Pre-learning stress differentially affects long-term memory for emotional words, depending on temporal proximity to the learning experience

Physiology and Behavior

Volumn 103, Issue 5, 2011, Pages 467-476

  Zoladz, Phillip R ^a   Clark, Brianne ^a   Warnecke, Ashlee ^a   Smith, Lindsay ^a   Tabar, Jennifer ^a   Talbot, Jeffery N ^a  

^a OHIO NORTHERN UNIVERSITY   (United States)

Author keywords

Amygdala; Cortisol; Hippocampus; Learning; Memory; Stress

Indexed keywords

HYDROCORTISONE;

ADULT; ARTICLE; BATH; DIASTOLIC BLOOD PRESSURE; FEMALE; HEART RATE; HUMAN; HUMAN EXPERIMENT; LEARNING; LONG TERM MEMORY; MALE; NORMAL HUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; SALIVA LEVEL; STRESS; SYSTOLIC BLOOD PRESSURE; WORD LIST RECALL; WORD RECOGNITION;

ADOLESCENT; ADULT; BLOOD PRESSURE; EMOTIONS; FEMALE; HEART RATE; HUMANS; HYDROCORTISONE; LEARNING; MALE; MEMORY, LONG-TERM; MENTAL RECALL; PAIN; RECOGNITION (PSYCHOLOGY); SALIVA; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 79954619939     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.01.016     Document Type: Article

References (71)

1. Joels M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cogn Sci 2006, 10:152-158.
2. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007, 2007:78970.
3. Zoladz P.R., Diamond D.M. Linear and non-linear dose-response functions reveal a hormetic relationship between stress and learning. Dose Response 2008, 7:132-148.
4. Schwabe, L, Wolf, OT, Oitzl, MS. Memory formation under stress: quantity and quality. Neurosci Biobehav Rev;34:584-591.
5. Wolf O.T. Stress and memory in humans: Twelve years of progress?. Brain Res 2009.
6. Diamond D.M., Campbell A.M., Park C.R., Woodson J.C., Conrad C.D., Bachstetter A.D., et al. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 2006, 16:571-576.
7. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
8. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. J Neurosci 2005, 25:2977-2982.
9. Buchanan T.W., Tranel D., Adolphs R. Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learn Mem 2006, 13:382-387.
10. Buchanan T.W., Tranel D. Stress and emotional memory retrieval: effects of sex and cortisol response. Neurobiol Learn Mem 2008, 89:134-141.
11. Smeets T., Otgaar H., Candel I., Wolf O.T. True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology 2008, 33:1378-1386.
12. Tollenaar M.S., Elzinga B.M., Spinhoven P., Everaerd W.A. The effects of cortisol increase on long-term memory retrieval during and after acute psychosocial stress. Acta Psychol (Amst) 2008, 127:542-552.
13. Schwabe L., Romer S., Richter S., Dockendorf S., Bilak B., Schachinger H. Stress effects on declarative memory retrieval are blocked by a beta-adrenoceptor antagonist in humans. Psychoneuroendocrinology 2009, 34:446-454.
14. Cahill L., Gorski L., Le K. Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learn Mem 2003, 10:270-274.
15. Hui I.R., Hui G.K., Roozendaal B., McGaugh J.L., Weinberger N.M. Posttraining handling facilitates memory for auditory-cue fear conditioning in rats. Neurobiol Learn Mem 2006, 86:160-163.
16. Park C.R., Zoladz P.R., Conrad C.D., Fleshner M., Diamond D.M. Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learn Mem 2008, 15:271-280.
17. Halonen J.D., Zoladz P.R., Park C.R., Diamond D.M. Propranolol blocks the stress-induced enhancement, but not impairment, of long-term spatial memory in adult rats. Thirty-Seventh Annual Meeting of the Society for Neuroscience 2007, San Diego, CA.
18. Kim J.J., Koo J.W., Lee H.J., Han J.S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J Neurosci 2005, 25:1532-1539.
19. Kim J.J., Lee H.J., Han J.S., Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 2001, 21:5222-5228.
20. Schwabe L., Bohringer A., Chatterjee M., Schachinger H. Effects of pre-learning stress on memory for neutral, positive and negative words: different roles of cortisol and autonomic arousal. Neurobiol Learn Mem 2008, 90:44-53.
21. Nater U.M., Moor C., Okere U., Stallkamp R., Martin M., Ehlert U., et al. Performance on a declarative memory task is better in high than low cortisol responders to psychosocial stress. Psychoneuroendocrinology 2007, 32:758-763.
22. Elzinga B.M., Bakker A., Bremner J.D. Stress-induced cortisol elevations are associated with impaired delayed, but not immediate recall. Psychiatry Res 2005, 134:211-223.
23. Payne J.D., Jackson E.D., Hoscheidt S., Ryan L., Jacobs W.J., Nadel L. Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories. Learn Mem 2007, 14:861-868.
24. Payne J.D., Jackson E.D., Ryan L., Hoscheidt S., Jacobs J.W., Nadel L. The impact of stress on neutral and emotional aspects of episodic memory. Memory 2006, 14:1-16.
25. Diamond D.M., Campbell A.M., Park C.R., Halonen J., Zoladz P.R. 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 Plast 2007, 2007:60803.
26. Akirav I., Richter-Levin G. Mechanisms of amygdala modulation of hippocampal plasticity. J Neurosci 2002, 22:9912-9921.
27. Akirav I., Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci 1999, 19:10530-10535.
28. Frey S., Bergado-Rosado J., Seidenbecher T., Pape H.C., Frey J.U. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci 2001, 21:3697-3703.
29. Wiegert O., Joels M., Krugers H. Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learn Mem 2006, 13:110-113.
30. Karst H., Berger S., Turiault M., Tronche F., Schutz G., Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA 2005, 102:19204-19207.
31. de Kloet E.R., Oitzl M.S., Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci 1999, 22:422-426.
32. Schwabe L., Haddad L., Schachinger H. HPA axis activation by a socially evaluated cold-pressor test. Psychoneuroendocrinology 2008, 33:890-895.
33. Bradley M.M., Lang P.J. Affective norms for English words (ANEW): instruction manual and affective ratings. Technical Report C-1, The Center for Research in Psychophysiology, University of Florida 1999.
34. Wickens T.D. Elementary signal detection theory 2002, University Press, Oxford.
35. Kensinger E.A., Corkin S. Memory enhancement for emotional words: are emotional words more vividly remembered than neutral words?. Mem Cognit 2003, 31:1169-1180.
36. Cahill L., Prins B., Weber M., McGaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 1994, 371:702-704.
37. Cahill L., McGaugh J.L. The neurobiology of memory for emotional events: adrenergic activation and the amygdala. Proc West Pharmacol Soc 1996, 39:81-84.
38. O'Carroll R.E., Drysdale E., Cahill L., Shajahan P., Ebmeier K.P. Stimulation of the noradrenergic system enhances and blockade reduces memory for emotional material in man. Psychol Med 1999, 29:1083-1088.
39. Strange B.A., Dolan R.J. Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proc Natl Acad Sci USA 2004, 101:11454-11458.
40. Dolcos F., LaBar K.S., Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 2004, 42:855-863.
41. Canli T., Zhao Z., Brewer J., Gabrieli J.D., Cahill L. Event-related activation in the human amygdala associates with later memory for individual emotional experience. J Neurosci 2000, 20:RC99.
42. Adolphs R., Cahill L., Schul R., Babinsky R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn Mem 1997, 4:291-300.
43. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci USA 1996, 93:8016-8021.
44. Vouimba R.M., Richter-Levin G. Physiological dissociation in hippocampal subregions in response to amygdala stimulation. Cereb Cortex 2005, 15:1815-1821.
45. Adamec R., Kent P., Anisman H., Shallow T., Merali Z. Neural plasticity, neuropeptides and anxiety in animals - implications for understanding and treating affective disorder following traumatic stress in humans. Neurosci Biobehav Rev 1998, 23:301-318.
46. Wang H.L., Wayner M.J., Chai C.Y., Lee E.H. Corticotrophin-releasing factor produces a long-lasting enhancement of synaptic efficacy in the hippocampus. Eur J Neurosci 1998, 10:3428-3437.
47. Wang H.L., Tsai L.Y., Lee E.H. Corticotropin-releasing factor produces a protein synthesis-dependent long-lasting potentiation in dentate gyrus neurons. J Neurophysiol 2000, 83:343-349.
48. Blank T., Nijholt I., Eckart K., Spiess J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J Neurosci 2002, 22:3788-3794.
49. Chen Y., Brunson K.L., Adelmann G., Bender R.A., Frotscher M., Baram T.Z. Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress. Neuroscience 2004, 126:533-540.
50. Ye L., Qi J.S., Qiao J.T. Long-term potentiation in hippocampus of rats is enhanced by endogenous acetylcholine in a way that is independent of N-methyl-D-aspartate receptors. Neurosci Lett 2001, 300:145-148.
51. Ovsepian S.V., Anwyl R., Rowan M.J. Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: in vivo study. Eur J Neurosci 2004, 20:1267-1275.
52. Li S., Cullen W.K., Anwyl R., Rowan M.J. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 2003, 6:526-531.
53. Ahmed T., Frey J.U., Korz V. Long-term effects of brief acute stress on cellular signaling and hippocampal LTP. J Neurosci 2006, 26:3951-3958.
54. Lemon N., Manahan-Vaughan D. Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 2006, 26:7723-7729.
55. Gray R., Johnston D. Noradrenaline and beta-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons. Nature 1987, 327:620-622.
56. Hopkins W.F., Johnston D. Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus. J Neurophysiol 1988, 59:667-687.
57. Katsuki H., Izumi Y., Zorumski C.F. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 1997, 77:3013-3020.
58. Izumi Y., Zorumski C.F. Norepinephrine promotes long-term potentiation in the adult rat hippocampus in vitro. Synapse 1999, 31:196-202.
59. Joels M. Corticosteroid actions in the hippocampus. J Neuroendocrinol 2001, 13:657-669.
60. Joels M., Velzing E., Nair S., Verkuyl J.M., Karst H. Acute stress increases calcium current amplitude in rat hippocampus: temporal changes in physiology and gene expression. Eur J Neurosci 2003, 18:1315-1324.
61. Zorumski C.F., Thio L.L. Properties of vertebrate glutamate receptors: calcium mobilization and desensitization. Prog Neurobiol 1992, 39:295-336.
62. Nakamichi N., Yoneda Y. Functional proteins involved in regulation of intracellular Ca(2+) for drug development: desensitization of N-methyl-D-aspartate receptor channels. J Pharmacol Sci 2005, 97:348-350.
63. Rosenmund C., Westbrook G.L. Rundown of N-methyl-D-aspartate channels during whole-cell recording in rat hippocampal neurons: role of Ca2+ and ATP. J Physiol 1993, 470:705-729.
64. Alford S., Frenguelli B.G., Schofield J.G., Collingridge G.L. Characterization of Ca2+ signals induced in hippocampal CA1 neurones by the synaptic activation of NMDA receptors. J Physiol 1993, 469:693-716.
65. Price C.J., Rintoul G.L., Baimbridge K.G., Raymond L.A. Inhibition of calcium-dependent NMDA receptor current rundown by calbindin-D28k. J Neurochem 1999, 72:634-642.
66. Brown M.W., Aggleton J.P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus?. Nat Rev Neurosci 2001, 2:51-61.
67. Aggleton J.P., Brown M.W. Interleaving brain systems for episodic and recognition memory. Trends Cogn Sci 2006, 10:455-463.
68. Sauvage M.M., Fortin N.J., Owens C.B., Yonelinas A.P., Eichenbaum H. Recognition memory: opposite effects of hippocampal damage on recollection and familiarity. Nat Neurosci 2008, 11:16-18.
69. Eichenbaum H., Yonelinas A.P., Ranganath C. The medial temporal lobe and recognition memory. Annu Rev Neurosci 2007, 30:123-152.
70. Squire L.R., Stark C.E., Clark R.E. The medial temporal lobe. Annu Rev Neurosci 2004, 27:279-306.
71. Wixted J.T. Dual-process theory and signal-detection theory of recognition memory. Psychol Rev 2007, 114:152-176.