When words are painful: Unraveling the mechanisms of the nocebo effect

Neuroscience

Volumn 147, Issue 2, 2007, Pages 260-271

  Benedetti, F ^a   Lanotte, M ^a   Lopiano, L ^a   Colloca, L ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

anxiety; cholecystokinin; endogenous opioids; pain; Parkinson's disease; placebo

Indexed keywords

CHOLECYSTOKININ; CHOLECYSTOKININ RECEPTOR BLOCKING AGENT; DIAZEPAM; PLACEBO; PROGLUMIDE;

ANXIETY; COGNITION; DIAGNOSTIC APPROACH ROUTE; DISEASE SEVERITY; DOCTOR PATIENT RELATION; DRUG EFFECT; EMOTION; HUMAN; HYPERALGESIA; MEDICAL ETHICS; NEUROBIOLOGY; NEUROIMAGING; OUTCOME ASSESSMENT; PAIN; PRIORITY JOURNAL; REVIEW;

ANIMALS; BRAIN; CHOLECYSTOKININ; COGNITION; EMOTIONS; FEAR; HUMANS; HYPERALGESIA; MAGNETIC RESONANCE IMAGING; PAIN; PARKINSON DISEASE;

EID: 34250204872     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.02.020     Document Type: Review

References (84)

1. Amanzio M., and Benedetti F. Neuropharmacological dissection of placebo analgesia: expectation-activated opioid systems versus conditioning-activated specific sub-systems. J Neurosci 19 (1999) 484-494
2. Amanzio M., Pollo A., Maggi G., and Benedetti F. Response variability to analgesics: a role for non-specific activation of endogenous opioids. Pain 90 (2001) 205-215
3. Andre J., Zeau B., Pohl M., Cesselin F., Benoliel J.J., and Becker C. Involvement of cholecystokininergic systems in anxiety-induced hyperalgesia in male rats: behavioral and biochemical studies. J Neurosci 25 35 (2005) 7896-7904
4. Baber N.S., Dourish C.T., and Hill D.R. The role of CCK caerulein, and CCK antagonists in nociception. Pain 39 3 (1989) 307-328
5. Barsky A.J., Saintfort R., Rogers M.P., and Borus J.F. Nonspecific medication side effects and the nocebo phenomenon. JAMA 287 (2002) 622-627
6. Beinfeld M.C. Cholecystokinin in the central nervous system: a minireview. Neuropeptides 3 6 (1983) 411-427
7. Benedetti F., Amanzio M., and Maggi G. Potentiation of placebo analgesia by proglumide. Lancet 346 (1995) 1231
8. Benedetti F. The opposite effects of the opiate antagonist naloxone and the cholecystokinin antagonist proglumide on placebo analgesia. Pain 64 (1996) 535-543
9. Benedetti F. Cholecystokinin type-A and type-B receptors and their modulation of opioid analgesia. News Physiol Sci 12 (1997) 263-268
10. Benedetti F., and Amanzio M. The neurobiology of placebo analgesia: from endogenous opioids to cholecystokinin. Progr Neurobiol 52 (1997) 109-125
11. Benedetti F., Amanzio M., Vighetti S., and Asteggiano G. The biochemical and neuroendocrine bases of the hyperalgesic nocebo effect. J Neurosci 26 46 (2006) 12014-12022
12. Benedetti F., Amanzio M., Casadio C., Oliaro A., and Maggi G. Blockade of nocebo hyperalgesia by the cholecystokinin antagonist proglumide. Pain 71 (1997) 135-140
13. Benedetti F., Arduino C., and Amanzio M. Somatotopic activation of opioid systems by target-directed expectations of analgesia. J Neurosci 19 (1999) 3639-3648
14. Benedetti F., Colloca L., Torre E., Lanotte M., Melcarne A., Pesare M., Bergamasco B., and Lopiano L. Placebo-responsive Parkinson patients show decreased activity in single neurons of subthalamic nucleus. Nat Neurosci 7 (2004) 587-588
15. Benedetti F., and Colloca L. Placebo-induced analgesia: methodology, neurobiology, clinical use, and ethics. Rev Analg 7 (2004) 129-143
16. Benedetti F., Maggi G., Lopiano L., Lanotte M., Rainero I., Vighetti S., and Pollo A. Open versus hidden medical treatments: the patient's knowledge about a therapy affects the therapy outcome. Prevent Treat (2003). http://journals.apa.org/prevention/volume6/toc-jun-03.html Available online at: http://journals.apa.org/prevention/volume6/toc-jun-03.html
17. Benedetti F., Pollo A., Lopiano L., Lanotte M., Vighetti S., and Rainero I. Conscious expectation and unconscious conditioning in analgesic, motor and hormonal placebo/nocebo responses. J Neurosci 23 (2003) 4315-4323
18. Benedetti F., Mayberg H.S., Wager T.D., Stohler C.S., and Zubieta J.K. Neurobiological mechanisms of the placebo effect. J Neurosci 25 45 (2005) 10390-10402
19. Chiodo L.A., and Bunney B.S. Proglumide: selective antagonism of excitatory effects of cholecystokinin in the central nervous system. Science 219 4591 (1983) 1449-1451
20. Chua P., Krams M., Toni I., Passingham R., and Dolan R. A functional anatomy of anticipatory anxiety. Neuroimage 9 6 Pt 1 (1999) 563-571
21. Colloca L., Lopiano L., Lanotte M., and Benedetti F. Overt versus covert treatment for pain, anxiety, and Parkinson's disease. Lancet Neurol 3 11 (2004) 679-684
22. Colloca L., and Benedetti F. Placebos and painkillers: is mind as really as matter?. Nat Rev Neurosci 6 7 (2005) 545-552
23. Crawley J.N., and Corwin R.L. Biological actions of cholecystokinin. Peptides 15 4 (1994) 731-755
24. Dannecker E.A., Price D.D., and Robinson M.E. An examination of the relationships among recalled, expected, and actual intensity and unpleasantness of delayed onset muscle pain. J Pain 4 2 (2003) 74-81
25. de la Fuente-Fernandez R., Ruth T.J., Sossi V., Schulzer M., Calne D.B., and Stoessl A.J. Expectation and dopamine release: mechanism of the placebo effect in Parkinson's disease. Science 293 (2001) 1164-1166
26. Dourish C.T., Hawley D., and Iversen S.D. Enhancement of morphine analgesia and prevention of morphine tolerance in the rat by the cholecystokinin antagonist L-364,718. Eur J Pharmacol 147 (1988) 469-472
27. Dworkin S.F., Chen A.C., LeResche L., and Clark D.W. Cognitive reversal of expected nitrous oxide analgesia for acute pain. Anesth Analg 62 (1983) 1073-1077
28. Finniss D.G., and Benedetti F. Mechanisms of the placebo response and their impact on clinical trials and clinical practice. Pain 114 (2005) 3-6
29. Flaten M.A., Simonsen T., and Olsen H. Drug-related information generates placebo and nocebo responses that modify the drug response. Psychosom Med 61 2 (1999) 250-255
30. Frith C., and Dolan R.J. Brain mechanisms associated with top-down processes in perception. Philos Trans R Soc Lond B Biol Sci 352 1358 (1997) 1221-1230
31. Gall C., Lauterborn J., Burks D., and Seroogy K. Co-localization of enkephalin and cholecystokinin in discrete areas of rat brain. Brain Res 403 2 (1987) 403-408
32. Gibbins I.L., Furness J.B., and Costa M. Pathway-specific patterns of the co-existence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 248 2 (1987) 417-437
33. Grevert P., Albert L.H., and Goldstein A. Partial antagonism of placebo analgesia by naloxone. Pain 16 (1983) 129-143
34. Hahn RA (1985) A sociocultural model of illness and healing. In: L. White, Tursky, B., Schwartz, G.E. (eds.), Placebo: Theory, Research, and Mechanisms, Guilford, New York, pp. 332-350.
35. Hahn R.A. The nocebo phenomenon: concept, evidence, and implications for public health. Prev Med 26 5 Pt 1 (1997) 607-611
36. Harro J., Pold M., and Vasar E. Anxiogenic-like action of caerulein, a CCK-8 receptor agonist, in the mouse: influence of acute and subchronic diazepam treatment. Naunyn Schmiedebergs Arch Pharmacol 341 1-2 (1990) 62-67
37. Harro J., and Vasar E. Evidence that CCK-B receptors mediate the regulation of exploratory behaviour in the rat. Eur J Pharmacol 193 3 (1991) 379-381
38. Hebb A.L.O., Poulin J.-F., Roach S.P., Zacharko R.M., and Drolet G. Cholecystokinin and endogenous opioid peptides: interactive influence on pain, cognition, and emotion. Prog Neuropsychopharmacol Biol Psychiatry 29 (2005) 1225-1238
39. Heinricher M.M., McGaraughty S., and Tortorici V. Circuitry underlying antiopioid actions of cholecystokinin within the rostral ventromedial medulla. J Neurophysiol 85 (2001) 280-286
40. Heinricher M.M., and Neubert M.J. Neural basis for the hyperalgesic action of cholecystokinin in the rostral ventromedial medulla. J Neurophysiol 92 (2004) 1982-1989
41. Hoffman G.A., Harrington A., and Fields H.L. Pain and the placebo: what we have learned. Perspect Biol Med 48 2 (2005) 248-265
42. Hsieh J.C., Stone-Elander S., and Ingvar M. Anticipatory coping of pain expressed in the human anterior cingulated cortex: a positron emission tomography study. Neurosci Lett 262 1 (1999) 61-64 26
43. Kantor T.G., Sunshine A., Laska E., Meisner M., and Hopper M. Oral analgesic studies: pentazocine hydrochloride, codeine, aspirin, and placebo and their influence on response to placebo. Clin Pharmacol Ther 7 4 (1966) 447-454
44. Keltner J.R., Furst A., Fan C., Redfern R., Inglis B., and Fields H.L. Isolating the modulatory effect of expectation on pain transmission: a functional magnetic resonance imaging study. J Neurosci 26 16 (2006) 4437-4443
45. Kennedy W.P. The nocebo reaction. Med Exp Int J Exp Med 95 (1961) 203-205
46. Kissel P., and Barrucand D. Placebos et effect placebo en medicine (1964), Masson, Paris
47. Koyama T., Tanaka Y.Z., and Mikami A. Nociceptive neurons in the macaque anterior cingulated activate during anticipation of pain. Neuroreport 9 11 (1998) 2663-2667
48. Koyama T., McHaffie J.G., Laurienti P.J., and Coghill R.C. The subjective experience of pain: where expectations become reality. Proc Natl Acad Sci U S A 102 36 (2005) 12950-12955
49. Laska E., and Sunshine A. Anticipation of analgesia. A placebo effect. Headache 13 1 (1973) 1-11
50. Lavigne G.J., Hargreaves K.M., Schmidt E.A., and Dionne R.A. Proglumide potentiates morphine analgesia for acute postsurgical pain. Clin Pharmacol Ther 45 6 (1989) 666-673
51. Leuchter A.F., Cook I.A., Witte E.A., Morgan M., and Abrams M. Changes in brain function of depressed subjects during treatment with placebo. Am J Psychiatry 159 (2002) 122-129
52. Levine J.D., Gordon N.C., and Fields H.L. The mechanism of placebo analgesia. Lancet 2 8091 (1978) 654-657
53. Levine J.D., Gordon N.C., Smith R., and Fields H.L. Analgesic responses to morphine and placebo in individuals with postoperative pain. Pain 10 3 (1981) 379-389
54. Lorenz J., Hauck M., Paur R.C., Nakamura Y., Zimmermann R., Bromm B., and Engel A.K. Cortical correlates of false expectations during pain intensity judgments: a possible manifestation of placebo/nocebo cognitions. Brain Behav Immun 19 4 (2005) 283-295
55. Maldonado R., Derrien M., Noble F., and Roques B.P. Association of the peptidase inhibitor RB 101 and CCK-B antagonist strongly enhances antinociceptive responses. Neuroreport 4 7 (1993) 947-950
56. Mayberg H.S., Silva J.A., Brannan S.K., Tekell J.L., Mahurin R.K., McGinnis S., and Jerabek P.A. The functional neuroanatomy of the placebo effect. Am J Psychiatry 159 5 (2002) 728-737
57. Mercado R., Constantoyannis C., Mandat T., Kumar A., Schulzer M., Stoessl A.J., and Honey C.R. Expectation and the placebo effect in Parkinson's disease patients with subthalamic nucleus deep brain stimulation. Mov Disord 21 9 (2006) 1457-1461
58. Mesulam M.M. From sensation to cognition. Brain 121 Pt 6 (1998) 1013-1052
59. Mitchell J.M., Lowe D., and Fields H.L. The contribution of the rostral ventromedial medulla to the antinociceptive effects of systemic morphine in restrained and unrestrained rats. Neuroscience 87 (1998) 123-133
60. Noble F., Derrien M., and Roques B.P. Modulation of opioid antinociception by CCK at the supraspinal level: evidence of regulatory mechanisms between CCK and enkephalin systems in the control pain. Br J Pharmacol 109 4 (1993) 1064-1070
61. Noble F., Wank S.A., Crawley J.N., Bradwejn J., Seroogy K.B., Hamon M., Roques B.P., and International Union of Pharmacology. XXI. Structure, disribution, and functions of cholecystokinin receptors. Pharmacol Rev 51 (1999) 745-781
62. Pacheco-Lopez G., Engler H., Niemi M.B., and Schedlowski M. Expectations and associations that heal: immunomodulatory placebo effects and its neurobiology. Brain Behav Immun 20 5 (2006) 430-446
63. Pessoa L., Kastner S., and Ungerleider L.G. Neuroimaging studies of attention: from modulation of sensory processing to top-down control. J Neurosci 23 10 (2003) 3990-3998
64. Petrovic P., Kalso E., Petersson K.M., and Ingvar M. Placebo and opioid analgesia: imaging a shared neuronal network. Science 295 5560 (2002) 1737-1740
65. Ploghaus A., Tracey I., Gati J.S., Clare S., Menon R.S., Matthews P.M., and Rawlins J.N. Dissociating pain from its anticipation in the human brain. Science 284 5422 (1999) 1979-1981
66. Pollo A., Torre E., Lopiano L., Rizzone M., Lanotte M., Cavanna A., Bergamasco B., and Benedetti F. Expectation modulates the response to subthalamic nucleus stimulation in Parkinsonian patients. Neuroreport 13 11 (2002) 1383-1386
67. Porro C.A., Baraldi P., Pagnoni G., Serafini M., Facchin P., Maieron M., and Nichelli P. Does anticipation of pain affect cortical nociceptive systems?. J Neurosci 22 8 (2002) 3206-3214
68. Porro C.A., Cettolo V., Francescato M.P., and Baraldi P. Functional activity mapping of the mesial hemispheric wall during anticipation of pain. Neuroimage 19 4 (2003) 1738-1747
69. Price D.D., von der Gruen A., Miller J., Rafii A., and Price C. Potentiation of systemic morphine analgesia in humans by proglumide, a cholecystokinin antagonist. Anesth Analg 64 8 (1985) 801-806
70. Price D.D. Psychological and neural mechanisms of the affective dimension of pain. Science 288 5472 (2000) 1769-1772
71. Price D.D. Assessing placebo effects without placebo groups: an untapped possibility?. Pain 90 3 (2001) 201-203
72. Price D.D., Craggs J., Nicholas Verne G., Perlstein W.M., and Robimson M.E. Placebo analgesia is accompanied by large reductions in pain-related brain activity in irritable bowel syndrome patients. Pain 127 1-2 (2006) 63-72
73. Sawamoto N., Honda M., Okada T., Hanakawa T., Kanda M., Fukuyama H., Konishi J., and Shibasaki H. Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulated cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. J Neurosci 20 19 (2000) 7438-7445
74. Stengaard-Pedersen K., and Larsson L.I. Localization and opiate binding of enkephalin, CCK and ACTH/beta-endorphin in the rat central nervous system. Peptides 2 Suppl 1 (1981) 3-19
75. Suberg S.N., Culhane E.S., Carstens E., and Watkins L.R. Behavioral and electrophysiological investigations of opiate/cholecystokinin interactions. In: Fields H.L., Dubner R., and Cervero F. (Eds). Advances in pain research and therapy Vol 9 (1985), Raven, New York 541-553
76. Valverde O., Maldonado R., Fournie-Zaluski M.C., and Roques B.P. Cholecystokinin B antagonists strongly potentiate antinociception mediated by endogenous enkephalins. J Pharmacol Exp Ther 270 1 (1994) 77-88
77. Vanderhaeghen J.J., Signeau J.C., and Gepts W. New peptide in the vertebrate CNS reacting with antigastrin antibodies. Nature 257 5527 (1975) 604-605
78. van Megen H.J., den Boer J.A., and Westenberg H.G. On the significance of cholecystokinin receptors in panic disorder. Prog Neuropsychopharmacol Biol Psychiatry 18 8 (1994) 1235-1246
79. Wager T.D., Rilling J.K., Smith E.E., Sokolik A., Casey K.L., Davidson R.J., Kosslyn S.M., Rose R.M., and Cohen J.D. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303 5661 (2004) 1162-1167
80. Watkins L.R., Kinscheck I.B., and Mayer D.J. Potentiation of morphine analgesia by the cholecystokinin antagonist proglumide. Brain Res 327 1-2 (1985) 169-180
81. Watkins L.R., Kinscheck I.B., Kaufman E.F., Miller J., Frenk H., and Mayer D.J. Cholecystokinin antagonists selectively potentiate analgesia induced by endogenous opiates. Brain Res 327 1-2 (1985) 181-190
82. Wiesenfeld-Hallin Z., Xu X.J., Hughes J., Horwell D.C., and Hokfelt T. PD134308, a selective antagonist of cholecystokinin type B receptor, enhances the analgesic effect of morphine and synergistically interacts with intrathecal galanin to depress spinal nociceptive reflexes. Proc Natl Acad Sci U S A 87 18 (1990) 7105-7109
83. Xu X.J., Hokfelt T., Hughes J., and Wiesenfeld-Hallin Z. The CCK-B antagonist CI988 enhances the reflex-depressive effect of morphine in axotomized rats. Neuroreport 5 6 (1994) 718-720
84. Zubieta J.K., Bueller J.A., Jackson L.R., Scott D.J., Xu Y., Koeppe R.A., Nichols T.E., and Stohler C. Placebo effects mediated by endogenous opioid activity on μ-opioid receptors. J Neurosci 25 34 (2005) 7754-7762