Sleep, dreams, and memory consolidation: The role of the stress hormone cortisol

Learning and Memory

Volumn 11, Issue 6, 2004, Pages 671-678

  Payne, Jessica D ^a   Nadel, Lynn ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MINERALOCORTICOID RECEPTOR; NEUROTRANSMITTER; NORADRENALIN; SEROTONIN;

CIRCADIAN RHYTHM; DREAM; ELECTROENCEPHALOGRAPHY; EMOTION; HIPPOCAMPUS; HUMAN; MEMORY CONSOLIDATION; MEMORY DISORDER; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MUSCLE TONE; NEOCORTEX; NERVE CELL NETWORK; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REM SLEEP; REVIEW; SCHIZOPHRENIA; SLEEP; SLEEP STAGE; SLOW WAVE SLEEP; STRESS;

ANIMALS; CEREBRAL CORTEX; DREAMS; HIPPOCAMPUS; HUMANS; HYDROCORTISONE; MEMORY; NEURAL PATHWAYS; NEUROTRANSMITTER AGENTS; SLEEP STAGES; THINKING;

EID: 10044246338     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.77104     Document Type: Review

References (99)

1. Alvarez, P. and Squire, L.R. 1994. Memory consolidation and the medial temporal lobe: A simple network model. Proc. Natl. Acad. Sci. 91: 7041-7045.
2. Antrobus, J. 1990. The neurocognition of sleep mentation: Rapid eye movements, visual imagery, and dreaming. In Sleep and cognition (eds. R.R. Bootzin, et al.), pp. 1-24. APA Books, Washington, D.C.
3. Aserinsky, E. and Kleitman, N. 1953. Regularly occurring periods of eye motility and concurrent phenomena during sleep. Science 118: 273-274.
4. Battaglia, F.P., Sutherland, G.R., and McNaughton, B.L. 2004. Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions. Learn. Mem. (this issue).
5. Baylor, G.W. and Cavallero, C. 2001. Memory sources associated with REM and NREM dream reports throughout the night: A new look at the data. Sleep 24: 165.
6. Braun, A.R., Balkin, T.J., Wesenten, N.J., Carson, R.E., Varga, M., Baldwin, P., Selbie, S., Belenky, G., and Herscovitch, P. 1997. Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain 120: 1173-1197.
7. Bremner, J.D. 1999. Does stress damage the brain? Biol. Psychiatry 45: 797-805.
8. Buchanan, T.W. and Lovallo, W.R. 2001. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26: 307-317.
9. Buzsaki, G. 1996. The hippocampo-neocortical dialogue. Cerebral Cortex 6: 81-92.
10. _. 1998. Memory consolidation during sleep: A neurophysiological perspective. J. Sleep Res. 7(Suppl): 17-23.
11. Buzsaki, G., Horvath, Z., Urioste, R., Hetke, J., and Wise, K. 1992. High frequency network oscillation in the hippocampus. Science 256: 1025-1027.
12. Cahill, L. and McGaugh, J.L. 1998. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21: 294-299.
13. Cavallero, C., Cicogna, P., Natale, V., Occhionero, M., and Zito, A. 1992. Slow wave sleep dreaming. Sleep 15: 562-566.
14. Chrobak, J.J. and Buzsaki, G. 1996. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci. 16: 3056-3066.
15. Cicogna, P., Cavallero, C., and Bosinelli, M. 1986. Differential access to memory traces in the production of mental experience. Int. J. Psychophysiol. 4: 209-216.
16. _. 1991. Cognitive aspects of mental activity during sleep. Am. J. Psychol. 104: 413-425.
17. deQuervain, D.J.F., Roozendaal, B., Nitsch, R.M., McGaugh, J.L., and Hock, C. 2000. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat. Neurosci. 3: 313-314.
18. de Quervain, D.J., Henke, K., Aerni, A., Treyer, V., McGaugh, J.L., Berthold, T., Nitsch, R.M., Buck, A., Roozendaal, B., and Hock, C. 2003. Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. Eur. J. Neurosci. 17: 1296-1302.
19. Diamond, D.M., Bennet, M.C., Fleshner, M., and Rose, G.M. 1992. Inverted U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2: 421-430.
20. Fouikes, W.D. 1962. Dream reports from different stages of sleep. J. Abnormal Social Psychol. 65: 14-25.
21. _. 1985. Dreaming: A cognitive-psychological analysis. Lawrence Erlbaum Associates, NJ.
22. _. 1999. Children's dreaming and the development of consciousness. Harvard University Press; Cambridge, MA.
23. Friedman, T.C., Garcia-Borreguero, D., Hardwick, D., Akuete, C.N., Doppman, J.L., Dorn, L.D., Barker, C.N., Yanovski, J.A., and Chrousos, G.P. 1994. Decreased 8-sleep and plasma S-sleep-inducing peptide in patients with Cushing syndrome. Neuroendocrinology 60: 626-634.
24. Gais, S. and Born, J. 2004. Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc. Natl. Acad. Sci. 101: 2140-2144.
25. Goldman-Rakic, P.S. 1992. Working memory and the mind. Sci. Am. 267: 111-117.
26. Golier, J.A., Yehuda, R., and Southwick, S.M. 1997. Memory and posttraumatic stress disorder. In Trauma and memory (eds. P.S. Appelbaum et al.), pp. 225-242. Oxford University Press, London.
27. Gray, M.J. and Lombardo, T.W. 2001. Complexity of trauma narratives as an index of fragmented memory in PTSD: A critical analysis. Appl. Cogn. Psychol. 15: S171-S186.
28. Han, J.-S., Bizon, J.L., Chun, H.-J., Maus, C.E., and Gallagher, M. 2002. Decreased glucocorticoid receptor mRNA and dysfunction of HPA axis in rats after removal of the cholinergic innervation to hippocampus. Eur. J. Neurosci. 16: 1399-1404.
29. Hasselmo, M.E. 1999. Neuromodulation: Acetylcholine and memory consolidation. Trends Cogn. Sci. 3: 351-359.
30. Hobson, J.A. 1988. The dreaming brain: How the brain creates both the sense and the nonsense of dreams. Basic Books, NY.
31. _. 2002. Dreaming: An introduction to the science of sleep. Oxford University Press, London.
32. Hobson, J.A., McCarley, R.W., and Wyzinski, P.W. 1975. Sleep cycle oscillation: Reciprocal discharge by two brainstem neuronal groups. Science 189: 55-58.
33. Hobson, J.A., Stickgold, R., and Pace-Schott, E.F. 1998. The neuropsychology of REM sleep dreaming. NeuroReport 9: R1-R14.
34. Hobson, J.A. and Pace-Schott, E.F. 2002. The cognitive neuroscience of sleep: Neuronal systems, consciousness and learning. Nature Rev. Neurosci. 3: 679-693.
35. Holden, K.J. and French, C.C. 2002. Alien abduction experiences: Some clues from neuropsychology and neuropsychiatry. Cogn. Neuropsychiatry 7: 163-178.
36. Jacobs, W.J. and Nadel, L. 1998. Neurobiology of reconstructed memory. Psychol. Public Policy Law 4: 1110-1134.
37. Johnson, M.K. 1991. Reality monitoring: Evidence from confabulation in organic brain disease patients. In Awareness of deficit after brain injury (eds. G. Prigatano and D.L. Schacter), pp. 176-197. Oxford University Press, Oxford, UK.
38. Kali, S. and Dayan, P. 2004. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat. Neurosci. 7: 286-294.
39. Karni, A., Tanne, D., Rubenstein, B.S., Askenasy, J.J., and Sagi, D. 1994. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265: 679-682.
40. Keenan, P.A., Jacobson, M.W., Soleymani, R.M., and Newcomer, J.W. 1995. Commonly used therapeutic doses of glucocorticoids impair explicit memory. Ann. NY Acad. Sci. 761: 400-402.
41. Kern, W., Dodt, C., Born, J., and Fehm, H.L. 1996. Changes in cortisol and growth hormone secretion during nocturnal sleep in the course of aging. J. Gerontol. A 51: M3-M9.
42. Kim, J.J. and Diamond, D.M. 2002. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3: 453-462.
43. Kirschbaum, C., Wolf, O.T., May, M., Wippich, W., and Hellhammer, D.H. 1996. Stress and treatment induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci. 58: 1475-1483.
44. Kondo, T., Antrobus, J., and Fein, G. 1989. Later REM activation and sleep mentation. Sleep Res. 18: 147.
45. Kuriyama, K., Stickgold, R., and Walker, M.P. 2004. Sleep-dependent learning and motor skill complexity. Learn. Mem. (this issue).
46. Lavie, P. 1996. The enchanted world of sleep. Yale University Press, New Haven, CT.
47. Lupien, S.J. and LePage, M. 2001. Stress, memory and the hippocampus: Can't live with it, can't live without it. Behav. Brain Res. 127: 137-158.
48. Lupien, S.J. and McEwen, B.S. 1997. The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Res. Rev. 24: 1-27
49. Lupien, S.J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N.P., Thakur, M., McEwen, B.S., Hauger, R.L., and Meaney, M.J. 1998. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1: 3-4.
50. Maquet, P. 2001. The role of sleep in learning and memory. Science 294: 1048-1052.
51. Mauri, M., Sinforiani, E., Bono, G., Vignati, F., Berselli, M.E., Attanasio, R., and Nappi, G. 1993. Memory impairment in Cushing's disease. Acta Neurologica Scandinavica 87: 52-55.
52. McClelland, J.L., McNaughton, B.L., O'Reilly, R., and Nadel, L. 1992. Complementary roles of hippocampus and neocortex in learning and memory. Society for Neuroscience Abstracts, 22.
53. McClelland, J.L., McNaughton, B.L., and O'Reilly, R.C. 1995. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102: 419-457.
54. McEwen, B. 1991. Nongenomic and genomic effects of steroids on neural activity. Trends Pharmacol. Sci. 12: 141-147.
55. Mitchell, K.J., Johnson, M.K., Raye, C.L., and D'Esposito, M. 2000. fMR1 evidence of age-related hippocampal dysfunction in feature binding in working memory. Cogn. Brain Res. 10: 197-206.
56. Nadel, L. and Moscovitch, M. 1997. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7: 217-227.
57. _. 1998. Hippocampal contribution to cortical plasticity. Neuropharmacology 37: 431-440.
58. Nadel, L. and Payne, J.D. 2002. The hippocampus, wayfinding, and episodic memory. In The neural basis of navigation: Evidence from single cell recording (ed. P. Sharp), pp. 235-247. Kluwer Academic Publishers, Boston.
59. Nadel, L., Payne, J.D., and Jacobs, W.J. 2002. The relationship between episodic memory and context: Clues from memory errors made while under stress. Physiol. Res. 51: S3-S11.
60. Newcomer, J.W., Craft, S., Hershey, T., Askins, K., and Bardgett, M.E. 1994. Glucocorticoid-induced impairment in declarative memory performance in adult humans. J. Neurosci. 14: 2047-2053.
61. Newcomer, J.W., Selke, G., Melson, A.K., Hershey, T., Craft, S., Richards, K., and Alderson, A.L. 1999. Decreased memory performance in healthy humans induced by stress-level cortisol treatment. Arch. Gen. Psychiatry 56: 527-533.
62. Nielsen, T.A. 2000. A review of mentation in REM and NREM sleep: "Covert" REM sleep as a possible reconciliation of two opposing models. Behav. Brain Sci. 23: 851-866, 904-1121.
63. Nofzinger, E.A., Mintun, M.A., Wiseman, M., Kupfer, D.J., and Moore, R.Y. 1997. Forebrain activation in REM sleep: An FDG PET study. Brain Res. 770: 192-201.
64. O'Keefe, J. and Nadel, L. 1978. The hippocampus as a cognitive map. The Clarendon Press, Oxford, UK.
65. Palier, K.A. and Voss, J.L. 2004. Memory reactivation and consolidation during sleep. Learn. Mem. (this issue).
66. Patel, A. and Bulloch, K. 2003. Type II glucocorticoid receptor immunoreactivity in the mossy cells of the rat and the mouse hippocampus. Hippocampus 13: 59-66.
67. Pavlides, D. and McEwen, B.S. 2000. Effects of mineralocorticoid and glucocorticoid receptors on long-term potentiation in the CA3 hippocampal field. Brain Res. 851: 204-214.
68. Payne, J.D., Nadel, L., Allen, J.J.B., Thomas, K.G.F., and Jacobs, W.J. 2002. The effects of experimentally induced stress on false recognition. Memory 10: 1-6.
69. Payne, J.D., Nadel, L., Britton, W.B., and Jacobs, W.J. 2004. The biopsychology of trauma and memory. In Memory and emotion (eds. D. Reisberg and P. Hertel), pp. 76-128. Oxford University Press, London.
70. Peigneux, P., Laureys, S., Delbeuck, X., and Maquet, P. 2001. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport. 12: A111-A124.
71. Plihal, W. and Born, J. 1997. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9: 534-547.
72. _. 1999a. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36: 571-582.
73. _. 1999b. Memory consolidation in human sleep depends on inhibition of glucocorticoid release. Neuroreport 10: 2741-2747.
74. Rasmusson, A.M., Lipschitz, D.S., Wang, S., Hu, S., Vojvoda, D., Bremner, J.D., Southwick, S.M., and Charney, D.S. 2001. Increased pituitary and adrenal reactivity in premenopausal women with posttraumatic stress disorder. Biol. Psychiatry 50: 965-977.
75. Roozendaal, B. 2003. Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Progress Neuropsychopharmaco. Biol. Psychiatry 27: 1213-1223.
76. Rubin, S.R., Bootzin, R.R., Franzen, P.L., and Al-Shajlawi, A. 1999. Memory performance after normal sleep or selective sleep fragmentation. Sleep Res. Online 2(Suppl 1): 241.
77. Sapolsky, R.M. 2000. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch. Gen. Psychiatry 57: 925-935.
78. Schwartz, S. 2003. Are life episodes replayed during dreaming. Trends Cogn. Sci. 7: 325-327.
79. Sheline, Y.I., Sanghavi, M., Mintun, M.A., and Gado, M.H. 1999. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J. Neurosci. 19: 5034-5043.
80. Shipley, J.E., Schteingart, D.E., Tandon, R., and Starkman, M.N. 1992. Sleep architecture and sleep apnea in patients with Cushing's disease. Sleep 15: 514-518.
81. Sirota, A., Csicsvari, J., Buhl, D., and Buzsaki, G. 2003. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. 100: 2065-2069.
82. Smith, E.E. and Jonides, J. 1999. Storage and executive processes in the frontal lobes. Science 283: 1657-1661.
83. Smith, C., Nixon, M., and Nader, R. 2004. Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential. Learn. Mem. (this issue).
84. Solms, M. 2000. Dreaming and REM sleep are controlled by different brain mechanisms. Behav. Brain Sci. 23: 843-850, 904-1121.
85. Starkman, M.N., Gebarski, S.S., Berent, S., and Schteingart, D.E. 1992. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry 32: 756-765.
86. Stickgold, R. and Walker, M. 2004. To sleep, perchance to gain creative insight? Trends Cogn. Sci. 8: 191-192.
87. Stickgold, R., Scott, L., Rittenhouse, C., and Hobson, J.A. 1999. Sleep-induced changes in associative memory. J. Cogn. Neurosci. 11: 182-193.
88. Stickgold, R., Hobson, J.A., Fosse, R., and Fosse, M. 2001. Sleep, learning, and dreams: Off-line memory reprocessing. Science 294: 1052-1057.
89. Tulving, E. 1983. Elements of episodic memory. Oxford University Press, London.
90. Van Cauter, E., Leproult, R., and Plat, L. 2000. Age-related changes in slow wave sleep and REM sleep and relationship with growth hormone and cortisol levels in healthy men. JAMA 284: 861-868.
91. van der Kolk, B.A., Hopper, J.W., and Osterman, J.E. 2001. Exploring the nature of traumatic memory: Combining clinical knowledge with laboratory methods. J. Aggression Maltreatment Trauma 4: 9-13.
92. Veneio, C. and Borrell, J. 1999. Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: A microdialysis study in freely moving rats. Eur. J. Neurosci. 11: 2465-2473.
93. Wagner, U., Gais, S., Haider, H., Verleger, R., and Born, J. 2004. Sleep inspires insight. Nature 427: 352-355.
94. Weitzman, E.D., Fukushima, D., Nogeire, C., Roffwarg, H., Gallagher, T.F., and Hellman, L. 1971. Twenty-four-hour pattern of the episodic secretion of cortisol in normal subjects. J. Clin. Endocrinol. Metabo. 33: 14-22.
95. Winson, J. 1985. Brain and psyche: The biology of the unconscious. Anchor Press/Doubleday, Garden City, NY.
96. _. 2002. The meaning of dreams. Sci. Am. 12: 54-61.
97. _. 2004. To sleep, perchance to dream. Learn. Mem. (this issue).
98. Wolkowitz, O.M., Reus, V.I., and Weingartner, H. 1990. Cognitive effects of corticostetoids. Am. J. Psychiatry 147: 1297-1303.
99. Wolkowitz, O.M., Weingartner, H., Rubinow, D.R., and Jimerson, D. 1993. Steroid modulation of human memory. Biochemical correlates. Biol. Psychiatry 33: 744-746.