Predicting individual differences in placebo analgesia: Contributions of brain activity during anticipation and pain experience

Journal of Neuroscience

Volumn 31, Issue 2, 2011, Pages 439-452

  Wager, Tor D ^a   Atlas, Lauren Y ^b   Leotti, Lauren A ^c   Rilling, James K ^d  

^a UNIVERSITY OF COLORADO   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ANALGESIA; ANTICIPATION; ARTICLE; COGNITION; EMOTION; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LIMBIC CORTEX; NOCICEPTION; NORMAL HUMAN; PARIETAL LOBE; PLACEBO EFFECT; PRIORITY JOURNAL;

ANALGESIA; ANALGESICS; ANTICIPATION, PSYCHOLOGICAL; BRAIN; CEREBRAL CORTEX; CLUSTER ANALYSIS; DATA INTERPRETATION, STATISTICAL; HUMANS; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; NERVE NET; PAIN; PLACEBO EFFECT; REGRESSION ANALYSIS;

EID: 78651477824     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3420-10.2011     Document Type: Article

References (93)

1. Alexander MP, Stuss DT, Picton T, Shallice T, Gillingham S (2007) Regional frontal injuries cause distinct impairments in cognitive control. Neurology 68:1515-1523.
2. Amanzio M, Benedetti F (1999) Neuropharmacological dissection of placebo analgesia: Expectation-activated opioid systems versus conditioningactivated specific subsystems. J Neurosci 19:484-494.
3. Aslaksen PM, Flaten MA (2008) The roles of physiological and subjective stress in the effectiveness of a placebo on experimentally induced pain. Psychosom Med 70:811-818.
4. Atlas LY, Bolger N, Lindquist MA, Wager TD (2010) Brain mediators of predictive cue effects on perceived pain. J Neurosci 30:12964-12977.
5. Beecher HK (1955) The powerful placebo. J AmMed Assoc 159:1602-1606.
6. Benedetti F (2007) Placebo and endogenous mechanisms of analgesia. Handb Exp Pharmacol (177):393-413.
7. Benedetti F, Pollo A, Lopiano L, Lanotte M, Vighetti S, Rainero I (2003) Conscious expectation and unconscious conditioning in analgesic, motor, and hormonal placebo/nocebo responses. J Neurosci 23:4315-4323.
8. Benedetti F, Colloca L, Torre E, Lanotte M, Melcarne A, Pesare M, Bergamasco B, Lopiano L (2004) Placebo-responsive Parkinson patients show decreased activity in single neurons of subthalamic nucleus. Nat Neurosci 7:587-588.
9. Benedetti F, Mayberg HS, Wager TD, Stohler CS, Zubieta JK (2005) Neurobiological mechanisms of the placebo effect. J Neurosci 25:10390-10402.
10. Berns GS, Chappelow J, Cekic M, Zink CF, Pagnoni G, Martin-Skurski ME (2006) Neurobiological substrates of dread. Science 312:754-758.
11. Bijur PE, Silver W, Gallagher EJ (2001) Reliability of the visual analog scale for measurement of acute pain. Acad Emerg Med 8:1153-1157.
12. Bingel U, Lorenz J, Schoell E, Weiller C, Büchel C (2006) Mechanisms of placebo analgesia: RACC recruitment of a subcortical antinociceptive network. Pain 120:8-15.
13. Bishop CM (2006) Pattern recognition and machine learning. New York: Springer.
14. Boly M, Balteau E, Schnakers C, Degueldre C, Moonen G, Luxen A, Phillips C, Peigneux P, Maquet P, Laureys S (2007) Baseline brain activity fluctuations predict somatosensory perception in humans. Proc Natl Acad Sci U S A 104:12187-12192.
15. Brown CA, Seymour B, Boyle Y, El-Deredy W, Jones AK (2008a) Modulation of pain ratings by expectation and uncertainty: Behavioral characteristics and anticipatory neural correlates. Pain 135:240-250.
16. Brown CA, Seymour B, El-Deredy W, Jones AK (2008b) Confidence in beliefs about pain predicts expectancy effects on pain perception and anticipatory processing in right anterior insula. Pain 139:324-332.
17. Buhle J, Wager TD (2010) Performance-dependent inhibition of pain by an executive working memory task. Pain 149:19-26.
18. Chapman CR, Casey KL, Dubner R, Foley KM, Gracely RH, Reading AE (1985) Pain measurement: An overview. Pain 22:1-31.
19. Clark WC, Yang JC, Tsui SL, Ng KF, Bennett Clark S (2002) Unidimensional pain rating scales: A multidimensional affect and pain survey (MAPS) analysis of what they really measure. Pain 98:241-247.
20. Coghill RC, Sang CN, Maisog JM, Iadarola MJ (1999) Pain intensity processing within the human brain: A bilateral, distributed mechanism. J Neurophysiol 82:1934-1943.
21. Colloca L, Benedetti F (2006) How prior experience shapes placebo analgesia. Pain 124:126-133.
22. Colloca L, Tinazzi M, Recchia S, Le Pera D, Fiaschi A, Benedetti F, ValerianiM (2008) Learning potentiates neurophysiological and behavioral placebo analgesic responses. Pain 139:306-314.
23. Colloca L, Petrovic P, Wager TD, Ingvar M, Benedetti F (2010) How the number of learning trials affects placebo and nocebo. Pain 151:430-439.
24. de la Fuente-Fernández R, Ruth TJ, Sossi V, Schulzer M, Calne DB, Stoessl AJ (2001) Expectation and dopamine release: Mechanism of the placebo effect in Parkinson's disease. Science 293:1164-1166.
25. De Pascalis V, Chiaradia C, Carotenuto E (2002) The contribution of suggestibility and expectation to placebo analgesia phenomenon in an experimental setting. Pain 96:393-402.
26. Eippert F, Bingel U, Schoell ED, Yacubian J, Klinger R, Lorenz J, Büchel C (2009a) Activation of the opioidergic descending pain control system underlies placebo analgesia. Neuron 63:533-543.
27. Eippert F, Finsterbusch J, Bingel U, Büchel C (2009b) Direct evidence for spinal cord involvement in placebo analgesia. Science 326:404.
28. Geers AL, Helfer SG, Kosbab K, Weiland PE, Landry SJ (2005) Reconsidering the role of personality in placebo effects: Dispositional optimism, situational expectations, and the placebo response. J Psychosom Res 58: 121-127.
29. Genkin A, Lewis DD, Madigan D (2007) Large-scale Bayesian logistic regression for text categorization. Technometrics 49:291-304.
30. Gracely RH, Dubner R, McGrath PA (1979) Narcotic analgesia: Fentanyl reduces the intensity but not the unpleasantness of painful tooth pulp sensations. Science 203:1261-1263.
31. Grosenick L, Anderson T, Smith SJ (2009) Elastic source selection for in vivo imaging of neuronal ensembles. In: Proceedings of the Sixth IEEE International Symposium on Biomedical Imaging: From Nano to Macro, pp 1263-1266.
32. Hastie T, Tibshirani R, Friedman J, Franklin J (2005) The elements of statistical learning: Data mining, inference and prediction. The Mathematical Intelligencer 27:83-85.
33. Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P (2001) Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293:2425-2430.
34. Hua LH, Strigo IA, Baxter LC, Johnson SC, Craig AD (2005) Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex. Am J Physiol Regul Integr Comp Physiol 289:R319-R325.
35. Keltner JR, Furst A, Fan C, Redfern R, Inglis B, Fields HL (2006) Isolating the modulatory effect of expectation on pain transmission: A functional magnetic resonance imaging study. J Neurosci 26:4437-4443.
36. Kirsch I, Deacon BJ, Huedo-Medina TB, Scoboria A, Moore TJ, Johnson BT (2008) Initial severity and antidepressant benefits: A meta-analysis of data submitted to the Food and Drug Administration. PLoS Med 5:e45.
37. Kober H, Barrett LF, Joseph J, Bliss-Moreau E, Lindquist K, Wager TD (2008) Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage 42:998-1031.
38. Kohavi R (1995) A study of cross-validation and bootstrap for accuracy estimation and model selection. In: Proceedings of the Fourteenth International Joint Conference on Artificial Intelligence, pp 1137-1143.
39. Kong J, Gollub RL, Rosman IS, Webb JM, Vangel MG, Kirsch I, Kaptchuk TJ (2006) Brain activity associated with expectancy-enhanced placebo analgesia as measured by functional magnetic resonance imaging. J Neurosci 26:381-388.
40. Koyama T, McHaffie JG, Laurienti PJ, Coghill RC (2005) The subjective experience of pain: Where expectations become reality. Proc Natl Acad Sci U S A 102:12950-12955.
41. Kriegeskorte N, Lindquist MA, Nichols TE, Poldrack RA, Vul E (2010) Everything you never wanted to know about circular analysis, but were afraid to ask. J Cereb Blood Flow Metab 30:1551-1557.
42. Lane RD, Wager TD (2009) The new field of brain-body medicine: What have we learned and where are we headed? Neuroimage 47:1135-1140.
43. Liberman R (1964) An experimental study of the placebo response under three different situations of pain. J Psychiatr Res 33:233-246.
44. Lidstone SC, Schulzer M, Dinelle K, Mak E, Sossi V, Ruth TJ, de la Fuente- Fernández R, Phillips AG, Stoessl AJ (2010) Effects of expectation on placebo-induced dopamine release in Parkinson disease. Arch Gen Psychiatry 67:857-865.
45. Lieberman MD, Jarcho JM, Berman S, Naliboff BD, Suyenobu BY, Mandelkern M, Mayer EA (2004) The neural correlates of placebo effects: A disruption account. Neuroimage 22:447-455.
46. Lieberman MD, Berkman ET, Wager TD (2009) Correlations in social neuroscience aren't voodoo: Commentary on Vul et al. (2009). Perspect Psychol Sci 4:299-307.
47. Lorenz J, Hauck M, Paur RC, Nakamura Y, Zimmermann R, Bromm B, Engel AK (2005) Cortical correlates of false expectations during pain intensity judgments-a possible manifestation of placebo/nocebo cognitions. Brain Behav Immun 19:283-295.
48. Lu H-C, Hsieh J-C, Lu C-L, Niddam DM, Wu Y-T, Yeh T-C, Cheng C-M, Chang F-Y, Lee S-D (2010) Neuronal correlates in the modulation of placebo analgesia in experimentally-induced esophageal pain: A 3T-fMRI study. Pain 148:75-83.
49. Lyby PS, Aslaksen PM, Flaten MA (2010) Is fear of pain related to placebo analgesia? J Psychosom Res 68:369-377.
50. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, et al. (2009) Finding the missing heritability of complex diseases. Nature 461:747-753.
51. Matre D, Casey KL, Knardahl S (2006) Placebo-induced changes in spinal cord pain processing. J Neurosci 26:559-563.
52. Melzack R, Casey KL (1968) Sensory, motivational, and central control de-terminants of pain. In: The skin senses (Kenshalo DR, ed), pp 423-439. Springfield: Thomas.
53. Michalski RS, Carbonell JG, Mitchell TM (1986) Machine learning: An artificial intelligence approach. San Mateo, CA: Kaufmann.
54. Miron D, Duncan GH, Bushnell MC (1989) Effects of attention on the intensity and unpleasantness of thermal pain. Pain 39:345-352.
55. Mitchell TM, Shinkareva SV, Carlson A, Chang K-M, Malave VL, Mason RA, Just MA (2008) Predicting human brain activity associated with the meanings of nouns. Science 320:1191-1195.
56. Morton DL, Watson A, El-Deredy W, Jones AKP (2009) Reproducibility of placebo analgesia: Effect of dispositional optimism. Pain 146:194-198.
57. Morton DL, El-Deredy W, Watson A, Jones AK (2010) Placebo analgesia as a case of a cognitive style driven by prior expectation. Brain Res 1359:137-141.
58. Moulton EA, Keaser ML, Gullapalli RP, Greenspan JD (2005) Regional intensive and temporal patterns of functional MRI activation distinguishing noxious and innocuous contact heat. J Neurophysiol 93:2183-2193.
59. Petrovic P, Kalso E, Petersson KM, Ingvar M (2002) Placebo and opioid analgesia- imaging a shared neuronal network. Science 295:1737-1740.
60. Petrovic P, Dietrich T, Fransson P, Andersson J, Carlsson K, IngvarM (2005) Placebo in emotional processing-induced expectations of anxiety relief activate a generalized modulatory network. Neuron 46:957-969.
61. Ploner M, Lee MC, Wiech K, Bingel U, Tracey I (2010) Prestimulus functional connectivity determines pain perception in humans. Proc Natl Acad Sci U S A 107:355-360.
62. Porro CA, Baraldi P, Pagnoni G, Serafini M, Facchin P, Maieron M, Nichelli P (2002) Does anticipation of pain affect cortical nociceptive systems? J Neurosci 22:3206-3214.
63. Porro CA, Cettolo V, Francescato MP, Baraldi P (2003) Functional activity mapping of the mesial hemispheric wall during anticipation of pain. Neuroimage 19:1738-1747.
64. Price DD, Barrell JJ, Gracely RH (1980) A psychophysical analysis of experimential factors that selectively influence the affective dimension of pain. Pain 8:137-149.
65. Price DD, Harkins SW, Baker C (1987) Sensory-affective relationships among different types of clinical and experimental pain. Pain 28:297-307.
66. Price DD, Craggs J, Verne GN, Perlstein WM, RobinsonME (2007) Placebo analgesia is accompanied by large reductions in pain-related brain activity in irritable bowel syndrome patients. Pain 127:63-72.
67. Quevedo AS, Coghill RC (2007) Attentional modulation of spatial integration of pain: Evidence for dynamic spatial tuning. J Neurosci 27: 11635-11640.
68. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968-971.
69. Rutherford B, Sneed J, Devanand D, Eisenstadt R, Roose S (2010) Antidepressant study design affects patient expectancy: A pilot study. Psychol Med 40:781-788.
70. Schweinhardt P, Seminowicz DA, Jaeger E, Duncan GH, Bushnell MC (2009) The anatomy of the mesolimbic reward system: A link between personality and the placebo analgesic response. J Neurosci 29:4882-4887.
71. Scott DJ, Stohler CS, Egnatuk CM, Wang H, Koeppe RA, Zubieta JK (2008) Placebo and nocebo effects are defined by opposite opioid and dopaminergic responses. Arch Gen Psychiatry 65:220-231.
72. Scott DJ, Stohler CS, Egnatuk CM, Wang H, Koeppe RA, Zubieta JK (2007) Individual differences in reward responding explain placebo-induced expectations and effects. Neuron 55:325-336.
73. Shao J (1993) Linear model selection by cross-validation. J Am Stat Assoc 88:486-494.
74. Shapiro AK, Struening EL, Shapiro E (1979) The reliability and validity of a placebo test. J Psychiatr Res 15:253-290.
75. Sneed JR, Rutherford BR, Rindskopf D, Lane DT, Sackeim HA, Roose SP (2008) Design makes a difference: A meta-analysis of antidepressant response rates in placebo-controlled versus comparator trials in late-life depression. Am J Geriatr Psychiatry 16:65-73.
76. Tibshirani R (1996) Regression shrinkage and selection via the lasso. J R Stat Soc Series B Stat Methodol 58:267-288.
77. Vase L, Robinson ME, Verne GN, Price DD (2003) The contributions of suggestion, desire, and expectation to placebo effects in irritable bowel syndrome patients. An empirical investigation. Pain 105:17-25.
78. Vase L, Petersen GL, Riley JL 3rd, Price DD (2009) Factors contributing to large analgesic effects in placebo mechanism studies conducted between 2002 and 2007. Pain 145:36-44.
79. Vul E, Harris C, Winkielman P, Pashler H (2009) Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect Psychol Sci 4:274-290.
80. Wager TD, Smith EE (2003) Neuroimaging studies of working memory: A meta-analysis. Cogn Affect Behav Neurosci 3:255-274.
81. Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL, Davidson RJ, Kosslyn SM, Rose RM, Cohen JD (2004) Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303:1162-1167.
82. Wager TD, Lindquist M, Kaplan L (2007a) Meta-analysis of functional neuroimaging data: Current and future directions. Soc Cogn Affect Neurosci 2:150-158.
83. Wager TD, Scott DJ, Zubieta JK (2007b) Placebo effects on humanμ-opioid activity during pain. Proc Natl Acad Sci U S A 104:11056-11061.
84. Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN (2008) Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59:1037-1050.
85. Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF (2009a) Brain mediators of cardiovascular responses to social threat, Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage 47:821-835.
86. Wager TD, van Ast VA, Hughes BL, Davidson ML, Lindquist MA, Ochsner KN (2009b) Brain mediators of cardiovascular responses to social threat, part II: Prefrontal-subcortical pathways and relationship with anxiety. Neuroimage 47:836-851.
87. Watson A, El-Deredy W, Vogt BA, Jones AK (2007) Placebo analgesia is not due to compliance or habituation: EEG and behavioural evidence. Neuroreport 18:771-775.
88. Watson A, El-Deredy W, Iannetti GD, Lloyd D, Tracey I, Vogt BA, Nadeau V, Jones AK (2009) Placebo conditioning and placebo analgesia modulate a common brain network during pain anticipation and perception. Pain 145:24-30.
89. Wiech K, Tracey I (2009) The influence of negative emotions on pain: Behavioral effects and neural mechanisms. Neuroimage 47:987-994.
90. Yarkoni T (2009) Big correlations in little studies: Inflated FMRI correlations reflect low statistical power-commentary on Vul et al. (2009). Perspect Psychol Sci 4:294-298.
91. Zeng X, Martinez TR (2000) Distribution-balanced stratified crossvalidation for accuracy estimation. J Exp Theor Artif Intell 12:1-12.
92. Zubieta J-K, Bueller JA, Jackson LR, Scott DJ, Xu Y, Koeppe RA, Nichols TE, Stohler CS (2005) Placebo effects mediated by endogenous opioid activity onμ-opioid receptors. J Neurosci 25:7754-7762.
93. Zubieta J-K, Yau W-Y, Scott DJ, Stohler CS (2006) Belief or Need? Accounting for individual variations in the neurochemistry of the placebo effect. Brain Behav Immun 20:15-26.