., Daudey, L., Weber, B., van Spaendonck, K. P. M., Kremer, H. P. H., & Fernández, G. (2004) · Neuron · doi:10.1016/j.neuron.2004.07.009 · Cited by 247 · see citing works
Noradrenergic Regulation of Synaptic Plasticity in the Hippocampal CA1 Region
Katsuki, H., Izumi, Y., & Zorumski, C. F. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3013 · Cited by 244 · see citing works
Postreactivation Glucocorticoids Impair Recall of Established Fear Memory
Cai, W.-H., Blundell, J. J., Han, J., Greene, R. W., & Powell, C. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2397-06.2006 · Cited by 244 · see citing works
Roozendaal, B., Hernandez, A., Cabrera, S. M., Hagewoud, R., Malvaez, M., Stefanko, D. P., Haettig, J., & Wood, M. A. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5717-09.2010 · Cited by 233 · see citing works
Self-citationSchwabe, L., Dalm, S., Schächinger, H., & Oitzl, M. S. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.07.015 · Cited by 228 · see citing works
Self-citationMechanisms of Amygdala Modulation of Hippocampal Plasticity
Akirav, I., & Richter‐Levin, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09912.2002 · Cited by 225 · see citing works
Corticosteroids Operate as a Switch between Memory Systems
Schwabe, L., Schächinger, H., de Kloet, E. R., & Oitzl, M. S. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21278 · Cited by 217 · see citing works
Self-citationDiamond, D. M., Campbell, A. M., Park, C. R., Woodson, J. C., Conrad, C. D., Bachstetter, A. D., & Mervis, R. F. (2006) · Hippocampus · doi:10.1002/hipo.20188 · Cited by 213 · see citing works
Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P.-V., & Abrous, D. N. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.009 · Cited by 211 · see citing works
Gelinas, J. N., & Nguyen, P. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4175-04.2005 · Cited by 205 · see citing works
Mnemonic functions of the basal ganglia
White, N. M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80004-9 · Cited by 204 · see citing works
Huang, Y.-Y., & Kandel, E. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80080-x · Cited by 199 · see citing works
Bredy, T. W., Zhang, T. Y., Grant, R. J., Diorio, J., & Meaney, M. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03599.x · Cited by 196 · see citing works
Schwabe, L., Böhringer, A., Chatterjee, M. B., & Schächinger, H. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.02.002 · Cited by 194 · see citing works
Self-citationDose-dependent suppression of adrenocortical activity with metyrapone: Effects on emotion and memory
Roozendaall, B., Bohus, B., & McGaugh, J. L. (1996) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(96)00028-5 · Cited by 192 · see citing works
Time-Dependent Effects of Corticosteroids on Human Amygdala Processing
Henckens, M. J. A. G., van Wingen, G. A., Joëls, M., & Fernández, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3112-10.2010 · Cited by 191 · see citing works
Self-citationOitzl, M. S., Workel, J. O., Fluttert, M., van Loenen-Frösch, F., & de Kloet, E. R. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00231.x · Cited by 184 · see citing works
Self-citationKim, J. J., Koo, J. W., Lee, H. J., & Han, J.-S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4623-04.2005 · Cited by 184 · see citing works
Roozendaal, B., McReynolds, J. R., van der Zee, E. A., Lee, S., McGaugh, J. D., & McIntyre, C. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3626-09.2009 · Cited by 182 · see citing works
Self-citationPreventive Effect of β-Adrenoceptor Blockade on Glucocorticoid-Induced Memory Retrieval Deficits
de Quervain, D. J. ‐., Aerni, A., & Roozendaal, B. (2007) · American Journal of Psychiatry · doi:10.1176/ajp.2007.164.6.967 · Cited by 181 · see citing works
Self-citationAmygdala and "emotional" modulation of the relative use of multiple memory systems.
Packard, M., & Wingard, J. C. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.06.008 · Cited by 179 · see citing works
Stress and emotional memory retrieval: Effects of sex and cortisol response
Buchanan, T. W., & Tranel, D. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.07.003 · Cited by 179 · see citing works
Endogenous cortisol level interacts with noradrenergic activation in the human amygdala
van Stegeren, A. H., Wolf, O. T., Everaerd, W. T. A. M., Scheltens, P., Barkhof, F., & Rombouts, S. A. R. B. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.05.008 · Cited by 170 · see citing works
Self-citationWiegert, O., Joëls, M., & Krugers, H. (2006) · Learning & Memory · doi:10.1101/lm.87706 · Cited by 162 · see citing works
Self-citationPrenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring
Yang, J., Han, H., Cao, J., Li, L., & Xu, L. (2006) · Hippocampus · doi:10.1002/hipo.20181 · Cited by 161 · see citing works
Multiple brain-memory systems: the whole does not equal the sum of its parts
Kim, J. J., & Baxter, M. G. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01818-x · Cited by 159 · see citing works
Abercrombie, H. C., Speck, N. S., & Monticelli, R. M. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.06.008 · Cited by 158 · see citing works
Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences
Roozendaal, B., Barsegyan, A., & Lee, S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67006-x · Cited by 154 · see citing works
Self-citationSchwabe, L., Tegenthoff, M., Hoffken, O., & Wolf, O. T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0734-10.2010 · Cited by 150 · see citing works
Self-citationvan Stegeren, A. V., Roozendaal, B., Kindt, M., Wolf, O. T., & Joëls, M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.08.004 · Cited by 148 · see citing works
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Wang, X., Zhao, M., Ghitza, U. E., Li, Y., & Lü, L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0750-08.2008 · Cited by 142 · see citing works
Domes, G., Heinrichs, M., Reichwald, U., & Hautzinger, M. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00085-3 · Cited by 135 · see citing works
Stress-induced cortisol elevations are associated with impaired delayed, but not immediate recall
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Acute effects of hydrocortisone on the human brain: An fMRI study
Lovallo, W. R., Robinson, J. L., Glahn, D. C., & Fox, P. T. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.09.010 · Cited by 121 · see citing works
Yaka, R., Salomon, S., Matzner, H., & Weinstock, M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.01.018 · Cited by 120 · see citing works
Oitzl, M. S., Fluttert, M., Sutanto, W., & de Kloet, E. R. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00381.x · Cited by 119 · see citing works
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Beckner, V., Tucker, D. M., Delville, Y., & Mohr, D. C. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.3.518 · Cited by 118 · see citing works
Context-dependent enhancement of declarative memory performance following acute psychosocial stress
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Does Maternal Prenatal Stress Adversely Affect the Child’s Learning and Memory at Age Six?
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Stress impairs the reconsolidation of autobiographical memories
Schwabe, L., & Wolf, O. T. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.05.001 · Cited by 111 · see citing works
Self-citationEffects of stress and corticosterone on activity and plasticity in the amygdala
Kavushansky, A., & Richter‐Levin, G. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.21058 · Cited by 106 · see citing works
Tollenaar, M. S., Elzinga, B. M., Spinhoven, P., & Everaerd, W. T. A. M. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.08.002 · Cited by 104 · see citing works
Stress selectively and lastingly promotes learning of context-related high arousing information
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Self-citationZoladz, 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
Stress effects on declarative memory retrieval are blocked by a β-adrenoceptor antagonist in humans
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Self-citationDiamond, D. M., Park, C. R., & Woodson, J. C. (2004) · Hippocampus · doi:10.1002/hipo.10186 · Cited by 95 · see citing works
Borrell, J. I., de Kloet, E. R., & Bohus, B. (1984) · Life Sciences · doi:10.1016/0024-3205(84)90336-9 · Cited by 81 · see citing works
Kuhlmann, S., & Wolf, O. T. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.02.007 · Cited by 78 · see citing works
Self-citationQuirarte, G. L., de la Teja, I. S. L., Casillas, M., Serafín, N., Prado-Alcalá, R. A., & Roozendaal, B. (2009) · Learning & Memory · doi:10.1101/lm.1493609 · Cited by 76 · see citing works
Self-citationWeymar, M., Schwabe, L., Löw, A., & Hamm, A. O. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00174 · Cited by 73 · see citing works
Self-citationZhao, L., Zhang, X., Shi, J., Epstein, D. H., & Lü, L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1406-2 · Cited by 73 · see citing works
Schwabe, L., & Wolf, O. T. (2009) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.9.3.229 · Cited by 71 · see citing works
Self-citationMiranda, M. I., Quirarte, G. L., Rodríguez-García, G., McGaugh, J. L., & Roozendaal, B. (2008) · Learning & Memory · doi:10.1101/lm.964708 · Cited by 70 · see citing works
Self-citationToki, S., Morinobu, S., Imanaka, A., Yamamoto, S., Yamawaki, S., & Honma, K. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05288.x · Cited by 69 · see citing works
Sutherland, R. J., McDonald, R. J., & Savage, D. D. (2000) · Psychobiology · doi:10.3758/bf03332012 · Cited by 63 · see citing works
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Acute blockade of hippocampal glucocorticoid receptors facilitates spatial learning in rats
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Self-citationMemory consolidation: Essays in honor of James L. McGaugh.
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Contribution of brainstem structures in modulating memory storage processes.
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- Authors
- Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S.
- Affiliations
- Ruhr University Bochum (DE)
- University Medical Center Utrecht (NL)
- University Medical Center Groningen (NL)
- Leiden University (NL)
- Corresponding author
- Schwabe, Lars
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 36
- Issue
- 7
- Pages
- 1740-1749
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2110419377
- Semantic Scholar
- d494d73469841f74b8b09dd726d7b690c27e38e7
- Cited by
- 714
- References
- 136
- Citations by year
- 2026: 16 · 2025: 32 · 2024: 47 · 2023: 49 · 2022: 42 · 2021: 61 · 2020: 58 · 2019: 53 · 2018: 57 · 2017: 62 · 2016: 67 · 2015: 46 · 2014: 53 · 2013: 41 · 2012: 24
- FWCI
- 3.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- stress, memory consolidation, learning, catecholamines, glucocorticoids, basolateral amygdala, hippocampus, memory interference, memory storage, critical period, brain development, stress hormones
- MeSH terms
- Amygdala, Animals, Glucocorticoids, Hippocampus, Humans, Neuronal Plasticity, Stress, Psychological, Memory, Long-Term
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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