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REVIEW ARTICLE

Memory dynamics under stress

&
Pages 364-376 | Received 31 Jan 2017, Accepted 26 May 2017, Published online: 19 Jun 2017

References

  • Akirav, I., & Maroun, M. (2013). Stress modulation of reconsolidation. Psychopharmacology (Berl), 226(4), 747–761. doi: 10.1007/s00213-012-2887-6
  • Atsak, P., Guenzel, F. M., Kantar-Gok, D., Zalachoras, I., Yargicoglu, P., Meijer, O. C., … Roozendaal, B. (2016). Glucocorticoids mediate stress-induced impairment of retrieval of stimulus-response memory. Psychoneuroendocrinology, 67, 207–215.
  • Backus, A. R., Schoffelen, J. M., Szebenyi, S., Hanslmayr, S., & Doeller, C. F. (2016). Hippocampal-prefrontal theta oscillations support memory integration. Current Biology, 26(4), 450–457. doi: 10.1016/j.cub.2015.12.048
  • Bogdanov, M., & Schwabe, L. (2016). Transcranial stimulation of the dorsolateral prefrontal cortex prevents stress-induced working memory deficits. Journal of Neuroscience, 36(4), 1429–1437. doi: 10.1523/JNEUROSCI.3687-15.2016
  • Bos, M. G., Schuijer, J., Lodestijn, F., Beckers, T., & Kindt, M. (2014). Stress enhances reconsolidation of declarative memory. Psychoneuroendocrinology, 46, 102–113. doi: 10.1016/j.psyneuen.2014.04.011
  • Braun, S., & Hauber, W. (2013). Acute stressor effects on goal-directed action in rats. Learning & Memory, 20(12), 700–709. doi: 10.1101/lm.032987.113
  • Buchanan, T. W., Tranel, D., & Adolphs, R. (2006). Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learning & Memory, 13(3), 382–387. doi: 10.1101/lm.206306
  • Burgess, N., Maguire, E. A., & O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35(4), 625–641.
  • Cahill, L., Gorski, L., & Le, K. (2003). Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning & Memory, 10(4), 270–274. doi: 10.1101/lm.62403
  • Christianson, S. A., & Mjorndal, T. (1985). Adrenalin, emotional arousal and memory. Scandinavian Journal of Psychology, 26(3), 237–248.
  • Clark, C. R., Geffen, G. M., & Geffen, L. B. (1987). Catecholamines and attention II: Pharmacological studies in normal humans. Neuroscience & Biobehavioral Reviews, 11(4), 353–364.
  • Coccoz, V., Maldonado, H., & Delorenzi, A. (2011). The enhancement of reconsolidation with a naturalistic mild stressor improves the expression of a declarative memory in humans. Neuroscience, 185, 61–72. doi: 10.1016/j.neuroscience.2011.04.023
  • Cousijn, H., Rijpkema, M., Qin, S., van Marle, H. J. F., Franke, B., Hermans, E. J., … Fernandez, G. (2010). Acute stress modulates genotype effects on amygdala processing in humans. Proceedings of the National Academy of Sciences USA, 107(21), 9867–9872. doi: 10.1073/pnas.1003514107
  • Cuthbert, B. N., Schupp, H. T., Bradley, M. M., Birbaumer, N., & Lang, P. J. (2000). Brain potentials in affective picture processing: Covariation with autonomic arousal and affective report. Biological Psychology, 52(2), 95–111.
  • Dandolo, L. C., & Schwabe, L. (2016). Stress-induced cortisol hampers memory generalization. Learning & Memory, 23(12), 679–683.
  • de Kloet, E. R., Joels, M., & Holsboer, F. (2005). Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience, 6(6), 463–475. doi: 10.1038/nrn1683
  • de Quervain, D. J., Aerni, A., & Roozendaal, B. (2007). Preventive effect of β-adrenoceptor blockade on glucocorticoid-induced memory retrieval deficits. American Journal of Psychiatry, 164(6), 967–969. doi: 10.1176/ajp.2007.164.6.967
  • de Quervain, D. J., Kolassa, I. T., Ertl, V., Onyut, P. L., Neuner, F., Elbert, T., & Papassotiropoulos, A. (2007). A deletion variant of the α2b-adrenoceptor is related to emotional memory in Europeans and Africans. Nature Neuroscience, 10(9), 1137–1139. doi: 10.1038/nn1945
  • de Quervain, D. J., Roozendaal, B., & McGaugh, J. L. (1998). Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature, 394(6695), 787–790. doi: 10.1038/29542
  • de Quervain, D. J., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000). Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neuroscience, 3(4), 313–314. doi: 10.1038/73873
  • de Quervain, D., Schwabe, L., & Roozendaal, B. (2017). Stress, glucocorticoids and memory: Implications for treating fear-related disorders. Nature Reviews Neuroscience, 18(1), 7–19. doi: 10.1038/nrn.2016.155
  • Derijk, R. H., & de Kloet, E. R. (2008). Corticosteroid receptor polymorphisms: Determinants of vulnerability and resilience. European Journal of Pharmacology, 583(2-3), 303–311. doi: 10.1016/j.ejphar.2007.11.072
  • Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007). 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. Neural Plasticity, 2007, 60803. doi: 10.1155/2007/60803
  • Dudai, Y. (2012). The restless engram: Consolidations never end. Annual Review of Neuroscience, 35, 227–247. doi: 10.1146/annurev-neuro-062111-150500
  • Dudai, Y., & Eisenberg, M. (2004). Rites of passage of the engram: Reconsolidation and the lingering consolidation hypothesis. Neuron, 44(1), 93–100. doi: 10.1016/j.neuron.2004.09.003
  • Eichenbaum, H., & Cohen, N. J. (2004). From conditioning to conscious recollection: Memory systems of the brain. New York: Oxford University Press.
  • Eichenbaum, H., Schoenbaum, G., Young, B., & Bunsey, M. (1996). Functional organization of the hippocampal memory system. Proceedings of the National Academy of Sciences USA, 93(24), 13500–13507.
  • Eichenbaum, H., Stewart, C., & Morris, R. G. (1990). Hippocampal representation in place learning. The Journal of Neuroscience, 10(11), 3531–3542.
  • Everitt, B. J., & Robbins, T. W. (2005). Neural systems of reinforcement for drug addiction: From actions to habits to compulsion. Nature Neuroscience, 8(11), 1481–1489. doi: 10.1038/nn1579
  • Goodman, J., Leong, K. C., & Packard, M. G. (2012). Emotional modulation of multiple memory systems: Implications for the neurobiology of post-traumatic stress disorder. Reviews in the Neurosciences, 23(5-6), 627–643. doi: 10.1515/revneuro-2012-0049
  • Gordon, W. C., & Spear, N. E. (1973). Effect of reactivation of a previously acquired memory on the interaction between memories in the rat. Journal of Experimental Psychology, 99(3), 349–355.
  • Gourley, S. L., Swanson, A. M., Jacobs, A. M., Howell, J. L., Mo, M., Dileone, R. J., … Taylor, J. R. (2012). Action control is mediated by prefrontal BDNF and glucocorticoid receptor binding. Proceedings of the National Academy of Sciences USA, 109(50), 20714–20719. doi: 10.1073/pnas.1208342109
  • Guenzel, F. M., Wolf, O. T., & Schwabe, L. (2013). Stress disrupts response memory retrieval. Psychoneuroendocrinology, 38(8), 1460–1465. doi: 10.1016/j.psyneuen.2012.12.010
  • Guenzel, F. M., Wolf, O. T., & Schwabe, L. (2014). Glucocorticoids boost stimulus-response memory formation in humans. Psychoneuroendocrinology, 45, 21–30. doi: 10.1016/j.psyneuen.2014.02.015
  • Hardt, O., Einarsson, E. O., & Nader, K. (2010). A bridge over troubled water: Reconsolidation as a link between cognitive and neuroscientific memory research traditions. Annual Review of Psychology, 61, 141–167. doi: 10.1146/annurev.psych.093008.100455
  • Henckens, M. J., Pu, Z., Hermans, E. J., van Wingen, G. A., Joels, M., & Fernandez, G. (2012). Dynamically changing effects of corticosteroids on human hippocampal and prefrontal processing. Human Brain Mapping, 33(12), 2885–2897. doi: 10.1002/hbm.21409
  • Henckens, M. J., van Wingen, G. A., Joels, M., & Fernandez, G. (2010). Time-dependent effects of corticosteroids on human amygdala processing. Journal of Neuroscience, 30(38), 12725–12732. doi: 10.1523/JNEUROSCI.3112-10.2010
  • Henckens, M. J., van Wingen, G. A., Joels, M., & Fernandez, G. (2011). Time-dependent corticosteroid modulation of prefrontal working memory processing. Proceedings of the National Academy of Sciences USA, 108(14), 5801–5806. doi: 10.1073/pnas.1019128108
  • Hermans, E. J., Henckens, M. J., Joels, M., & Fernandez, G. (2014). Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends in Neurosciences, 37(6), 304–314. doi: 10.1016/j.tins.2014.03.006
  • Hermans, E. J., van Marle, H. J. F., Ossewaarde, L., Henckens, M. J. A. G., Qin, S., van Kesteren, M. T., … Fernandez, G. (2011). Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science, 334(6059), 1151–1153. doi: 10.1126/science.1209603
  • Hoscheidt, S. M., LaBar, K. S., Ryan, L., Jacobs, W. J., & Nadel, L. (2014). Encoding negative events under stress: High subjective arousal is related to accurate emotional memory despite misinformation exposure. Neurobiology of Learning and Memory, 112, 237–247. doi: 10.1016/j.nlm.2013.09.008
  • Hupbach, A., Gomez, R., Hardt, O., & Nadel, L. (2007). Reconsolidation of episodic memories: A subtle reminder triggers integration of new information. Learning & Memory, 14(1-2), 47–53. doi: 10.1101/lm.365707
  • Joels, M., & Baram, T. Z. (2009). The neuro-symphony of stress. Nature Reviews Neuroscience, 10(6), 459–466. doi: 10.1038/nrn2632
  • Joels, M., Fernandez, G., & Roozendaal, B. (2011). Stress and emotional memory: A matter of timing. Trends in Cognitive Sciences, 15(6), 280–288. doi: 10.1016/j.tics.2011.04.004
  • Joels, M., Karst, H., DeRijk, R., & de Kloet, E. R. (2008). The coming out of the brain mineralocorticoid receptor. Trends in Neurosciences, 31(1), 1–7. doi: 10.1016/j.tins.2007.10.005
  • Joels, M., Krugers, H., & Karst, H. (2008). Stress-induced changes in hippocampal function. Progress in Brain Research, 167, 3–15. doi: 10.1016/S0079-6123(07)67001-0
  • Joels, M., Pu, Z., Wiegert, O., Oitzl, M. S., & Krugers, H. J. (2006). Learning under stress: How does it work? Trends in Cognitive Sciences, 10(4), 152–158. doi: 10.1016/j.tics.2006.02.002
  • Joels, M., Sarabdjitsingh, R. A., & Karst, H. (2012). Unraveling the time domains of corticosteroid hormone influences on brain activity: Rapid, slow, and chronic modes. Pharmacological Reviews, 64(4), 901–938. doi: 10.1124/pr.112.005892
  • Johnson, H. M., & Seifert, C. M. (1994). Sources of the continued influence effect: When misinformation in memory affects later inferences. Journal of Experimental Psychology: Learning, Memory, and Cognition, 20(6), 1420–1436.
  • Karst, H., Berger, S., Erdmann, G., Schutz, G., & Joels, M. (2010). Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proceedings of the National Academy of Sciences USA, 107(32), 14449–14454. doi: 10.1073/pnas.0914381107
  • Kensinger, E. A. (2004). Remembering emotional experiences: The contribution of valence and arousal. Reviews in the Neurosciences, 15(4), 241–251.
  • Kim, J. J., & Diamond, D. M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nature Reviews Neuroscience, 3(6), 453–462. doi: 10.1038/nrn849
  • Kim, J. J., Lee, H. J., Han, J. S., & Packard, M. G. (2001). Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. Journal of Neuroscience, 21(14), 5222–5228.
  • Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011). The structural and functional connectivity of the amygdala: From normal emotion to pathological anxiety. Behavioural Brain Research, 223(2), 403–410. doi: 10.1016/j.bbr.2011.04.025
  • Kluen, L. M., Agorastos, A., Wiedemann, K., & Schwabe, L. (2017). Noradrenergic stimulation impairs memory generalization in women. Journal of Cognitive Neuroscience, 1–13. doi: 10.1162/jocn_a_01118
  • Kluen, L. M., Nixon, P., Agorastos, A., Wiedemann, K., & Schwabe, L. (2016). Impact of stress and glucocorticoids on schema-based learning. Neuropsychopharmacology. doi: 10.1038/npp.2016.256
  • Krugers, H. J., Karst, H., & Joels, M. (2012). Interactions between noradrenaline and corticosteroids in the brain: From electrical activity to cognitive performance. Frontiers in Cellular Neuroscience, 6, 15. doi: 10.3389/fncel.2012.00015
  • Kuhlmann, S., Piel, M., & Wolf, O. T. (2005). Impaired memory retrieval after psychosocial stress in healthy young men. Journal of Neuroscience, 25(11), 2977–2982. doi: 10.1523/JNEUROSCI.5139-04.2005
  • Loftus, E. F. (2005). Planting misinformation in the human mind: A 30-year investigation of the malleability of memory. Learning & Memory, 12(4), 361–366. doi: 10.1101/lm.94705
  • Lonergan, M. H., Olivera-Figueroa, L. A., Pitman, R. K., & Brunet, A. (2013). Propranolol’s effects on the consolidation and reconsolidation of long-term emotional memory in healthy participants: A meta-analysis. Journal of Psychiatry & Neuroscience, 38(4), 222–231. doi: 10.1503/jpn.120111
  • Lovallo, W. R., Robinson, J. L., Glahn, D. C., & Fox, P. T. (2010). Acute effects of hydrocortisone on the human brain: An fMRI study. Psychoneuroendocrinology, 35(1), 15–20. doi: 10.1016/j.psyneuen.2009.09.010
  • Lupien, S. J., & Lepage, M. (2001). Stress, memory, and the hippocampus: Can't live with it, can't live without it. Behavioural Brain Research, 127(1-2), 137–158.
  • Marin, M. F., Hupbach, A., Maheu, F. S., Nader, K., & Lupien, S. J. (2011). Metyrapone administration reduces the strength of an emotional memory trace in a long-lasting manner. The Journal of Clinical Endocrinology & Metabolism, 96(8), E1221–E1227. doi: 10.1210/jc.2011-0226
  • Marin, M. F., Pilgrim, K., & Lupien, S. J. (2010). Modulatory effects of stress on reactivated emotional memories. Psychoneuroendocrinology, 35(9), 1388–1396. doi: 10.1016/j.psyneuen.2010.04.002
  • McGaugh, J. L. (1966). Time-dependent processes in memory storage. Science, 153(3742), 1351–1358.
  • McGaugh, J. L. (2000). Memory – a century of consolidation. Science, 287(5451), 248–251.
  • McGaugh, J. L., McIntyre, C. K., & Power, A. E. (2002). Amygdala modulation of memory consolidation: Interaction with other brain systems. Neurobiology of Learning and Memory, 78(3), 539–552.
  • McKenzie, S., & Eichenbaum, H. (2011). Consolidation and reconsolidation: Two lives of memories? Neuron, 71(2), 224–233. doi: 10.1016/j.neuron.2011.06.037
  • Medina, A. C., Charles, J. R., Espinoza-Gonzalez, V., Sanchez-Resendis, O., Prado-Alcala, R. A., Roozendaal, B., & Quirarte, G. L. (2007). Glucocorticoid administration into the dorsal stratium facilitates memory consolidation of inhibitory avoidance training but not of the context or footshock components. Learning & Memory, 14(10), 673–677. doi: 10.1101/lm.654407
  • Misanin, J. R., Miller, R. R., & Lewis, D. J. (1968). Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science, 160(3827), 554–555.
  • Morgan, C. A., 3rd, Southwick, S., Steffian, G., Hazlett, G. A., & Loftus, E. F. (2013). Misinformation can influence memory for recently experienced, highly stressful events. International Journal of Law and Psychiatry, 36(1), 11–17. doi: 10.1016/j.ijlp.2012.11.002
  • Murchison, C. F., Zhang, X. Y., Zhang, W. P., Ouyang, M., Lee, A., & Thomas, S. A. (2004). A distinct role for norepinephrine in memory retrieval. Cell, 117(1), 131–143.
  • Myers, C. E., Shohamy, D., Gluck, M. A., Grossman, S., Onlaor, S., & Kapur, N. (2003). Dissociating medial temporal and basal ganglia memory systems with a latent learning task. Neuropsychologia, 41(14), 1919–1928.
  • Nadel, L., Hupbach, A., Gomez, R., & Newman-Smith, K. (2012). Memory formation, consolidation and transformation. Neuroscience & Biobehavioral Reviews, 36(7), 1640–1645. doi: 10.1016/j.neubiorev.2012.03.001
  • Nadel, L., & Payne, J. D. (2002). The relationship between episodic memory and context: Clues from memory errors made while under stress. Physiological Research, 51((Suppl. 1), S3–S11.
  • Nader, K. (2015). Reconsolidation and the dynamic nature of memory. Cold Spring Harbor Perspectives in Biology, 7(10), a021782. doi: 10.1101/cshperspect.a021782
  • Nader, K., & Hardt, O. (2009). A single standard for memory: The case for reconsolidation. Nature Reviews Neuroscience, 10(3), 224–234. doi: 10.1038/nrn2590
  • Packard, M. G., & Goodman, J. (2012). Emotional arousal and multiple memory systems in the mammalian brain. Frontiers in Behavioral Neuroscience, 6, 14. doi: 10.3389/fnbeh.2012.00014
  • Packard, M. G., & Wingard, J. C. (2004). Amygdala and “emotional” modulation of the relative use of multiple memory systems. Neurobiology of Learning and Memory, 82(3), 243–252. doi: 10.1016/j.nlm.2004.06.008
  • Pardilla-Delgado, E., Alger, S. E., Cunningham, T. J., Kinealy, B., & Payne, J. D. (2016). Effects of post-encoding stress on performance in the DRM false memory paradigm. Learning & Memory, 23(1), 46–50.
  • Payne, J. D., Nadel, L., Allen, J. J., Thomas, K. G., & Jacobs, W. J. (2002). The effects of experimentally induced stress on false recognition. Memory, 10(1), 1–6. doi: 10.1080/09658210143000119
  • Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54(5), 504–514.
  • Pitman, R. K., Sanders, K. M., Zusman, R. M., Healy, A. R., Cheema, F., Lasko, N. B., … Orr, S. P. (2002). Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biological Psychiatry, 51(2), 189–192.
  • Qin, S., Hermans, E. J., van Marle, H. J., & Fernandez, G. (2012). Understanding low reliability of memories for neutral information encoded under stress: Alterations in memory-related activation in the hippocampus and midbrain. Journal of Neuroscience, 32(12), 4032–4041. doi: 10.1523/JNEUROSCI.3101-11.2012
  • Qin, S., Hermans, E. J., van Marle, H. J. F., Luo, J., & Fernandez, G. (2009). Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological Psychiatry, 66(1), 25–32. doi: 10.1016/j.biopsych.2009.03.006
  • Quaedflieg, C. W. E. M., Schwabe, L., Meyer, T., & & Smeets, T. (2013). Time dependent effects of stress prior to encoding on event-related potentials and 24 h delayed retrieval. Psychoneuroendocrinology, 38(12), 3057–3069. doi: 10.1016/j.psyneuen.2013.09.002
  • Quaedflieg, C. W. E. M., Smulders, F. T., Meyer, T., Peeters, F., Merckelbach, H., & Smeets, T. (2016). The validity of individual frontal alpha asymmetry EEG neurofeedback. Social Cognitive and Affective Neuroscience, 11(1), 33–43. doi: 10.1093/scan/nsv090
  • Quaedflieg, C. W. E. M., van de Ven, V., Meyer, T., Siep, N., Merckelbach, H., & Smeets, T. (2015). Temporal dynamics of stress-induced alternations of intrinsic amygdala connectivity and neuroendocrine levels. PLoS ONE, 10(5), e0124141. doi: 10.1371/journal.pone.0124141
  • Quirarte, G. L., Ledesma de la Teja, I. S., Casillas, M., Serafin, N., Prado-Alcala, R. A., & Roozendaal, B. (2009). Corticosterone infused into the dorsal striatum selectively enhances memory consolidation of cued water-maze training. Learning & Memory, 16(10), 586–589. doi: 10.1101/lm.1493609
  • Rasch, B., Spalek, K., Buholzer, S., Luechinger, R., Boesiger, P., Papassotiropoulos, A., & de Quervain, D. J. (2009). A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proceedings of the National Academy of Sciences USA, 106(45), 19191–19196. doi: 10.1073/pnas.0907425106
  • Reul, J. M., & de Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology, 117(6), 2505–2511. doi: 10.1210/endo-117-6-2505
  • Robbins, T. W. (1984). Cortical noradrenaline, attention and arousal. Psychological Medicine, 14(1), 13–21.
  • Robbins, M. J., & Meyer, D. R. (1970). Motivational control of retrograde amnesia. Journal of Experimental Psychology, 84(2), 220–225.
  • Roozendaal, B., Griffith, Q. K., Buranday, J., De Quervain, D. J., & McGaugh, J. L. (2003). The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: Dependence on the basolateral amygdala. Proceedings of the National Academy of Sciences USA, 100(3), 1328–1333. doi: 10.1073/pnas.0337480100
  • Roozendaal, B., Hahn, E. L., Nathan, S. V., de Quervain, D. J., & McGaugh, J. L. (2004). Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. Journal of Neuroscience, 24(37), 8161–8169. doi: 10.1523/JNEUROSCI.2574-04.2004
  • Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009). Stress, memory and the amygdala. Nature Reviews Neuroscience, 10(6), 423–433. doi: 10.1038/nrn2651
  • Roozendaal, B., & McGaugh, J. L. (1996). Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiology of Learning and Memory, 65(1), 1–8. doi: 10.1006/nlme.1996.0001
  • Roozendaal, B., McReynolds, J. R., & McGaugh, J. L. (2004). The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. Journal of Neuroscience, 24(6), 1385–1392. doi: 10.1523/JNEUROSCI.4664-03.2004
  • Roozendaal, B., Okuda, S., de Quervain, D. J., & McGaugh, J. L. (2006). Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience, 138(3), 901–910. doi: 10.1016/j.neuroscience.2005.07.049
  • Roozendaal, B., Okuda, S., Van der Zee, E. A., & McGaugh, J. L. (2006). Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences USA, 103(17), 6741–6746. doi: 10.1073/pnas.0601874103
  • Roozendaal, B., Quirarte, G. L., & McGaugh, J. L. (2002). Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/cAMP/PKA system in influencing memory consolidation. European Journal of Neuroscience, 15(3), 553–560.
  • Sandrini, M., Censor, N., Mishoe, J., & Cohen, L. G. (2013). Causal role of prefrontal cortex in strengthening of episodic memories through reconsolidation. Current Biology, 23(21), 2181–2184. doi: 10.1016/j.cub.2013.08.045
  • Sara, S. J. (2000). Retrieval and reconsolidation: Toward a neurobiology of remembering. Learning & Memory, 7(2), 73–84.
  • Schacter, D. L. (1999). The seven sins of memory. Insights from psychology and cognitive neuroscience. American Psychologist, 54(3), 182–203.
  • Schacter, D. L., & Addis, D. R. (2007). The cognitive neuroscience of constructive memory: Remembering the past and imagining the future. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1481), 773–786. doi: 10.1098/rstb.2007.2087
  • Schacter, D. L., Guerin, S. A., & St Jacques, P. L. (2011). Memory distortion: An adaptive perspective. Trends in Cognitive Sciences, 15(10), 467–474. doi: 10.1016/j.tics.2011.08.004
  • Schacter, D. L., & Loftus, E. F. (2013). Memory and law: What can cognitive neuroscience contribute? Nature Neuroscience, 16(2), 119–123. doi: 10.1038/nn.3294
  • Schilling, T. M., Kolsch, M., Larra, M. F., Zech, C. M., Blumenthal, T. D., Frings, C., & Schachinger, H. (2013). For whom the bell (curve) tolls: Cortisol rapidly affects memory retrieval by an inverted U-shaped dose-response relationship. Psychoneuroendocrinology, 38(9), 1565–1572. doi: 10.1016/j.psyneuen.2013.01.001
  • Schmidt, P. I., Rosga, K., Schatto, C., Breidenstein, A., & Schwabe, L. (2014). Stress reduces the incorporation of misinformation into an established memory. Learning & Memory, 21(1), 744–747. doi: 10.1101/lm.033043.113
  • Schneider, A. M., & Sherman, W. (1968). Amnesia: A function of the temporal relation of footshock to electroconvulsive shock. Science, 159(3811), 219–221.
  • Schonfeld, P., Ackermann, K., & Schwabe, L. (2014). Remembering under stress: Different roles of autonomic arousal and glucocorticoids in memory retrieval. Psychoneuroendocrinology, 39, 249–256. doi: 10.1016/j.psyneuen.2013.09.020
  • Schwabe, L. (2013). Stress and the engagement of multiple memory systems: Integration of animal and human studies. Hippocampus, 23(11), 1035–1043. doi: 10.1002/hipo.22175
  • Schwabe, L. (2016). Memory under stress: From single systems to network changes. European Journal of Neuroscience. doi: 10.1111/ejn.13478
  • Schwabe, L., Joels, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012). Stress effects on memory: An update and integration. Neuroscience & Biobehavioral Reviews, 36(7), 1740–1749. doi: 10.1016/j.neubiorev.2011.07.002
  • Schwabe, L., Nader, K., & Pruessner, J. C. (2014). Reconsolidation of human memory: Brain mechanisms and clinical relevance. Biological Psychiatry, 76(4), 274–280. doi: 10.1016/j.biopsych.2014.03.008
  • Schwabe, L., Nader, K., Wolf, O. T., Beaudry, T., & Pruessner, J. C. (2012). Neural signature of reconsolidation impairments by propranolol in humans. Biological Psychiatry, 71(4), 380–386. doi: 10.1016/j.biopsych.2011.10.028
  • Schwabe, L., Oitzl, M. S., Philippsen, C., Richter, S., Bohringer, A., Wippich, W., & Schachinger, H. (2007). Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learning & Memory, 14(1), 109–116. doi: 10.1101/lm.435807
  • Schwabe, L., Romer, S., Richter, S., Dockendorf, S., Bilak, B., & Schachinger, H. (2009). Stress effects on declarative memory retrieval are blocked by a β-adrenoceptor antagonist in humans. Psychoneuroendocrinology, 34(3), 446–454. doi: 10.1016/j.psyneuen.2008.10.009
  • Schwabe, L., Tegenthoff, M., Hoffken, O., & Wolf, O. T. (2010). Concurrent glucocorticoid and noradrenergic activity shifts instrumental behavior from goal-directed to habitual control. Journal of Neuroscience, 30(24), 8190–8196. doi: 10.1523/JNEUROSCI.0734-10.2010
  • Schwabe, L., Tegenthoff, M., Hoffken, O., & Wolf, O. T. (2012). Simultaneous glucocorticoid and noradrenergic activity disrupts the neural basis of goal-directed action in the human brain. Journal of Neuroscience, 32(30), 10146–10155. doi: 10.1523/JNEUROSCI.1304-12.2012
  • Schwabe, L., Tegenthoff, M., Hoffken, O., & Wolf, O. T. (2013). Mineralocorticoid receptor blockade prevents stress-induced modulation of multiple memory systems in the human brain. Biological Psychiatry, 74(11), 801–808. doi: 10.1016/j.biopsych.2013.06.001
  • Schwabe, L., & Wolf, O. T. (2009a). The context counts: Congruent learning and testing environments prevent memory retrieval impairment following stress. Cognitive, Affective, & Behavioral Neuroscience, 9(3), 229–236. doi: 10.3758/CABN.9.3.229
  • Schwabe, L., & Wolf, O. T. (2009b). Stress prompts habit behavior in humans. Journal of Neuroscience, 29(22), 7191–7198. doi: 10.1523/JNEUROSCI.0979-09.2009
  • Schwabe, L., & Wolf, O. T. (2010a). Stress impairs the reconsolidation of autobiographical memories. Neurobiology of Learning and Memory, 94(2), 153–157. doi: 10.1016/j.nlm.2010.05.001
  • Schwabe, L., & Wolf, O. T. (2010b). Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action. Psychoneuroendocrinology, 35, 977–986.
  • Schwabe, L., & Wolf, O. T. (2011). Stress increases behavioral resistance to extinction. Psychoneuroendocrinology, 36(9), 1287–1293. doi: 10.1016/j.psyneuen.2011.02.002
  • Schwabe, L., & Wolf, O. T. (2012). Stress modulates the engagement of multiple memory systems in classification learning. Journal of Neuroscience, 32(32), 11042–11049. doi: 10.1523/JNEUROSCI.1484-12.2012
  • Schwabe, L., & Wolf, O. T. (2013). Stress and multiple memory systems: From “thinking” to “doing”. Trends in Cognitive Sciences, 17(2), 60–68. doi: 10.1016/j.tics.2012.12.001
  • Schwabe, L., & Wolf, O. T. (2014). Timing matters: Temporal dynamics of stress effects on memory retrieval. Cognitive, Affective, & Behavioral Neuroscience, 14(3), 1041–1048. doi: 10.3758/s13415-014-0256-0
  • Schwabe, L., Wolf, O. T., & Oitzl, M. S. (2010). Memory formation under stress: Quantity and quality. Neuroscience & Biobehavioral Reviews, 34(4), 584–591. doi: 10.1016/j.neubiorev.2009.11.015
  • Seehagen, S., Schneider, S., Rudolph, J., Ernst, S., & Zmyj, N. (2015). Stress impairs cognitive flexibility in infants. Proceedings of the National Academy of Sciences USA, 112(41), 12882–12886. doi: 10.1073/pnas.1508345112
  • Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., … Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27(9), 2349–2356. doi: 10.1523/JNEUROSCI.5587-06.2007
  • Shohamy, D., & Wagner, A. D. (2008). Integrating memories in the human brain: Hippocampal-midbrain encoding of overlapping events. Neuron, 60(2), 378–389. doi: 10.1016/j.neuron.2008.09.023
  • Sinha, R. (2007). The role of stress in addiction relapse. Current Psychiatry Reports, 9(5), 388–395.
  • Smeets, T., Jelicic, M., & Merckelbach, H. (2006). Stress-induced cortisol responses, sex differences, and false recollections in a DRM paradigm. Biological Psychology, 72(2), 164–172. doi: 10.1016/j.biopsycho.2005.09.004
  • Smeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008). True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology, 33(10), 1378–1386. doi: 10.1016/j.psyneuen.2008.07.009
  • Smith, S. M., & Vela, E. (2001). Environmental context-dependent memory: A review and meta-analysis. Psychonomic Bulletin & Review, 8(2), 203–220.
  • Soravia, L. M., Heinrichs, M., Aerni, A., Maroni, C., Schelling, G., Ehlert, U., … de Quervain, D. J. (2006). Glucocorticoids reduce phobic fear in humans. Proceedings of the National Academy of Sciences USA, 103(14), 5585–5590. doi: 10.1073/pnas.0509184103
  • Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171–177. doi: 10.1016/j.nlm.2004.06.005
  • Squire, L. R. (2009). Memory and brain systems: 1969-2009. Journal of Neuroscience, 29(41), 12711–12716. doi: 10.1523/JNEUROSCI.3575-09.2009
  • St Jacques, P. L., & & Schacter, D. L. (2013). Modifying memory: Selectively enhancing and updating personal memories for a museum tour by reactivating them. Psychological Science, 24(4), 537–543. doi: 10.1177/0956797612457377
  • Ulrich-Lai, Y. M., & Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress responses. Nature Reviews Neuroscience, 10(6), 397–409. doi: 10.1038/nrn2647
  • van Ast, V. A., Cornelisse, S., Meeter, M., Joels, M., & Kindt, M. (2013). Time-dependent effects of cortisol on the contextualization of emotional memories. Biological Psychiatry, 74(11), 809–816. doi: 10.1016/j.biopsych.2013.06.022
  • van Ast, V. A., Cornelisse, S., Meeter, M., & Kindt, M. (2014). Cortisol mediates the effects of stress on the contextual dependency of memories. Psychoneuroendocrinology, 41, 97–110. doi: 10.1016/j.psyneuen.2013.12.007
  • van Kesteren, M. T. R., Beul, S. F., Takashima, A., Henson, R. N., Ruiter, D. J., & Fernandez, G. (2013). Differential roles for medial prefrontal and medial temporal cortices in schema-dependent encoding: From congruent to incongruent. Neuropsychologia, 51(12), 2352–2359. doi: 10.1016/j.neuropsychologia.2013.05.027
  • van Marle, H. J. F., Hermans, E. J., Qin, S., & Fernandez, G. (2010). Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. Neuroimage, 53(1), 348–354. doi: 10.1016/j.neuroimage.2010.05.070
  • van Stegeren, A. H., Roozendaal, B., Kindt, M., Wolf, O. T., & Joels, M. (2010). Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding. Neurobiology of Learning and Memory, 93(1), 56–65. doi: 10.1016/j.nlm.2009.08.004
  • Vogel, S., Fernandez, G., Joels, M., & Schwabe, L. (2016). Cognitive adaptation under stress: A case for the mineralocorticoid receptor. Trends in Cognitive Sciences, 20(3), 192–203. doi: 10.1016/j.tics.2015.12.003
  • Vogel, S., Kluen, L. M., Fernandez, G., & Schwabe, L. (2017a). Stress leads to aberrant hippocampal involvement when processing schema-related information. Unpublished manuscript.
  • Vogel, S., Kluen, L. M., Fernandez, G., & Schwabe, L. (2017b). Stress affects the neural networks underlying the integration of new information with prior knowledge. Unpublished manuscript.
  • Vogel, S., Klumpers, F., Schroder, T. N., Oplaat, K. T., Krugers, H. J., Oitzl, M. S., & Fernandez, G. (2017). Stress induces a shift towards striatum-dependent stimulus-response learning via the mineralocorticoid receptor. Neuropsychopharmacology, doi:10.1038/npp.2016.262
  • Vogel, S., & Schwabe, L. (2016a). Learning and memory under stress: Implications for the classroom. Science of Learning, 1, 16011. doi: 10.1038/npjscilearn.2016.11
  • Vogel, S., & Schwabe, L. (2016b). Stress in the zoo: Tracking the impact of stress on memory formation over time. Psychoneuroendocrinology, 71, 64–72.
  • Wang, S. H., & Morris, R. G. (2010). Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annual Review of Psychology, 61(1), 49–79, C41-44. doi:10.1146/annurev.psych.093008.100523.
  • Weymar, M., Schwabe, L., Low, A., & Hamm, A. O. (2012). Stress sensitizes the brain: Increased processing of unpleasant pictures after exposure to acute stress. Journal of Cognitive Neuroscience, 24(7), 1511–1518. doi: 10.1162/jocn_a_00174
  • Wiegert, O., Joels, M., & Krugers, H. (2006). Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learning & Memory, 13(2), 110–113. doi: 10.1101/lm.87706
  • Wirz, L., Wacker, J., Felten, A., Reuter, M., & Schwabe, L. (2017). A deletion variant of the alpha2b-adrenoceptor modulates the stress-induced shift from “cognitive” to “habit” memory. Journal of Neuroscience. doi: 10.1523/JNEUROSCI.3507-16.2017
  • Zhao, L. Y., Zhang, X. L., Shi, J., Epstein, D. H., & Lu, L. (2009). Psychosocial stress after reactivation of drug-related memory impairs later recall in abstinent heroin addicts. Psychopharmacology (Berl), 203(3), 599–608. doi: 10.1007/s00213-008-1406-2
  • Zoladz, P. R., Clark, B., Warnecke, A., Smith, L., Tabar, J., & Talbot, J. N. (2011). Pre-learning stress differentially affects long-term memory for emotional words, depending on temporal proximity to the learning experience. Physiology & Behavior, 103(5), 467–476. doi: 10.1016/j.physbeh.2011.01.016

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