Placebo analgesia and reward processing: Integrating genetics, personality, and intrinsic brain activity

Human Brain Mapping

Volumn 35, Issue 9, 2014, Pages 4583-4593

  Yu, Rongjun ^a   Gollub, Randy L ^a   Vangel, Mark ^a   Kaptchuk, Ted ^b   Smoller, Jordan W ^a   Kong, Jian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Conditioning; FMRI; Placebo analgesia; Regional homogeneity; Resting state

Indexed keywords

CATECHOL METHYLTRANSFERASE; COMT PROTEIN, HUMAN;

ADULT; BRAIN; BRAIN MAPPING; CORPUS STRIATUM; FEMALE; GENETIC POLYMORPHISM; GENETICS; GENOTYPING TECHNIQUE; HUMAN; MALE; NERVE TRACT; NOCICEPTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN MEASUREMENT; PERSONALITY; PERSONALITY TEST; PHYSIOLOGY; PLACEBO EFFECT; REGRESSION ANALYSIS; REST; YOUNG ADULT;

ADULT; BRAIN; BRAIN MAPPING; CATECHOL O-METHYLTRANSFERASE; CORPUS STRIATUM; FEMALE; GENOTYPING TECHNIQUES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PAIN MEASUREMENT; PAIN PERCEPTION; PERSONALITY; PERSONALITY TESTS; PLACEBO EFFECT; POLYMORPHISM, GENETIC; REGRESSION ANALYSIS; REST; YOUNG ADULT;

EID: 84904472318     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22496     Document Type: Article

References (88)

1. Atlas LY, Bolger N, Lindquist MA, Wager TD (2010): Brain mediators of predictive cue effects on perceived pain. J Neurosci 30:12964-12977.
2. Beedie C, Foad AJ, Coleman DA (2008): Identification of placebo responsive participants in 40km laboratory cycling performance. J Sports Sci Med:166-175.
3. Benedetti F (2008) Mechanisms of placebo and placebo-related effects across diseases and treatments. Annu Rev Pharmacol Toxicol 48:33-60.
4. Benedetti F (2009) Placebo Effects: Understnding the Mechanism in Health and Disease. New York. Oxford University Press.
5. 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.
6. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
7. Cocchi L, Bramati IE, Zalesky A, Furukawa E, Fontenelle LF, Moll J, Tripp G, Mattos P (2012) Altered functional brain connectivity in a non-clinical sample of young adults with attention-deficit/hyperactivity disorder. J Neurosci 32:17753-17761.
8. Coghill RC, McHaffie JG, Yen YF (2003) Neural correlates of interindividual differences in the subjective experience of pain. Proc Natl Acad Sci U S A 100:8538-8542.
9. Costa PT Jr, McCrae RR (1997) Stability and change in personality assessment: the revised NEO Personality Inventory in the year 2000. J Pers Assess 68:86-94.
10. de la Fuente-Fernandex R, Schulzer M, Stoessl AJ (2002) The placebo effect in neurological disorders. Lancet Neurol 1:85-91.
11. de la Fuente-Fernandez 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.
12. DeYoung CG, Peterson JB, Higgins DM (2005) Sources of openness/intellect: cognitive and neuropsychological correlates of the fifth factor of personality. J Pers 73:825-858.
13. Edwards RR, Ness TJ, Weigent DA, Fillingim RB (2003) Individual differences in diffuse noxious inhibitory controls (DNIC): association with clinical variables. Pain 106:427-437.
14. Elsenbruch S, Kotsis V, Benson S, Rosenberger C, Reidick D, Schedlowski M, Bingel U, Theysohn N, Forsting M, Gizewski ER (2012) Neural mechanisms mediating the effects of expectation in visceral placebo analgesia: an fMRI study in healthy placebo responders and nonresponders. Pain 153:382-390.
15. Finniss DG, Kaptchuk TJ, Miller F, Benedetti F (2010) Biological, clinical, and ethical advances of placebo effects. Lancet 375:686-695.
16. Flaten MA, Aslaksen PM, Lyby PS, Bjorkedal E (2011) The relation of emotions to placebo responses. Philos Trans R Soc Lond B Biol Sci 366:1818-1827.
17. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700-711.
18. Fruyt FD, De Wiele LV, Van Heeringen C (2000) Cloninger's psychobiological model of temperament and character and the five-factor model of personality. Pers Indiv Differ:441-452.
19. Gear RW, Aley KO, Levine JD (1999) Pain-induced analgesia mediated by mesolimbic reward circuits. J Neurosci 19:7175-7181.
20. Geers AL, Wellman JA, Fowler SL, Helfer SG, France CR (2010) Dispositional optimism predicts placebo analgesia. J Pain 11:1165-1171.
21. Gracely RH, McGrath PA, Dubner R (1978) Validity and sensitivity of ratio scales of sensory and affective verbal pain descriptors: manipulation of affect by diazepam. Pain 5:19-29.
22. Hall KT, Lembo AJ, Kirsch I, Ziogas DC, Douaiher J, Jensen KB, Conboy LA, Kelley JM, Kokkotou E, Kaptchuk TJ. (2012) Catechol-O-methyltransferase val158met polymorphism predicts placebo effect in irritable bowel syndrome. PLoS One 7:e48135.
23. Hashmi JA, Baria AT, Baliki MN, Huang L, Schnitzer TJ, Apkarian AV (2012) Brain networks predicting placebo analgesia in a clinical trial for chronic back pain. Pain 153:2393-2402.
24. Jensen KB, Kaptchuk TJ, Kirsch I, Raicek J, Lindstrom KM, Berna C, Gollub RL, Ingvar M, Kong J (2012) Nonconscious activation of placebo and nocebo pain responses. Proc Natl Acad Sci U S A, 109:15959-15964.
25. Kelley JM, Lembo AJ, Ablon JS, Villanueva JJ, Conboy LA, Levy R, Marci CD, Kerr CE, Kirsch I, Jacobson EE, Riess H, Kaptchuk TJ (2009) Patient and practitioner influences on the placebo effect in irritable bowel syndrome. Psychosom Med 71:789-797.
26. 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.
27. Kim H, Neubert JK, San Miguel A, Xu K, Krishnaraju RK, Iadarola MJ, Goldman D, Dionne RA (2004) Genetic influence on variability in human acute experimental pain sensitivity associated with gender, ethnicity and psychological temperament. Pain 109:488-496.
28. Kim H, Shimojo S, O'Doherty JP (2006) Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain. PLoS Biol 4:e233.
29. Kong J, Fufa DT, Gerber AJ, Rosman IS, Vangel MG, Gracely RH, Gollub RL (2005) Psychophysical outcomes from a randomized pilot study of manual, electro, and sham acupuncture treatment on experimentally induced thermal pain. J Pain 6:55-64.
30. Kong J, Gollub RL, Polich G, Kirsch I, Laviolette P, Vangel M, Rosen B, Kaptchuk TJ (2008) A functional magnetic resonance imaging study on the neural mechanisms of hyperalgesic nocebo effect. J Neurosci 28:13354-13362. PMCID: PMC2649754.
31. Kong J, Gollub RL, Rosman IS, Webb JM, Vangel MG, Kirsch I, Kaptchuk TJ (2006a) Brain activity associated with expectancy-enhanced placebo analgesia as measured by functional magnetic resonance imaging. J Neurosci 26:381-388.
32. Kong J, White NS, Kwong KK, Vangel MG, Rosman IS, Gracely RH, Gollub RL (2006b) Using fMRI to dissociate sensory encoding from cognitive evaluation of heat pain intensity. Hum Brain Mapp 27:715-721.
33. Kong J, Jensen K, Loiotile R, Cheetham A, Wey HY, Tan Y, Rosen B, Smoller JW, Kaptchuk TJ, Gollub RL (2013a) Functional connectivity of the frontoparietal network predicts cognitive modulation of pain. Pain 154:459-467.
34. Kong J, Spaeth R, Cook A, Kirsch I, Claggett B, Vangel M, Gollub R, Smoller JS, Kaptchuk TJ (2013b) Are All Placebo Effects Equal? Placebo pills, sham acupuncture, cue conditioning and their Association. PLoS ONE 8:e67485. doi:67410.61371/journal.pone.0067485.
35. Kong J, Kaptachuk TJ, Polich G, Kirsch IV, Angel M, Zyloney C, Rosen B, Gollub R (2009a) Expectancy and treatment interactions: A dissociation between acupuncture analgesia and expectancy evoked placebo analgesia. Neuroimage 45:940-949. PMID: 19159691.
36. Kong J, Kaptchuk TJ, Polich G, Kirsch I, Vangel M, Zyloney C, Rosen B, Gollub RL (2009b) An fMRI study on the interaction and dissociation between expectation of pain relief and acupuncture treatment. Neuroimage 47:1066-1076. PMID: 19501656.
37. 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.
38. Lai CH, Wu YT (2012) Frontal regional homogeneity increased and temporal regional homogeneity decreased after remission of first-episode drug-naive major depressive disorder with panic disorder patients under duloxetine therapy for 6 weeks. J Affect Disord 136:453-458.
39. Legrain V, Guerit JM, Bruyer R, Plaghki L (2002) Attentional modulation of the nociceptive processing into the human brain: selective spatial attention, probability of stimulus occurrence, and target detection effects on laser evoked potentials. Pain 99:21-39.
40. Leknes S, Lee M, Berna C, Andersson J, Tracey I (2011) Relief as a reward: hedonic and neural responses to safety from pain. PLoS One 6:e17870.
41. Leuchter AF, McCracken JT, Hunter AM, Cook IA, Alpert JE (2009) Monoamine oxidase a and catechol-o-methyltransferase functional polymorphisms and the placebo response in major depressive disorder. J Clin Psychopharmacol 29:372-377.
42. Lidstone SC, Schulzer M, Dinelle K, Mak E, Sossi V, Ruth TJ, de la Fuente-Fernandez R, Phillips AG, Stoessl AJ (2010) Effects of expectation on placebo-induced dopamine release in Parkinson disease. Arch Gen Psychiatry 67:857-865.
43. Lidstone SC, Stoessl AJ (2007) Understanding the placebo effect: contributions from neuroimaging. Mol Imaging Biol 9:176-185.
44. Liu D, Yan C, Ren J, Yao L, Kiviniemi VJ, Zang Y (2010) Using coherence to measure regional homogeneity of resting-state FMRI signal. Front Syst Neurosci 4:24.
45. Liu Y, Wang K, Yu C, He Y, Zhou Y, Liang M, Wang L, Jiang T (2008) Regional homogeneity, functional connectivity and imaging markers of Alzheimer's disease: a review of resting-state fMRI studies. Neuropsychologia 46:1648-1656.
46. Loggia ML, Jensen K, Gollub RL, Wasan AD, Edwards RR, Kong J (2011) The catechol-O-methyltransferase (COMT) val158met polymorphism affects brain responses to repeated painful stimuli. PLoS One 6:e27764.
47. Lu HC, Hsieh JC, Lu CL, Niddam DM, Wu YT, Yeh TC, Cheng CM, Chang FY, Lee SD (2010) Neuronal correlates in the modulation of placebo analgesia in experimentally-induced esophageal pain: a 3T-fMRI study. Pain 148:75-83.
48. Mannisto PT, Kaakkola S (1999) Catechol-O-methyltransferase (COMT): biochemistry, molecular biology, pharmacology, and clinical efficacy of the new selective COMT inhibitors. Pharmacol Rev 51:593-628.
49. McLeod HL, Fang L, Luo X, Scott EP, Evans WE (1994) Ethnic differences in erythrocyte catechol-O-methyltransferase activity in black and white Americans. J Pharmacol Exp Ther 270:26-29.
50. Meyer-Lindenberg A, Kohn PD, Kolachana B, Kippenhan S, McInerney-Leo A, Nussbaum R, Weinberger DR, Berman KF (2005) Midbrain dopamine and prefrontal function in humans: interaction and modulation by COMT genotype. Nat Neurosci 8:594-596.
51. Mogil JS, Sternberg WF, Marek P, Sadowski B, Belknap JK, Liebeskind JC (1996) The genetics of pain and pain inhibition. Proc Natl Acad Sci U S A 93:3048-3055.
52. Morton DL, Watson A, El-Deredy W, Jones AK (2009) Reproducibility of placebo analgesia: Effect of dispositional optimism. Pain 146:194-198.
53. Ochsner KN, Ludlow DH, Knierim K, Hanelin J, Ramachandran T, Glover GC, Mackey SC (2006) Neural correlates of individual differences in pain-related fear and anxiety. Pain 120:69-77.
54. Paakki JJ, Rahko J, Long X, Moilanen I, Tervonen O, Nikkinen J, Starck T, Remes J, Hurtig T, Haapsamo H, Jussila K, Kuusikko-Gauffin S, Mattila ML, Zang Y, Kiviniemi V (2010) Alterations in regional homogeneity of resting-state brain activity in autism spectrum disorders. Brain Res 1321:169-179.
55. Palmatier MA, Kang AM, Kidd KK (1999) Global variation in the frequencies of functionally different catechol-O-methyltransferase alleles. Biol Psychiatry 46:557-567.
56. Pecina M, Azhar H, Love TM, Lu T, Fredrickson BL, Stohler CS, Zubieta JK (2012) Personality trait predictors of placebo analgesia and neurobiological correlates. Neuropsychopharmacology.
57. Petrovic P, Dietrich T, Fransson P, Andersson J, Carlsson K, Ingvar M (2005) Placebo in emotional processing - induced expectations of anxiety relief activate a generalized modulatory network. Neuron 46:957-969.
58. Ploghaus A, Narain C, Beckmann CF, Clare S, Bantick S, Wise R, Matthews PM, Rawlins JN, Tracey I (2001) Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J Neurosci 21:9896-9903.
59. 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.
60. Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449-476.
61. Rhudy JL, Williams AE, McCabe KM, Russell JL, Maynard LJ (2008) Emotional control of nociceptive reactions (ECON): do affective valence and arousal play a role? Pain 136:250-261.
62. Robbins TW (2007) Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications. Philos Trans R Soc Lond B Biol Sci 362:917-932.
63. Roffman JL, Brohawn DG, Nitenson AZ, Macklin EA, Smoller JW, Goff DC (2013) Genetic variation throughout the folate metabolic pathway influences negative symptom severity in schizophrenia. Schizophr Bull 39:330-338.
64. Schmahl C, Ludascher P, Greffrath W, Kraus A, Valerius G, Schulze TG, Treutlein J, Rietschel M, Smolka MN, Bohus M (2012) COMT val158met polymorphism and neural pain processing. PLoS One 7:e23658.
65. 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.
66. 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.
67. 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.
68. Seymour B, O'Doherty JP, Koltzenburg M, Wiech K, Frackowiak R, Friston K, Dolan R (2005) Opponent appetitive-aversive neural processes underlie predictive learning of pain relief. Nat Neurosci 8:1234-1240.
69. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031.
70. Stein N, Sprenger C, Scholz J, Wiech K, Bingel U (2012) White matter integrity of the descending pain modulatory system is associated with interindividual differences in placebo analgesia. Pain 153:2210-2217.
71. Sutin AR, Beason-Held LL, Resnick SM, Costa PT (2009) Sex differences in resting-state neural correlates of openness to experience among older adults. Cereb Cortex 19:2797-2802.
72. Taddio A, Goldbach M, Ipp M, Stevens B, Koren G (1995) Effect of neonatal circumcision on pain responses during vaccination in boys. Lancet 345:291-292.
73. Taddio A, Shah V, Gilbert-MacLeod C, Katz J (2002) Conditioning and hyperalgesia in newborns exposed to repeated heel lances. JAMA 288:857-861.
74. Tian L, Ren J, Zang Y (2012) Regional homogeneity of resting state fMRI signals predicts Stop signal task performance. Neuroimage 60:539-544.
75. Tracey I, Mantyh PW (2007) The cerebral signature for pain perception and its modulation. Neuron 55:377-391.
76. Vase L, Robinson ME, Verne GN, Price DD (2005) Increased placebo analgesia over time in irritable bowel syndrome (IBS) patients is associated with desire and expectation but not endogenous opioid mechanisms. Pain 115:338-347.
77. Villemure C, Bushnell MC (2002) Cognitive modulation of pain: how do attention and emotion influence pain processing? Pain 95:195-199.
78. Wager TD, Atlas LY, Leotti LA, Rilling JK (2011) Predicting individual differences in placebo analgesia: contributions of brain activity during anticipation and pain experience. J Neurosci 31:439-452.
79. Wanigasekera V, Lee MC, Rogers R, Kong Y, Leknes S, Andersson J, Tracey I (2012) Baseline reward circuitry activity and trait reward responsiveness predict expression of opioid analgesia in healthy subjects. Proc Natl Acad Sci U S A 109:17705-17710.
80. Wu QZ, Li DM, Kuang WH, Zhang TJ, Lui S, Huang XQ, Chan RC, Kemp GJ, Gong QY (2011) Abnormal regional spontaneous neural activity in treatment-refractory depression revealed by resting-state fMRI. Hum Brain Mapp 32:1290-1299.
81. Wu T, Long X, Zang Y, Wang L, Hallett M, Li K, Chan P (2009) Regional homogeneity changes in patients with Parkinson's disease. Hum Brain Mapp 30:1502-1510.
82. Xu J, Potenza MN (2012) White matter integrity and five-factor personality measures in healthy adults. Neuroimage 59:800-807.
83. Yao Z, Wang L, Lu Q, Liu H, Teng G (2009) Regional homogeneity in depression and its relationship with separate depressive symptom clusters: a resting-state fMRI study. J Affect Disord 115:430-438.
84. Yarnitsky D, Sprecher E, Zaslansky R, Hemli JA (1995) Heat pain thresholds: normative data and repeatability. Pain 60:329-332.
85. Yuan Y, Zhang Z, Bai F, Yu H, Shi Y, Qian Y, Liu W, You J, Zhang X, Liu Z (2008) Abnormal neural activity in the patients with remitted geriatric depression: a resting-state functional magnetic resonance imaging study. J Affect Disord 111:145-152.
86. Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22:394-400.
87. Zeidan F, Martucci KT, Kraft RA, Gordon NS, McHaffie JG, Coghill RC (2011) Brain mechanisms supporting the modulation of pain by mindfulness meditation. J Neurosci 31:5540-5548.
88. Zubieta JK, Yau WY, 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.