System Consolidation During Sleep - A Common Principle Underlying Psychological and Immunological Memory Formation

Trends in Neurosciences

Volumn 38, Issue 10, 2015, Pages 585-597

  Westermann, Jürgen ^a   Lange, Tanja ^a   Textor, Johannes ^b   Born, Jan ^c  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN PRESENTING CELL; CENTRAL NERVOUS SYSTEM; HIPPOCAMPUS; HUMAN; IMMUNE SYSTEM; IMMUNOLOGICAL MEMORY; MEMORY; MEMORY CONSOLIDATION; NONHUMAN; PRIORITY JOURNAL; PSYCHOLOGICAL MEMORY; REVIEW; SLEEP; SLOW WAVE SLEEP; T LYMPHOCYTE; ANIMAL; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; IMMUNOLOGIC MEMORY; MEMORY CONSOLIDATION; SLEEP;

EID: 84943265710     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2015.07.007     Document Type: Review

References (119)

1. Kioussis D., Pachnis V. Immune and nervous systems: more than just a superficial similarity?. Immunity 2009, 31:705-710.
2. Anastasio T.J., et al. Individual and Collective Memory Consolidation: Analogous Processes on Different Levels 2012, MIT Press.
3. Steinman L. Lessons learned at the intersection of immunology and neuroscience. J. Clin. Invest. 2012, 122:1146-1148.
4. Rasch B., Born J. About sleep's role in memory. Physiol. Rev. 2013, 93:681-766.
5. Besedovsky L., et al. Sleep and immune function. Pflugers Arch. 2012, 463:121-137.
6. Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11:114-126.
7. Hebb D. The Organization of Behavior A Neuropsychological Theory 1949, Wiley.
8. Caporale N., Dan Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 2008, 31:25-46.
9. McClelland J.L., et al. 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. 1995, 102:419-457.
10. Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1971, 262:23-81.
11. Kumaran D., McClelland J.L. Generalization through the recurrent interaction of episodic memories: a model of the hippocampal system. Psychol. Rev. 2012, 119:573-616.
12. Frankland P.W., Bontempi B. The organization of recent and remote memories. Nat. Rev. Neurosci. 2005, 6:119-130.
13. Moscovitch M., et al. The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr. Opin. Neurobiol. 2006, 16:179-190.
14. Winocur G., et al. Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal-neocortical interactions. Neuropsychologia 2010, 48:2339-2356.
15. Nadel L., et al. Memory formation, consolidation and transformation. Neurosci. Biobehav. Rev. 2012, 36:1640-1645.
16. O'Neill J., et al. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010, 33:220-229.
17. Heine R. Über Wiedererkennen und rückwirkende Hemmung 1914, Barth.
18. Ngo H.V., et al. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 2013, 78:545-553.
19. Rasch B., et al. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 2007, 315:1426-1429.
20. Bendor D., Wilson M.A. Biasing the content of hippocampal replay during sleep. Nat. Neurosci. 2012, 15:1439-1444.
21. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
22. Ji D., Wilson M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 2007, 10:100-107.
23. Clemens Z., et al. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130:2868-2878.
24. Chauvette S., et al. Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 2012, 75:1105-1113.
25. Yang G., et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 2014, 344:1173-1178.
26. Inostroza M., Born J. Sleep for preserving and transforming episodic memory. Annu. Rev. Neurosci. 2013, 36:79-102.
27. Payne J.D., et al. The role of sleep in false memory formation. Neurobiol. Learn. Mem. 2009, 92:327-334.
28. Wagner U., et al. Sleep inspires insight. Nature 2004, 427:352-355.
29. Wilhelm I., et al. The sleeping child outplays the adult's capacity to convert implicit into explicit knowledge. Nat. Neurosci. 2013, 16:391-393.
30. Batterink L.J., et al. Sleep facilitates learning a new linguistic rule. Neuropsychologia 2014, 65:169-179.
31. Cousins J.N., et al. Cued memory reactivation during slow-wave sleep promotes explicit knowledge of a motor sequence. J. Neurosci. 2014, 34:15870-15876.
32. Ellenbogen J.M., et al. Human relational memory requires time and sleep. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:7723-7728.
33. Friedrich M., et al. Generalization of word meanings during infant sleep. Nat. Commun. 2015, 6:6004.
34. Pace-Schott E.F., et al. Sleep promotes generalization of extinction of conditioned fear. Sleep 2009, 32:19-26.
35. Cairney S.A., et al. Sleep and environmental context: interactive effects for memory. Exp. Brain Res. 2011, 214:83-92.
36. Lewis P.A., Durrant S.J. Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn. Sci. 2011, 15:343-351.
37. Antony J.W., et al. Cued memory reactivation during sleep influences skill learning. Nat. Neurosci. 2012, 15:1114-1116.
38. Albouy G., et al. Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 2008, 58:261-272.
39. Durrant S.J., et al. Overnight consolidation aids the transfer of statistical knowledge from the medial temporal lobe to the striatum. Cereb. Cortex 2013, 23:2467-2478.
40. Censor N. Generalization of perceptual and motor learning: a causal link with memory encoding and consolidation?. Neuroscience 2013, 250:201-207.
41. Matzinger P., Kamala T. Tissue-based class control: the other side of tolerance. Nat. Rev. Immunol. 2011, 11:221-230.
42. Neefjes J., et al. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 2011, 11:823-836.
43. Westermann J., et al. Naive, effector, and memory T lymphocytes efficiently scan dendritic cells in vivo: contact frequency in T cell zones of secondary lymphoid organs does not depend on LFA-1 expression and facilitates survival of effector T cells. J. Immunol. 2005, 174:2517-2524.
44. Mueller S.N., et al. Memory T cell subsets, migration patterns, and tissue residence. Annu. Rev. Immunol. 2013, 31:137-161.
45. + T cell-dendritic cell interaction kinetics and memory fate decisions. Immunity 2013, 39:496-507.
46. + T cell immunity. Science 2013, 340:630-635.
47. Bell E.B., Westermann J. CD4 memory T cells on trial: immunological memory without a memory T cell. Trends Immunol. 2008, 29:405-411.
48. McHeyzer-Williams M., et al. Molecular programming of B cell memory. Nat. Rev. Immunol. 2012, 12:24-34.
49. Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annu. Rev. Psychol. 2004, 55:51-86.
50. Battaglia F.P., et al. The hippocampus: hub of brain network communication for memory. Trends Cogn. Sci. 2011, 15:310-318.
51. Preston A.R., Eichenbaum H. Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 2013, 23:R764-R773.
52. Mizumori S.J. Context prediction analysis and episodic memory. Front. Behav. Neurosci. 2013, 7:132.
53. Polyn S.M., Kahana M.J. Memory search and the neural representation of context. Trends Cogn. Sci. 2008, 12:24-30.
54. Bartlett F.C. Remembering: A Study in Experimental and Social Psychology 1932, Cambridge University Press.
55. Rumelhart D.E. Schemata: The Building Blocks of Cognition. Center for Human Information Processing 1978, University of California, San Diego.
56. Ghosh V.E., Gilboa A. What is a memory schema? A historical perspective on current neuroscience literature. Neuropsychologia 2014, 53:104-114.
57. Wang S.H., et al. Anterior cingulate cortex in schema assimilation and expression. Learn. Mem. 2012, 19:315-318.
58. van Kesteren M.T., et al. How schema and novelty augment memory formation. Trends Neurosci. 2012, 35:211-219.
59. Tse D., et al. Schemas and memory consolidation. Science 2007, 316:76-82.
60. Hu X., et al. Cognitive neuroscience. Unlearning implicit social biases during sleep. Science 2015, 348:1013-1015.
61. Cunningham T.J., et al. Prospection and emotional memory: how expectation affects emotional memory formation following sleep and wake. Front. Psychol. 2014, 5:862.
62. + T cell responses. Immunity 2006, 25:533-543.
63. Wallace M.E., et al. The cytotoxic T-cell response to herpes simplex virus type 1 infection of C57BL/6 mice is almost entirely directed against a single immunodominant determinant. J. Virol. 1999, 73:7619-7626.
64. Blom K., et al. Temporal dynamics of the primary human T cell response to yellow fever virus 17D as it matures from an effector- to a memory-type response. J. Immunol. 2013, 190:2150-2158.
65. Baker B.M., et al. Structural and dynamic control of T-cell receptor specificity, cross-reactivity, and binding mechanism. Immunol. Rev. 2012, 250:10-31.
66. Brehm M.A., et al. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 2002, 3:627-634.
67. Weng N.P., et al. The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation. Nat. Rev. Immunol. 2012, 12:306-315.
68. + T cells enter the splenic T-cell zone and induce autoantibody-producing germinal centers through bystander activation. Eur. J. Immunol. 2014, 44:93-102.
69. Toth L.A. Sleep, sleep deprivation and infectious disease: studies in animals. Adv. Neuroimmunol. 1995, 5:79-92.
70. Krueger J.M., et al. Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 2008, 9:910-919.
71. Imeri L., Opp M.R. How (and why) the immune system makes us sleep. Nat. Rev. Neurosci. 2009, 10:199-210.
72. Spiegel K., et al. Effect of sleep deprivation on response to immunization. JAMA 2002, 288:1471-1472.
73. Lange T., et al. Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom. Med. 2003, 65:831-835.
74. Lange T., et al. Sleep after vaccination boosts immunological memory. J. Immunol. 2011, 187:283-290.
75. Benedict C., et al. Acute sleep deprivation has no lasting effects on the human antibody titer response following a novel influenza A H1N1 virus vaccination. BMC. Immunol. 2012, 13:1.
76. Prather A.A., et al. Sleep and antibody response to hepatitis B vaccination. Sleep 2012, 35:1063-1069.
77. Dickstein J.B., et al. The relationship of lymphocytes in blood and in lymph to sleep/wake states in sheep. Sleep 2000, 23:185-190.
78. Dimitrov S., et al. Number and function of circulating human antigen presenting cells regulated by sleep. Sleep 2007, 30:401-411.
79. Lange T., et al. Shift of monocyte function toward cellular immunity during sleep. Arch. Intern. Med. 2006, 166:1695-1700.
80. Stellwagen D., Malenka R.C. Synaptic scaling mediated by glial TNF-alpha. Nature 2006, 440:1054-1059.
81. del Rey A., et al. A cytokine network involving brain-borne IL-1beta, IL-1ra, IL-18, IL-6, and TNFalpha operates during long-term potentiation and learning. Brain Behav. Immun. 2013, 33:15-23.
82. Holz J., et al. EEG Sigma and slow-wave activity during NREM sleep correlate with overnight declarative and procedural memory consolidation. J. Sleep Res. 2012, 21:612-619.
83. Benca R.M., Quintas J. Sleep and host defenses: a review. Sleep 1997, 20:1027-1037.
84. Tononi G., Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 2014, 81:12-34.
85. Wagner U., Born J. Memory consolidation during sleep: interactive effects of sleep stages and HPA regulation. Stress 2008, 11:28-41.
86. Kelemen E., et al. Hippocampal corticosterone impairs memory consolidation during sleep but improves consolidation in the wake state. Hippocampus 2014, 24:510-515.
87. De Kloet E.R., et al. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301.
88. Weiss E.K., et al. Fast effects of glucocorticoids on memory-related network oscillations in the mouse hippocampus. J. Neuroendocrinol. 2008, 20:549-557.
89. Hasselmo M.E., McGaughy J. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog. Brain Res. 2004, 145:207-231.
90. Gais S., Born J. Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2140-2144.
91. Wilder R.L. Neuroendocrine-immune system interactions and autoimmunity. Annu. Rev. Immunol. 1995, 13:307-338.
92. Dracott B.N., Smith C.E. Hydrocortisone and the antibody response in mice. II. Correlations between serum and antibody and PFC in thymus, spleen, marrow and lymph nodes. Immunology 1979, 38:437-443.
93. Cross R.J., et al. Potentiation of antibody responsiveness after the transplantation of a syngeneic pituitary gland. J. Neuroimmunol. 1989, 25:29-35.
94. Hallschmid M., et al. A role for central nervous growth hormone-releasing hormone signaling in the consolidation of declarative memories. PLoS ONE 2011, 6:e23435.
95. Straub R.H., et al. Energy regulation and neuroendocrine-immune control in chronic inflammatory diseases. J. Intern. Med. 2010, 267:543-560.
96. Krueger J.M., et al. Sleep: a synchrony of cell activity-driven small network states. Eur. J. Neurosci. 2013, 38:2199-2209.
97. Seibt J., Frank M.G. Translation regulation in sleep: making experience last. Commun. Integr. Biol. 2012, 5:491-495.
98. Mednick S.C., et al. An opportunistic theory of cellular and systems consolidation. Trends Neurosci. 2011, 34:504-514.
99. Hupbach A., et al. Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. Learn. Mem. 2007, 14:47-53.
100. Rasch B., Born J. Maintaining memories by reactivation. Curr. Opin. Neurobiol. 2007, 17:698-703.
101. Huber R., Born J. Sleep, synaptic connectivity, and hippocampal memory during early development. Trends Cogn. Sci. 2014, 18:141-152.
102. Vorster A.P., Born J. Sleep and memory in mammals, birds and invertebrates. Neurosci. Biobehav. Rev. 2015, 50C:103-119.
103. Frahm N., et al. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 2004, 78:2187-2200.
104. Frankild S., et al. Amino acid similarity accounts for T cell cross-reactivity and for 'holes' in the T cell repertoire. PLoS ONE 2008, 3:e1831.
105. Tulving E. Episodic memory: from mind to brain. Annu. Rev. Psychol. 2002, 53:1-25.
106. + T cells. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18036-18041.
107. Textor J., et al. Random migration and signal integration promote rapid and robust T cell recruitment. PLoS. Comput. Biol. 2014, 10:e1003752.
108. Ribeiro S. Sleep and plasticity. Pflugers Arch. 2012, 463:111-120.
109. Diekelmann S., et al. Labile or stable: opposing consequences for memory when reactivated during waking and sleep. Nat. Neurosci. 2011, 14:381-386.
110. Payne J.D. Sleep on it!: stabilizing and transforming memories during sleep. Nat. Neurosci. 2011, 14:272-274.
111. Stickgold R., Walker M.P. Sleep-dependent memory triage: evolving generalization through selective processing. Nat. Neurosci. 2013, 16:139-145.
112. Rolls A., et al. Sleep to forget: interference of fear memories during sleep. Mol. Psychiatry 2013, 18:1166-1170.
113. Verleger R., et al. Insights into sleep's role for insight: studies with the number reduction task. Adv. Cogn. Psychol. 2013, 9:160-172.
114. Tamminen J., et al. The role of sleep spindles and slow-wave activity in integrating new information in semantic memory. J. Neurosci. 2013, 33:15376-15381.
115. Sterpenich V., et al. Memory reactivation during rapid eye movement sleep promotes its generalization and integration in cortical stores. Sleep 2014, 37:1061B-1075B.
116. Cai D.J., et al. REM, not incubation, improves creativity by priming associative networks. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:10130-10134.
117. Calais J.B., et al. Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobiol. Learn. Mem. 2015, 122:19-27.
118. Deliens G., et al. Sleep unbinds memories from their emotional context. Cortex 2013, 49:2221-2228.
119. Deliens G., Peigneux P. One night of sleep is insufficient to achieve sleep-to-forget emotional decontextualisation processes. Cogn. Emot. 2014, 28:698-706.