Lipopolysaccharide-induced experimental immune activation does not impair memory functions in humans

Neurobiology of Learning and Memory

Volumn 94, Issue 4, 2010, Pages 561-567

  Grigoleit, Jan Sebastian ^a   Oberbeck, J Reiner ^a   Lichte, Philipp ^a   Kobbe, Philipp ^a   Wolf, Oliver T ^b   Montag, Thomas ^c   Rey, Adriana del ^d   Gizewski, Elke R ^a,e   Engler, Harald ^a   Schedlowski, Manfred ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c PAUL EHRLICH INSTITUT   (Germany)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Cortisol; Cytokines; Endotoxin; Memory; Prolactin; Sickness behavior

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CORTICOTROPIN; ENDOTOXIN; HYDROCORTISONE; INTERLEUKIN 10; INTERLEUKIN 6; NORADRENALIN; PROLACTIN; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; BODY TEMPERATURE; COGNITION; CONTROLLED STUDY; ENDOTOXEMIA; HUMAN; HUMAN EXPERIMENT; IMMUNOMODULATION; INFLAMMATION; MALE; MEMORY; NEUROENDOCRINE SYSTEM; NEUROPSYCHOLOGICAL TEST; NEUTROPHIL COUNT; NORMAL HUMAN; TASK PERFORMANCE; VOLUNTEER;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ATTENTION; COGNITION; CYTOKINES; HUMANS; HYDROCORTISONE; IMMUNE SYSTEM; LIPOPOLYSACCHARIDES; MALE; MEMORY; NEUROPSYCHOLOGICAL TESTS; REFERENCE VALUES; STROOP TEST; YOUNG ADULT;

EID: 78149406326     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2010.09.011     Document Type: Article

References (51)

1. Asai Y., Makimura Y., Kawabata A., Ogawa T. Soluble CD14 discriminates slight structural differences between lipid as that lead to distinct host cell activation. Journal of Immunology 2007, 179(11):7674-7683. 179/11/7674 [pii].
2. Aubert A., Vega C., Dantzer R., Goodall G. Pyrogens specifically disrupt the acquisition of a task involving cognitive processing in the rat. Brain, Behavior and Immunity 1995, 9(2):129-148. doi: S0889-1591(85)71013-6 [pii] 10.1006/brbi.1995.1013.
3. Bahador M., Cross A.S. From therapy to experimental model: a hundred years of endotoxin administration to human subjects. Journal of Endotoxin Research 2007, 13(5):251-279. doi: 13/5/251 [pii] 10.1177/0968051907085986.
4. Bäumler G. Farbe-Wort-Interferenztest nach J.R. Stroop (FWIT) 1985, Hogrefe, Göttingen.
5. Ben-Jonathan N., Hnasko R. Dopamine as a prolactin (PRL) inhibitor. Endocrine Reviews 2001, 22(6):724-763.
6. Besedovsky H.O., del Rey A. Immune-neuro-endocrine interactions: Facts and hypotheses. Endocrine Reviews 1996, 17(1):64-102.
7. Brydon L., Harrison N.A., Walker C., Steptoe A., Critchley H.D. Peripheral inflammation is associated with altered substantia nigra activity and psychomotor slowing in humans. Biological Psychiatry 2008, 63(11):1022-1029. doi: S0006-3223(07)01241-3 [pii] 10.1016/j.biopsych.2007.12.007.
8. Cahill L., Prins B., Weber M., McGaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 1994, 371(6499):702-704. 10.1038/371702a0.
9. Childs E., de Wit H. Hormonal, cardiovascular, and subjective responses to acute stress in smokers. Psychopharmacology (Berl) 2009, 203(1):1-12. doi: 10.1007/s00213-008-1359-5.
10. Cohen O., Reichenberg A., Perry C., Ginzberg D., Pollmacher T., Soreq H., et al. Endotoxin-induced changes in human working and declarative memory associate with cleavage of plasma "readthrough" acetylcholinesterase. Journal of Molecular Neuroscience 2003, 21(3):199-212. JMN:21:3:199 [pii].
11. Conti B., Tabarean I., Andrei C., Bartfai T. Cytokines and fever. Frontiers in Bioscience 2004, 9:1433-1449.
12. Dantzer R. Cytokine-induced sickness behavior: Where do we stand?. Brain, Behavior and Immunity 2001, 15(1):7-24. doi: 10.1006/brbi.2000.0613 S0889-1591(00)90613-5 [pii].
13. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: When the immune system subjugates the brain. Nature Reviews Neuroscience 2008, 9(1):46-56. doi: nrn2297 [pii] 10.1038/nrn2297.
14. De Laurentiis A., Pisera D., Caruso C., Candolfi M., Mohn C., Rettori V., et al. Lipopolysaccharide- and tumor necrosis factor-alpha-induced changes in prolactin secretion and dopaminergic activity in the hypothalamic-pituitary axis. Neuroimmunomodulation 2002, 10(1):30-39. doi: nim10030 [pii].
15. de Quervain D.J., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Frontiers in Neuroendocrinology 2009, 30(3):358-370. doi: S0091-3022(09)00003-X [pii] 10.1016/j.yfrne.2009.03.002.
16. del Rey A., Wolff C., Wildmann J., Randolf A., Hahnel A., Besedovsky H.O., et al. Disrupted brain-immune system-joint communication during experimental arthritis. Arthritis & Rheumatism 2008, 58(10):3090-3099. doi: 10.1002/art.23869.
17. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., et al. A meta-analysis of cytokines in major depression. Biological Psychiatry 2010, 67(5):446-457. doi: S0006-3223(09)01229-3 [pii] 10.1016/j.biopsych.2009.09.033.
18. Drexhage R.C., Knijff E.M., Padmos R.C., Heul-Nieuwenhuijzen L., Beumer W., Versnel M.A., et al. The mononuclear phagocyte system and its cytokine inflammatory networks in schizophrenia and bipolar disorder. Expert Review of Neurotherapeutics 2010, 10(1):59-76. doi: 10.1586/ern.09.144.
19. Eisenberger N.I., Inagaki T.K., Rameson L.T., Mashal N.M., Irwin M.R. An fMRI study of cytokine-induced depressed mood and social pain: The role of sex differences. Neuroimage 2009, 47(3):881-890. doi: S1053-8119(09)00388-7 [pii] 10.1016/j.neuroimage.2009.04.040.
20. Engler H., Doenlen R., Riether C., Engler A., Niemi M.B., Besedovsky H.O., et al. Time-dependent alterations of peripheral immune parameters after nigrostriatal dopamine depletion in a rat model of Parkinson's disease. Brain, Behavior and Immunity 2009, 23(4):518-526. doi: S0889-1591(09)00045-2 [pii] 10.1016/j.bbi.2009.01.018.
21. Feghali C.A., Wright T.M. Cytokines in acute and chronic inflammation. Frontiers in Bioscience 1997, 2:d12-d26.
22. Fries E., Hellhammer D.H., Hellhammer J. Attenuation of the hypothalamic-pituitary-adrenal axis responsivity to the Trier Social Stress Test by the benzodiazepine alprazolam. Psychoneuroendocrinology 2006, 31(10):1278-1288. doi: S0306-4530(06)00153-3 [pii] 10.1016/j.psyneuen.2006.09.009.
23. Gibertini M. Cytokines and cognitive behavior. Neuroimmunomodulation 1998, 5(3-4):160-165. doi: nim05160 [pii].
24. Grattan D.R., Kokay I.C. Prolactin: A pleiotropic neuroendocrine hormone. Journal of Neuroendocrinology 2008, 20(6):752-763. doi: JNE1736 [pii] 10.1111/j.1365-2826.2008.01736.x.
25. Harrison N.A., Brydon L., Walker C., Gray M.A., Steptoe A., Critchley H.D. Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biological Psychiatry 2009, 66(5):407-414. doi: S0006-3223(09)00396-5 [pii] 10.1016/j.biopsych.2009.03.015.
26. Hayley S., Poulter M.O., Merali Z., Anisman H. The pathogenesis of clinical depression: Stressor- and cytokine-induced alterations of neuroplasticity. Neuroscience 2005, 135(3):659-678. doi: S0306-4522(05)00403-3 [pii] 10.1016/j.neuroscience.2005.03.051.
27. Kirschbaum C., Wolf O.T., May M., Wippich W., Hellhammer D.H. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences 1996, 58(17):1475-1483. doi: 002432059600118X [pii].
28. Klaiberg A. Wechsler Gedächtnistest - Revidierte Fassung Deutsche Adaptation der revidierten Fassung der Wechsler Memory Scale (WMS-R). Brickenkamp Handbuch psychologischer und pädagogischer Tests 2002, Vol. 2:1259-1261. Hogrefe, Göttingen. third ed.
29. Krabbe K.S., Reichenberg A., Yirmiya R., Smed A., Pedersen B.K., Bruunsgaard H. Low-dose endotoxemia and human neuropsychological functions. Brain, Behavior and Immunity 2005, 19(5):453-460. doi: S0889-1591(05)00076-0 [pii] 10.1016/j.bbi.2005.04.010.
30. Lupien S.J., Maheu F., Tu M., Fiocco A., Schramek T.E. The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain and cognition 2007, 65(3):209-237. doi: S0278-2626(07)00032-2 [pii] 10.1016/j.bandc.2007.02.007.
31. McAfoose J., Baune B.T. Evidence for a cytokine model of cognitive function. Neuroscience & Biobehavioral Reviews 2009, 33(3):355-366. doi: S0149-7634(08)00183-8 [pii] 10.1016/j.neubiorev.2008.10.005.
32. McGaugh J.L. Dissociating learning and performance: Drug and hormone enhancement of memory storage. Brain Research Bulletin 1989, 23(4-5):339-345. doi: 0361-9230(89)90220-7 [pii].
33. Meyer J.M., McEvoy J.P., Davis V.G., Goff D.C., Nasrallah H.A., Davis S.M., et al. Inflammatory markers in schizophrenia: Comparing antipsychotic effects in phase 1 of the clinical antipsychotic trials of intervention effectiveness study. Biological Psychiatry 2009, 66(11):1013-1022. doi: S0006-3223(09)00730-6 [pii] 10.1016/j.biopsych.2009.06.005.
34. Meyer U., Murray P.J., Urwyler A., Yee B.K., Schedlowski M., Feldon J. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Molecular Psychiatry 2008, 13(2):208-221. doi: 4002042 [pii] 10.1038/sj.mp. 4002042.
35. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: The role of cytokines in the pathophysiology of major depression. Biological Psychiatry 2009, 65(9):732-741. doi: S0006-3223(08)01532-1 [pii] 10.1016/j.biopsych.2008.11.029.
36. Mullington J., Korth C., Hermann D.M., Orth A., Galanos C., Holsboer F., et al. Dose-dependent effects of endotoxin on human sleep. American Journal of Physiology - Regulatory Integrative and Comperative Physiology 2000, 278(4):R947-R955.
37. Pugh C.R., Kumagawa K., Fleshner M., Watkins L.R., Maier S.F., Rudy J.W. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain, Behavior and Immunity 1998, 12(3):212-229. doi: S0889-1591(98)90524-4 [pii] 10.1006/brbi.1998.0524.
38. Quan N. Immune-to-brain signaling: How important are the blood-brain barrier-independent pathways?. Molecular Neurobiology 2008, 37(2-3):142-152. 10.1007/s12035-008-8026-z.
39. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends in Immunology 2006, 27(1):24-31. doi: S1471-4906(05)00288-7 [pii] 10.1016/j.it.2005.11.006.
40. Rasch B., Spalek K., Buholzer S., Luechinger R., Boesiger P., Papassotiropoulos A., et al. 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 of the United States of America 2009, 106(45):19191-19196. doi: 0907425106 [pii] 10.1073/pnas.0907425106.
41. Reichenberg A., Yirmiya R., Schuld A., Kraus T., Haack M., Morag A., et al. Cytokine-associated emotional and cognitive disturbances in humans. Archives of General Psychiatry 2001, 58(5):445-452. doi: yoa20072 [pii].
42. Scullion G.A., Kendall D.A., Sunter D., Marsden C.A., Pardon M.C. Central noradrenergic depletion by DSP-4 prevents stress-induced memory impairments in the object recognition task. Neuroscience 2009, 164(2):415-423. doi: S0306-4522(09)01337-2 [pii] 10.1016/j.neuroscience.2009.08.046.
43. Segal S.K., Cahill L. Endogenous noradrenergic activation and memory for emotional material in men and women. Psychoneuroendocrinology 2009, 34(9):1263-1271. doi: S0306-4530(09)00150-4 [pii] 10.1016/j.psyneuen.2009.04.020.
44. Seruga B., Zhang H., Bernstein L.J., Tannock I.F. Cytokines and their relationship to the symptoms and outcome of cancer. Nature Reviews Cancer 2008, 8(11):887-899. doi: nrc2507 [pii] 10.1038/nrc2507.
45. Sobrinho L.G. The psychogenic effects of prolactin. Acta Endocrinologica (Copenhagen) 1993, 129(Suppl 1):38-40.
46. Stroop J.R. Studies of interference in serial verbal reactions. Journal of Experimental Psychology 1935, 18:643-662.
47. Turnbull A.V., Rivier C. Regulation of the HPA axis by cytokines. Brain, Behavior and Immunity 1995, 9(4):253-275. doi: S0889-1591(85)71026-4 [pii] 10.1006/brbi.1995.1026.
48. Wechsler D. Manual for the Wechsler memory scale-revised 1987, Psychological Corporation, San Antonio, TX.
49. Wirtz P.H., Ehlert U., Bartschi C., Redwine L.S., von Kanel R. Changes in plasma lipids with psychosocial stress are related to hypertension status and the norepinephrine stress response. Metabolism 2009, 58(1):30-37. doi: S0026-0495(08)00317-X [pii] 10.1016/j.metabol.2008.08.003.
50. Wolf O.T. Stress and memory in humans: Twelve years of progress?. Brain Research 2009, 1293:142-154. doi: S0006-8993(09)00768-9 [pii] 10.1016/j.brainres.2009.04.013.
51. Wright C.E., Strike P.C., Brydon L., Steptoe A. Acute inflammation and negative mood: Mediation by cytokine activation. Brain, Behavior and Immunity 2005, 19(4):345-350. doi: S0889-1591(04)00133-3 [pii] 10.1016/j.bbi.2004.10.003.