Learned immunosuppression: Extinction, renewal, and the challenge of reconsolidation

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 1, 2013, Pages 180-188

  Hadamitzky, Martin ^a   Engler, Harald ^a   Schedlowski, Manfred ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Conditioned taste aversion; Cyclosporine A; Extinction; Immunosuppression; Renewal

Indexed keywords

ANISOMYCIN; CELL RECEPTOR; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; GAMMA INTERFERON; INTERLEUKIN 2; PROPRANOLOL; SACCHARIN;

ADRENERGIC SYSTEM; ANTIBODY PRODUCTION; ARTHRITIS; BEHAVIOR; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTACT ALLERGY; CYTOKINE PRODUCTION; EFFERENT NERVE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INSULA; LATERAL HYPOTHALAMUS; LUPUS ERYTHEMATOSUS; LYMPHOCYTE PROLIFERATION; MULTIPLE SCLEROSIS; NERVE ENDING; ORGAN TRANSPLANTATION; PARABRACHIAL NUCLEUS; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SCLEROSIS; SENSORY NERVE; SOLITARY TRACT NUCLEUS; STATE DEPENDENT LEARNING; TUMOR GROWTH;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR; BRAIN; CONDITIONING (PSYCHOLOGY); CYCLOSPORINE; EXTINCTION, PSYCHOLOGICAL; HUMANS; IMMUNE TOLERANCE; IMMUNOSUPPRESSIVE AGENTS; LEARNING; NEURAL PATHWAYS; RATS; TASTE;

EID: 84874658783     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-012-9388-6     Document Type: Review

References (100)

1. Acosta JI, Thiel KJ, Sanabria F, Browning JR, Neisewander JL (2008) Effect of schedule of reinforcement on cue-elicited reinstatement of cocaine-seeking behavior. Behav Pharmacol 19:129-136
2. Ader R (2003) Conditioned immunomodulation: research needs and directions. Brain Behav Immun 17:51-57
3. Ader R, Cohen N (1975) Behaviorally conditioned immunosuppression. Psychosom Med 37:333-340
4. Ader R, Cohen N (1982) Behaviorally conditioned immunosuppression and murine systemic lupus erythematosus. Science 215:1534-1536
5. Ader R, Mercurio MG, Walton J, James D, Davis M, Ojha V, Kimball AB, Fiorentino D (2010) Conditioned pharmacotherapeutic effects: a preliminary study. Psychosom Med 72:192-197
6. Bahar A, Dorfman N, Dudai Y (2004) Amygdalar circuits required for either consolidation or extinction of taste aversion memory are not required for reconsolidation. Eur J Neurosci 19:1115-1118
7. Banks WA (2005) Blood-brain barrier transport of cytokines: a mechanism for neuro-pathology. Curr Pharm Des 11:973-984
8. Batiuk TD, Halloran PF (1997) The downstream consequences of calcineurin inhibition. Transplan Proc 29:1239-1240
9. Berman DE, Dudai Y (2001) Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291:2417-2419
10. Berman DE, Hazvi S, Stehberg J, Bahar A, Dudai Y (2003) Conflicting processes in the extinction of conditioned taste aversion: behavioral and molecular aspects of latency, apparent stagnation, and spontaneous recovery. Learn Mem 10:16-25
11. Bermúdez-Rattoni F (2004) Molecular mechanisms of taste-recognition memory. Nat Rev Neurosci 5:209-217
12. Bermúdez-Rattoni F, McGaugh JL (1991) Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion. Brain Res 549:165-170
13. Blalock JE, Smith EM (2007) Conceptual development of the immune system as a sixth sense. Brain Behav Immun 21:23-33
14. Bouton ME, Westbrook RF, Corcoran KA, Maren S (2006) Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol Psychiatry 60:352-360
15. Bovbjerg D (2003) Conditioning, cancer, and immune regulation. Brain Behav Immun 17:58-S61
16. Brynskikh A, Warren T, Zhu J, Kipnis J (2008) Adaptive immunity affects learning behavior in mice. Brain Behav Immun 22:861-869
17. Buske-Kirschbaum A, Kirschbaum C, Stierle H, Lehnert H, Hellhammer D (1992) Conditioned increase of natural killer cell activity (NKCA) in humans. Psychosom Med 54:123-132
18. Cefalu WT, Pardridge WM (1985) Restrictive transport of a lipid-soluble peptide (Cyclosporin) through the blood-brain-barrier. J Neurochem 45:1954-1956
19. Chen J, Lin W, Wang W, Shao F, Yang J, Wang B, Kuang F, Duan X, Ju G (2004) Enhancement of antibody production and expression of c-Fos in the insular cortex in response to a conditioned stimulus after a single-trial learning paradigm. Behav Brain Res 154:557-565
20. Colloca L, Benedetti F (2005) Placebos and painkillers: is mind as real as matter? Nature Rev 6:545-552
21. Cubero I, Thiele TE, Bernstein IL (1999) Insular cortex lesions and taste aversion learning: effects of conditioning method and timing of lesion. Brain Res 839:323-330
22. Dantzer R, Konsman JP, Bluthe RM, Kelley KW (2000) Neural and humoral pathways of communication from the immune system to the brain: parallel or convergent? Auton Neurosci 85:60-65
23. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46-56
24. Doenlen R, Krügel U, Wirth T, Riether C, Engler A, Prager G, Engler H, Schedlowski M, Pacheco-López G (2011) Electrical activity in rat cortico-limbic structures after single or repeated administration of lipopolysaccharide or staphylococcal enterotoxin B. Proc Biol Sci 278:1864-1872
25. Doering B, Rief W (2012) Utilizing placebo mechanisms for dose reduction in pharmaco-therapy. Trends Pharmacol Sci 33:165-172
26. Dudai Y, Eisenberg M (2004) Rites of passage of the Engram: reconsolidation and the lingering consolidation hypothesis. Neuron 44:93-100
27. Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301:1102-1104
28. Enck P, Benedetti F, Schedlowski M (2008) New insights into the placebo and nocebo responses. Neuron 59:195-206
29. Exton MS, von Horsten S, Schult M, Voge J, Strubel T, Donath S, Steinmuller C, Seeliger H, Nagel E, Westermann J, Schedlowski M (1998) Behaviorally conditioned immunosuppression using cyclosporine A: central nervous system reduces IL-2 production via splenic innervation. J Neuroimmunol 88:182-191
30. Exton MS, Schult M, Donath S, Strubel T, Bode U, del Rey A, Westermann J, Schedlowski M (1999) Conditioned immunosuppression makes subtherapeutic cyclosporin effective via splenic innervation. Am J Physiol 276:1710-1717
31. Exton MS, Elfers A, Jeong WY, Bull DF, Westermann J, Schedlowski M (2000a) Conditioned suppression of contact sensitivity is independent of sympathetic splenic innervation. Am J Physiol Regul Integr Comp Physiol 279:1310-1315
32. Exton MS, von Horsten S, Strubel T, Donath S, Schedlowski M, Westermann J (2000b) Conditioned alterations of specific blood leukocyte subsets are reconditionable. Neuroimmunomodulation 7:106-114
33. Exton MS, Herklotz J, Westermann J, Schedlowski M (2001) Conditioning in the rat: an in vivo model to investigate the molecular mechanisms and clinical implications of brain-immune communication. Immunol Rev 184:226-235
34. Exton MS, Gierse C, Meier B, Mosen M, Xie Y, Frede S, Goebel MU, Limmroth V, Schedlowski M (2002) Behaviorally conditioned immunosuppression in the rat is regulated via noradrenaline and beta-adrenoceptors. J Neuroimmunol 131:21-30
35. Felten SY, Olschowka J (1987) Noradrenergic sympathetic innervation of the spleen: II. Tyrosine hydroxylase (TH)-positive nerve terminals form synapticlike contacts on lymphocytes in the splenic white pulp. J Neurosci Res 18:37-48
36. Garcia J, Kimeldorf DJ, Koelling RA (1955) Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122:157-158
37. Garcia J, Lasiter PS, Bermudez-Rattoni F, Deems DA (1985) A general theory of aversion learning. Ann N Y Acad Sci 443:8-21
38. Garcia-DeLaTorre P, Rodriguez-Ortiz CJ, Arreguin-Martinez JL, Cruz-Castaneda P, Bermudez-Rattoni F (2009) Simultaneous but not independent anisomycin infusions in insular cortex and amygdala hinder stabilization of taste memory when updated. Learn Mem 16:514-519
39. Garg SK, Banerjee R, Kipnis J (2008) Neuroprotective immunity: T cell-derived glutamate endows astrocytes with a neuroprotective phenotype. J Immunol 180:3866-3873
40. Gauci M, Husband AJ, Saxarra H, King MG (1994) Pavlovian conditioning of nasal tryptase release in human subjects with allergic rhinitis. Physiol Behav 55:823-825
41. Giang DW, Goodman AD, Schiffer RB, Mattson DH, Petrie M, Cohen N, Ader R (1996) Conditioning of cyclophosphamide-induced leukopenia in humans. J Neuropsychiatry Clin Neurosci 8:194-201
42. Goebel MU, Trebst AE, Steiner J, Xie YF, Exton MS, Frede S, Canbay AE, Michel MC, Heemann U, Schedlowski M (2002) Behavioral conditioning of immunosuppression is possible in humans. FASEB J 16:1869-1873
43. Goebel MU, Meykadeh N, Kou W, Schedlowski M, Hengge UR (2008) Behavioral conditioning of antihistamine effects in patients with allergic rhinitis. Psychother Psychosom 77:227-234
44. Goehler LE, Gaykema RP, Hansen MK, Anderson K, Maier SF, Watkins LR (2000) Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton Neurosci 85:49-59
45. Goehler LE, Erisir A, Gaykema RP (2006) Neural-immune interface in the rat area postrema. Neuroscience 140:1415-1434
46. Goehler LE, Lyte M, Gaykema RP (2007) Infection-induced viscerosensory signals from the gut enhance anxiety: implications for psychoneuroimmunology. Brain Behav Immun 21:721-726
47. Gottschalk S, Cummins CL, Leibfritz D, Christians U et al (2010) Age and sex differences in the effects of the immunosuppressants cyclosporine, sirolimus and everolimus on rat brain metabolism. Neurotoxicology 32:50-57
48. Halloran PF, Helms LM, Kung L, Noujaim J (1999) The temporal profile of calcineurin inhibition by cyclosporine in vivo. Transplantation 68:1356-1361
49. Hansen MK, Daniels S, Goehler LE, Gaykema RP, Maier SF, Watkins LR (2000) Subdiaphragmatic vagotomy does not block intraperitoneal lipopolysaccharide- induced fever. Auton Neurosci 85:83-87
50. Hiramoto R, Hiramoto N, Rish M, Soong S, Miller D, Ghanta V (1991) Role of immune cells in the Pavlovian conditioning of specific resistance to cancer. Int J Neurosci 59:101-117
51. Kapturczak MH, Meier-Kriesche HU, Kaplan B (2004) Pharmacology of calcineurin antagonists. Transplant Proc 36:25-32
52. Klosterhalfen W, Klosterhalfen S (1983) Pavlovian conditioning of immunosuppression modifies adjuvant arthritis in rats. Behav Neurosci 97:663-666
53. Klosterhalfen S, Klosterhalfen W (1990) Conditioned cyclosporine effects but not conditioned taste aversion in immunized rats. Behav Neurosci 104:716-724
54. Leech J, Mazzone SB, Farrell MJ (2012) The effect of placebo conditioning on capsaicin-evoked urge-to-cough. Chest. doi: 10.1378
55. Longo DL, Duffey PL, Kopp WC, Heyes MP, Alvord WG, Sharfman WH, Schmidt PJ, Rubinow DR, Rosenstein D (1999) Conditioned immune response to interferon-gamma in humans. Clin Immunol 90:173-181
56. Lyson T, McMullan DM, Ermel LD, Morgan BJ, Victor RG (1994) Mechanism of cyclosporine-induced sympathetic activation and acute hypertension in rats. Hypertension 23:667-675
57. Maier SF, Goehler LE, Fleshner M, Watkins LR (1998) The role of the vagus nerve in cytokine-to-brain communication. Ann N Y Acad Sci 840:289-300
58. McCaffrey PG, Luo C, Kerppola TK, Jain J, Badalian TM, Ho AM, Burgeon E, Lane WS, Lambert JN, Curran T (1993) Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262:750-754
59. Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinction- reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324:951-955
60. Moss NG, Powell SL, Falk RJ (1985) Intravenous cyclosporine activates afferent and efferent renal nerves and causes sodium retention in innervated kidneys in rats. Proc Natl Acad Sci U S A 82:8222-8226
61. Myers KM, Carlezon WA Jr (2010) Extinction of drug- and withdrawal-paired cues in animal models: relevance to the treatment of addiction. Neurosci Biobehav Rev 35:285-302
62. Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10:224-234
63. Nance DM, Sanders VM (2007) Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav Immun 21:736-745
64. Ober K, Benson S, Vogelsang M, Bylica A, Günther D, Witzke O, Kribben A, Engler H, Schedlowski M (2012) Plasma noradrenaline and state anxiety levels predict placebo response in learned immunosuppression. Clin Pharmacol Ther 91:220-226
65. Pacheco-López G, Bermúdez-Rattoni F (2011) Brain-immune interactions and the neural basis of disease-avoidant ingestive behaviour. Philos Trans R Soc Lond B Biol Sci 366:3389-3405
66. Pacheco-López G, Niemi MB, Kou W, Härting M, Fandrey J, Schedlowski M (2005) Neural substrates for behaviorally conditioned immunosuppression in the rat. J Neurosci 25:2330-2337
67. Pacheco-López G, Engler H, Niemi MB, Schedlowski M (2006) Expectations and associations that heal: immunomodulatory placebo effects and its neurobiology. Brain Behav Immun 20:430-446
68. Pacheco-López G, Riether C, Doenlen R, Engler H, Niemi MB, Engler A, Kavelaars A, Heijnen CJ, Schedlowski M (2009) Calcineurin inhibition in splenocytes induced by pavlovian conditioning. FASEB J 23:1161-1167
69. Pacheco-López G, Doenlen R, Krügel U, Arnold M, Wirth T, Riether C, Engler A, Niemi MB, Christians U, Engler H, Schedlowski M (2012) Neurobehavioural activation during peripheral immunosuppression. Int J Neuropsychopharmacol 5:1-13
70. Pavlov I (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. Oxford University Press, Cambridge
71. Ramírez-Amaya V, Bermúdez-Rattoni F (1999) Conditioned enhancement of antibody production is disrupted by insular cortex and amygdala but not hippocampal lesions. Brain Behav Immun 13:46-60
72. Rief W, Bingel U, Schedlowski M, Enck P (2011) Mechanisms involved in placebo and nocebo responses and implications for drug trials. Clin Pharmacol Ther 90:722-726
73. Riether C, Doenlen R, Pacheco-Lopez G, Niemi MB, Engler A, Engler H, Schedlowski M (2008) Behavioural conditioning of immune functions: how the central nervous system controls peripheral immune responses by evoking associative learning processes. Rev Neurosci 19:1-17
74. Riether C, Kavelaars A, Wirth T, Pacheco-López G, Doenlen R, Willemen H, Cj Heijnen, Schedlowski M, Engler H (2011) Stimulation of β2-adrenergic receptors inhibits calcineurin activity in CD4+ T cells via PKA-AKAP interaction. Brain Behav Immun 25:59-66
75. Romanovsky AA (2000) Thermoregulatory manifestations of systemic inflammation: lessons from vagotomy. Auton Neurosci 85:39-48
76. Romanovsky AA, Simons CT, Szekely M, Kulchitsky VA (1997) The vagus nerve in the thermoregulatory response to systemic inflammation. Am J Physiol 273:407-413
77. Romanovsky AA, Ivanov AI, Lenczowski MJ, Kulchitsky VA, Van Dam AM, Poole S, Homer LD, Tilders FJ (2000) Lipopolysaccharide transport from the peritoneal cavity to the blood: is it controlled by the vagus nerve? Auton Neurosci 85:133-140
78. Rosas JM, Bouton ME (1997) Renewal of a conditioned taste aversion upon return to the conditioning context after extinction in another one. Learn Motiv 28:216-229
79. Rosas JM, Bouton ME (1998) Context change and retention interval can have additive, rather than interactive, effects after taste aversion extinction. Psychon Bull Rev 5:79-83
80. Sanders V, Kohm A (2002) Sympathetic nervous system interaction with the immune system. Int Rev Neurobiol 52:17-41
81. Sanders VM, Straub RH (2002) Norepinephrine, the beta-adrenergic receptor, and immunity. Brain Behav Immun 16:290-332
82. Sandler AD, Glesne CE, Bodfish JW (2010) Conditioned placebo dose reduction: a new treatment in attention-deficit hyperactivity disorder? J Dev Behav Pediatr 31:369-375
83. Sato Y, Takayanagi Y, Onaka T, Kobayashi E (2007) Impact of cyclosporine upon emotional and social behavior in mice. Transplantation 83:1365-1370
84. Schedlowski M, Pacheco-Lopez G (2010) The learned immune response: Pavlov and beyond. Brain Behav Immun 24:176-185
85. Schedlowski M, Hosch W, Oberbeck R, Benschop RJ, Jacobs R, Raab HR, Schmidt RE (1996) Catecholamines modulate human NK cell circulation and function via spleen-independent beta 2-adrenergic mechanisms. J Immunol 156:93-99
86. Schiller D, Monfils MH, Raio CM, Johnson DC, Ledoux JE, Phelps EA (2010) Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463:49-53
87. Sewards TV (2004) Dual separate pathways for sensory and hedonic aspects of taste. Brain Res Bull 62:271-283
88. Sewards TV, Sewards MA (2001) Cortical association areas in the gustatory system. Neurosci Biobehav Rev 25:395-407
89. Simon SA, de Araujo IE, Gutierrez R, Nicolelis MA (2006) The neural mechanisms of gustation: a distributed processing code. Nat Rev Neurosci 7:890-901
90. Smith GR Jr, McDaniel SM (1983) Psychologically mediated effect on the delayed hypersensitivity reaction to tuberculin in humans. Psychosom Med 45:65-70
91. Spector N (1996) Neuroimmunomodulation: a brief review. Can conditioning of natural killer cell activity reverse cancer and/or aging? Regul Toxicol Pharmacol 24:32-38
92. Steinbach WJ, Reedy JL, Cramer RA, Perfect JR, Heitma J (2007) Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections. Nat Rev Microbiology 5:418-430
93. Tracey KJ (2010) Understanding immunity requires more than immunology. Nat Immunol 11:561-564
94. Tronson NC, Taylor JR (2007) Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 8:262-275
95. von Horsten S, Exton MS, Voge J, Schult M et al (1998) Cyclosporine A affects open field behavior in DA rats. Pharmacol Biochem Behav 60:71-76
96. Welzl H, D'Adamo P, Lipp HP (2001) Conditioned taste aversion as a learning and memory paradigm. Behav Brain Res 125:205-213
97. Wirth T, Ober K, Prager G, Vogelsang M, Benson S, Witzke O, Kribben A, Engler H, Schedlowski M (2011) Repeated recall of learned immunosuppression: evidence from rats and men. Brain Behav Immun 25:1444-1451
98. Yamamoto T, Shimura T, Sako N, Yasoshima Y, Sakai N (1994) Neural substrates for conditioned taste aversion in the rat. Behav Brain Res 65:123-137
99. Zhang W, Li JL, Hosaka M, Janz R et al (2000) Cyclosporine A-induced hypertension involves synapsin in renal sensory nerve endings. Proc Natl Acad Sci U S A 97:9765-9770
100. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M (2006) Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9:268-275