Enhancing influence of intranasal interleukin-6 on slow-wave activity and memory consolidation during sleep

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3629-3636

  Benedict, Christian ^a   Scheller, Jürgen ^b   Rose John, Stefan ^b   Born, Jan ^a   Marshall, Lisa ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

Cognition; Cytokine; Electroencephalogram power; Neuromodulation

Indexed keywords

INTERLEUKIN 6;

ADULT; ARTICLE; DECLARATIVE MEMORY; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY CONSOLIDATION; MENTAL TASK; NONREM SLEEP; NORMAL HUMAN; PRIORITY JOURNAL; PROCEDURAL MEMORY; PROTEIN FUNCTION; REM SLEEP; SIGNAL TRANSDUCTION; SLEEP PATTERN; SLOW BRAIN WAVE; TASK PERFORMANCE;

ADMINISTRATION, INTRANASAL; ADULT; BODY TEMPERATURE; EMOTIONS; FATIGUE; HUMANS; INTERLEUKIN-6; MALE; MEMORY; SLEEP; YOUNG ADULT;

EID: 70349652812     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-122853     Document Type: Article

References (49)

1. Born, J., Lange, T., Hansen, K., Molle, M., and Fehm, H. L. (1997) Effects of sleep and circadian rhythm on human circulating immune cells. J. Immunol. 158, 4454-4464 (Pubitemid 127483950)
2. Marshall, L., and Born, J. (2002) Brain-immune interactions in sleep. Int. Rev. Neurobiol. 52, 93-131
3. Krueger, J. M., and Majde, J. A. (2003) Humoral links between sleep and the immune system: research issues. Ann. N. Y. Acad. Sci. 992, 9-20
4. Seres, J., Herichova, I., Roman, O., Bornstein, S., and Jurcovicova, J. (2004) Evidence for daily rhythms of the expression of proopiomelanocortin, interleukin-1-β and interleukin-6 in adenopituitaries of male long-evans rats: effect of adjuvant arthritis. Neuroimmunomodulation 11, 316-322 (Pubitemid 39194330)
5. Vgontzas, A. N., Bixler, E. O., Lin, H. M., Prolo, P., Trakada, G., and Chrousos, G. P. (2005) IL-6 and its circadian secretion in humans. Neuroimmunomodulation 12, 131-140 (Pubitemid 40868672)
6. Guan, Z., Vgontzas, A. N., Omori, T., Peng, X., Bixler, E. O., and Fang, J. (2005) Interleukin-6 levels fluctuate with the light-dark cycle in the brain and peripheral tissues in rats. Brain Behav. Immun. 19, 526-529 (Pubitemid 41407702)
7. Dimitrov, S., Lange, T., Benedict, C., Nowell, M. A., Jones, S. A., Scheller, J., Rose-John, S., and Born, J. (2006) Sleep enhances IL-6 trans-signaling in humans. FASEB J. 20, 2174-2176 (Pubitemid 44953891)
8. Rose-John, S. (2003) Interleukin-6 biology is coordinated by membrane bound and soluble receptors. Acta Biochim. Pol. 50, 603-611
9. Scheller, J., and Rose-John, S. (2006) Interleukin-6 and its receptor: from bench to bedside. Med. Microbiol. Immunol. 195, 173-183 (Pubitemid 44600378)
10. Schobitz, B., Pezeshki, G., Pohl, T., Hemmann, U., Heinrich, P. C., Holsboer, F., and Reul, J. M. (1995) Soluble interleukin-6 (IL-6) receptor augments central effects of IL-6 in vivo. FASEB J. 9, 659-664
11. Gais, S., Lucas, B., and Born, J. (2006) Sleep after learning aids memory recall. Learn. Mem. 13, 259-262 (Pubitemid 43830669)
12. Born, J., Rasch, B., and Gais, S. (2006) Sleep to remember. Neuroscientist 12, 410-424
13. Marshall, L., and Born, J. (2007) The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn. Sci. 11, 442-450 (Pubitemid 47588990)
14. Plihal, W., and Born, J. (1999) Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36, 571-582 (Pubitemid 29357552)
15. Wagner, U., Gais, S., and Born, J. (2001) Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn. Mem. 8, 112-119 (Pubitemid 32297808)
16. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A., and Stickgold, R. (2002) Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205-211 (Pubitemid 34804334)
17. Sallmann, S., Juttler, E., Prinz, S., Petersen, N., Knopf, U., Weiser, T., and Schwaninger, M. (2000) Induction of interleukin- 6 by depolarization of neurons. J. Neurosci. 20, 8637-8642
18. Juttler, E., Tarabin, V., and Schwaninger, M. (2002) Interleukin- 6 (IL-6): a possible neuromodulator induced by neuronal activity. Neuroscientist 8, 268-275 (Pubitemid 34538794)
19. Balschun, D., Wetzel, W., Del, R. A., Pitossi, F., Schneider, H., Zuschratter, W., and Besedovsky, H. O. (2004) Interleukin-6: a cytokine to forget. FASEB J. 18, 1788-1790
20. Born, J., Lange, T., Kern, W., McGregor, G. P., Bickel, U., and Fehm, H. L. (2002) Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 5, 514-516 (Pubitemid 34568991)
21. LeMay, L. G., Vander, A. J., and Kluger, M. J. (1990) Role of interleukin 6 in fever in rats. Am. J. Physiol. 258, R798-R803
22. Späth-Schwalbe, E., Hansen, K., Schmidt, F., Schrezenmeier, H., Marshall, L., Burger, K., Fehm, H. L., and Born, J. (1998) Acute effects of recombinant human interleukin-6 on endocrine and central nervous sleep functions in healthy men. J. Clin. Endocrinol. Metab. 83, 1573-1579 (Pubitemid 28501024)
23. Mullington, J., Korth, C., Hermann, D. M., Orth, A., Galanos, C., Holsboer, F., and Pollmacher, T. (2000) Dose-dependent effects of endotoxin on human sleep. Am. J. Physiol. 278, R947-R955 (Pubitemid 30215208)
24. MacLean, A. W., Fekken, G. C., Saskin, P., and Knowles, J. B. (1992) Psychometric evaluation of the Stanford Sleepiness Scale. J. Sleep Res. 1, 35-39
25. Aschenbrenner, S., Tucha, O., and Lange, K. (2000) Regensburger Wortflüssigkeitstest, Hogrefe, Göttingen, Germany
26. Christensen, P., and Guilford, J. (1958) Word Fluency, Form A, Sheridan Supply, Beverly Hills, CA, USA
27. De Quervain, D. J., 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 (Pubitemid 30185479)
28. Schürer-Necker, E. (1994) Gedächtnis und Emotion: Zum Einfluss von Emotionen auf das Behalten von Texten, Psychologie Verlags Union, Munich, Germany
29. Sommer, T., Rose, M., Glascher, J., Wolbers, T., and Büchel, C. (2005) Dissociable contributions within the medial temporal lobe to encoding of object-location associations. Learn. Mem. 12, 343-351 (Pubitemid 40958346)
30. Rasch, B., Büchel, C., Gais, S., and Born, J. (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315, 1426-1429 (Pubitemid 46399554)
31. Rechtschaffen, A., and Kales, A. (1968) A Manual of Standardized Terminology, Techniques and Scoring System for Sleep of Human Subjects, U.S. Government Printing Office, Washington, DC, USA
32. Marshall, L., Helgadottir, H., Mölle, M., and Born, J. (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444, 610-613 (Pubitemid 44864437)
33. Huber, R., Ghilardi, M. F., Massimini, M., and Tononi, G. (2004) Local sleep and learning. Nature 430, 78-81
34. Mölle, M., Marshall, L., Gais, S., and Born, J. (2004) Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc. Natl. Acad. Sci. U. S. A. 101, 13963-13968 (Pubitemid 39298515)
35. Gais, S., Mölle, M., Helms, K., and Born, J. (2002) Learning-dependent increases in sleep spindle density. J. Neurosci. 22, 6830-6834 (Pubitemid 35386440)
36. Wagner, U., Degirmenci, M., Drosopoulos, S., Perras, B., and Born, J. (2005) Effects of cortisol suppression on sleep-associated consolidation of neutral and emotional memory. Biol. Psychiatry 58, 885-893 (Pubitemid 41790717)
37. Rasch, B., and Born, J. (2007) Maintaining memories by reactivation. Curr. Opin. Neurobiol. 17, 698-703
38. McGaugh, J. L. (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1-28
39. Babiloni, C., Vecchio, F., Mirabella, G., Buttiglione, M., Sebastiano, F., Picardi, A., Di, G. G., Quarato, P. P., Grammaldo, L. G., Buffo, P., Esposito, V., Manfredi, M., Cantore, G., and Eusebi, F. (2009) Hippocampal, amygdala, and neocortical synchronization of theta rhythms is related to an immediate recall during Rey auditory verbal learning test. Hum. Brain Mapp. 30, 2077-2089
40. Pare, D., Collins, D. R., and Pelletier, J. G. (2002) Amygdala oscillations and the consolidation of emotional memories. Trends Cogn. Sci. 6, 306-314 (Pubitemid 34754470)
41. Maquet, P. (2001) The role of sleep in learning and memory. Science 294, 1048-1052
42. Fischer, S., Hallschmid, M., Elsner, A. L., and Born, J. (2002) Sleep forms memory for finger skills. Proc. Natl. Acad. Sci. U. S. A. 99, 11987-11991 (Pubitemid 34994511)
43. Payne, J. D., Stickgold, R., Swanberg, K., and Kensinger, E. A. (2008) Sleep preferentially enhances memory for emotional components of scenes. Psychol. Sci. 19, 781-788
44. Baier, P. C., May, U., Scheller, J., Rose-John, S., and Schiffelholz, T. (2009) Impaired hippocampus-dependent and -independent learning in IL-6 deficient mice. Behav. Brain Res. 200, 192-196
45. Braida, D., Sacerdote, P., Panerai, A. E., Bianchi, M., Aloisi, A. M., Iosue, S., and Sala, M. (2004) Cognitive function in young and adult IL (interleukin)-6 deficient mice. Behav. Brain Res. 153, 423-429 (Pubitemid 38953117)
46. Marsland, A. L., Petersen, K. L., Sathanoori, R., Muldoon, M. F., Neumann, S. A., Ryan, C., Flory, J. D., and Manuck, S. B. (2006) Interleukin-6 covaries inversely with cognitive performance among middle-aged community volunteers. Psychosom. Med. 68, 895-903 (Pubitemid 44808715)
47. Luterman, J. D., Haroutunian, V., Yemul, S., Ho, L., Purohit, D., Aisen, P. S., Mohs, R., and Pasinetti, G. M. (2000) Cytokine gene expression as a function of the clinical progression of Alzheimer disease dementia. Arch. Neurol. 57, 1153-1160 (Pubitemid 30644662)
48. Tancredi, V., D'Antuono, M., Cafe, C., Giovedi, S., Bue, M. C., D'Arcangelo, G., Onofri, F., and Benfenati, F. (2000) The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogenactivated protein kinase ERK. J. Neurochem. 75, 634-643 (Pubitemid 30485444)
49. Denecke, H., Czehak, N., and Pietrowsky, R. (2002) Dose-response relationships of intranasal cholecystokinin and the P300 eventrelated brain potential. Pharmacol. Biochem. Behav. 73, 593-600 (Pubitemid 34876710)