Repeated verum but not placebo acupuncture normalizes connectivity in brain regions dysregulated in chronic pain

NeuroImage: Clinical

Volumn 9, Issue , 2015, Pages 430-435

  Egorova, Natalia ^a   Gollub, Randy L ^a   Kong, Jian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Acupuncture; Chronic pain; Osteoarthritis; Resting state fMRI

Indexed keywords

PLACEBO;

ACUPUNCTURE; ADULT; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN REGION; CHRONIC PAIN; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; KNEE OSTEOARTHRITIS; MALE; MEDIAL FRONTAL CORTEX; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE SCANNER; PAIN ASSESSMENT; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RESTING STATE NETWORK; BRAIN MAPPING; COMPLICATION; FRONTAL LOBE; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN MEASUREMENT; PATHOPHYSIOLOGY;

ACUPUNCTURE THERAPY; BRAIN MAPPING; CHRONIC PAIN; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; OSTEOARTHRITIS, KNEE; PAIN MEASUREMENT; PERIAQUEDUCTAL GRAY;

EID: 84943426183     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2015.09.012     Document Type: Article

References (56)

1. M. Amanzio, F. Benedetti, C.A. Porro, S. Palermo, and F. Cauda Activation likelihood estimation meta-analysis of brain correlates of placebo analgesia in human experimental pain Hum. Brain Mapp. 34 2013 738 752 10.1002/hbm.21471
2. A.V. Apkarian, J.A. Hashmi, and M.N. Baliki Pain and the brain: specificity and plasticity of the brain in clinical chronic pain Pain 152 2011 49 64 10.1016/j.pain.2010.11.010.Pain
3. M.M. Baliki, A. Baria, and A.V. Apkarian The cortical rhythms of chronic back pain J. Neurosci. 31 2011 13981 13990 10.1523/JNEUROSCI.1984-11.2011
4. M.N. Baliki, A.R. Mansour, A.T. Baria, and A.V. Apkarian Functional reorganization of the default mode network across chronic pain conditions PLoS One 9 2014 e106133 10.1371/journal.pone.0106133
5. B.M. Berman, L. Lao, P. Langenberg, W.L. Lee, A.M. Gilpin, and M.C. Hochberg Effectiveness of acupuncture as adjunctive therapy in osteoarthritis of the knee: a randomized, controlled trial Ann. Intern. Med. 141 2004 901 910
6. R.M. Carter, J.P. O'Doherty, B. Seymour, C. Koch, and R.J. Dolan Contingency awareness in human aversive conditioning involves the middle frontal gyrus Neuroimage 29 2006 1007 1012 10.1016/j.neuroimage.2005.09.011
7. F. Cauda, S. Palermo, T. Costa, R. Torta, S. Duca, U. Vercelli, G. Geminiani, and D.M.E. Torta Gray matter alterations in chronic pain: a network-oriented meta-analytic approach NeuroImage Clin. 4 2014 676 686 10.1016/j.nicl.2014.04.007
8. Y. Chae, D. Chang, S. Lee, W. Jung, I. Lee, S. Jackson, J. Kong, H. Lee, H. Park, H. Lee, and C. Wallraven Inserting needles into the body: a meta-analysis of brain activity associated with acupuncture needle stimulation J. Pain 14 2013 215 222
9. X.Y. Chen, R.B. Spaeth, K. Retzepi, D. Ott, and J. Kong Acupuncture modulates cortical thickness and functional connectivity in knee osteoarthritis patients Sci. Rep. 4 2014 1 7 10.1038/srep06482
10. X.N. Cheng Chinese Acupuncture and Moxibustion 1987 Foreign Language Press Beijing
11. M.S. Corbett, S.J.C. Rice, V. Madurasinghe, R. Slack, D.A. Fayter, M. Harden, A.J. Sutton, H. MacPherson, and N.F. Woolacott Acupuncture and other physical treatments for the relief of pain due to osteoarthritis of the knee: network meta-analysis Osteoarthr. Cartil. 21 2013 1290 1298 10.1016/j.joca.2013.05.007
12. S.W.G. Derbyshire, and J. Osborn Offset analgesia is mediated by activation in the region of the periaqueductal grey and rostral ventromedial medulla Neuroimage 47 2009 1002 1006 10.1016/j.neuroimage.2009.04.032
13. W. Durnez, and S. Van Damme Trying to fix a painful problem: the impact of pain control attempts on the attentional prioritization of a threatened body location J. Pain 16 2015 135 143
14. F. Eippert, U. Bingel, E.D. Schoell, J. Yacubian, R. Klinger, J. Lorenz, C. Büchel, and C. Buchel Activation of the opioidergic descending pain control system underlies placebo analgesia Neuron 63 2009 533 543 10.1016/j.neuron.2009.07.014
15. M. Gondo, Y. Moriguchi, N. Kodama, N. Sato, N. Sudo, C. Kubo, and G. Komaki Daily physical complaints and hippocampal function: an fMRI study of pain modulation by anxiety Neuroimage 63 2012 1011 1019 10.1016/j.neuroimage.2012.07.025
16. J.A. Hashmi, M.N. Baliki, L. Huang, A.T. Baria, S. Torbey, K.M. Hermann, T.J. Schnitzer, and A.V. Apkarian Shape shifting pain: chronification of back pain shifts brain representation from nociceptive to emotional circuits Brain 136 2013 2751 2768 10.1093/brain/awt211
17. J.A. Hashmi, J. Kong, R. Spaeth, S. Khan, T.J. Kaptchuk, and R.L. Gollub Functional network architecture predicts psychologically mediated analgesia related to treatment in chronic knee pain patients J. Neurosci. 34 2014 3924 3936 10.1523/JNEUROSCI.3155-13.2014
18. R.S. Hinman, P. McCrory, M. Pirotta, I. Relf, A. Forbes, K.M. Crossley, E. Williamson, M. Kyriakides, K. Novy, B.R. Metcalf, A. Harris, P. Reddy, P.G. Conaghan, and K.L. Bennell Acupuncture for chronic knee pain JAMA 312 2014 1313 10.1001/jama.2014.12660
19. J.-Y. Hong, L.A. Kilpatrick, J. Labus, A. Gupta, Z. Jiang, C. Ashe-McNalley, J. Stains, N. Heendeniya, B. Ebrat, S. Smith, K. Tillisch, B. Naliboff, and E.A. Mayer Patients with chronic visceral pain show sex-related alterations in intrinsic oscillations of the resting brain J. Neurosci. 33 2013 11994 12002 10.1523/JNEUROSCI.5733-12.2013
20. T.J. Kaptchuk Acupuncture: theory, efficacy, and practice Ann. Intern. Med. 136 2002 374 383
21. J. Kong, T.J. Kaptchuk, G. Polich, I. Kirsch, M. Vangel, C. Zyloney, B. Rosen, and R.L. Gollub An fMRI study on the interaction and dissociation between expectation of pain relief and acupuncture treatment Neuroimage 47 2009 1066 1076 10.1016/j.neuroimage.2009.05.087
22. J. Kong, T.J. Kaptachuk, G. Polich, I.V. Kirsch, M. Angel, C. Zyloney, B. Rosen, R. Gollub, T.J. Kaptchuk, G. Polich, I.V. Kirsch, M. Vangel, C. Zyloney, B. Rosen, and R. Gollub Expectancy and treatment interactions: a dissociation between acupuncture analgesia and expectancy evoked placebo analgesia Neuroimage 45 2009 940 949
23. J. Kong, M.L. Loggia, C. Zyloney, P. Tu, P. Laviolette, and R.L. Gollub Exploring the brain in pain: activations, deactivations and their relation Pain 148 2010 257 267 10.1016/j.pain.2009.11.008
24. J. Kong, R. Spaeth, A. Cook, I. Kirsch, B. Claggett, M. Vangel, R.L. Gollub, J.S.W. Smoller, and T.J. Kaptchuk Are all placebo effects equal? Placebo pills, sham acupuncture, cue conditioning and their association PLoS One 8 2013 e67485 10.1371/journal.pone.0067485
25. A. Kucyi, T.V. Salomons, and K.D. Davis Mind wandering away from pain dynamically engages antinociceptive and default mode brain networks Proc. Natl. Acad. Sci. U. S. A. 110 2013 18692 18697 10.1073/pnas.1312902110
26. S. Lang, A. Kroll, S.J. Lipinski, M. Wessa, S. Ridder, C. Christmann, L.R. Schad, and H. Flor Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex Eur. J. Neurosci. 29 2009 823 832 10.1111/j.1460-9568.2009.06624.x
27. H.M. Langevin, P.M. Wayne, H. MacPherson, R. Schnyer, R.M. Milley, V. Napadow, L. Lao, J. Park, R.E. Harris, M. Cohen, K.J. Sherman, A. Haramati, and R. Hammerschlag Paradoxes in acupuncture research: strategies for moving forward. Evidence-based complement Altern. Med. 2011 10.1155/2011/180805
28. S. Leknes, C. Berna, M.C. Lee, G.D. Snyder, G. Biele, and I. Tracey The importance of context: when relative relief renders pain pleasant Pain 154 2013 402 410 10.1016/j.pain.2012.11.018
29. J. Li, J.-H. Zhang, T. Yi, W.-J. Tang, S.-W. Wang, and J.-C. Dong Acupuncture treatment of chronic low back pain reverses an abnormal brain default mode network in correlation with clinical pain relief Acupunct. Med. 32 2014 102 108 10.1136/acupmed-2013-010423
30. C. Linnman, E.A. Moulton, G. Barmettler, L. Becerra, and D. Borsook Neuroimaging of the periaqueductal gray: state of the field Neuroimage 60 2012 505 522 10.1016/j.neuroimage.2011.11.095
31. C. Linnman, J.-C.C. Beucke, K.B. Jensen, R.L. Gollub, and J. Kong Sex similarities and differences in pain-related periaqueductal gray connectivity Pain 153 2012 444 454 10.1016/j.pain.2011.11.006
32. Y. Ma, S. Wang, Y. Tian, L. Chen, G. Li, and J. Mao Disruption of persistent nociceptive behavior in rats with learning impairment PLoS One 8 2013 e74533 10.1371/journal.pone.0074533
33. A.R. Mansour, M.A. Farmer, M.N. Baliki, and A.V. Apkarian Chronic pain: the role of learning and brain plasticity Restor. Neurol. Neurosci. 32 2014 129 139 10.3233/RNN-139003
34. T. Manyanga, M. Froese, R. Zarychanski, A. Abou-Setta, C. Friesen, M. Tennenhouse, and B.L. Shay Pain management with acupuncture in osteoarthritis: a systematic review and meta-analysis BMC Complement. Altern. Med. 14 2014 312 10.1186/1472-6882-14-312
35. A.A. Mutso, B. Petre, L. Huang, M.N. Baliki, S. Torbey, K. Herrmann, T.J. Schnitzer, and A.V. Apkarian Reorganization of hippocampal functional connectivity with transition to chronic back pain J. Neurophysiol. 2013 1065 1076 10.1152/jn.00611.2013
36. A. Ploghaus, C. Narain, C.F. Beckmann, S. Clare, S. Bantick, R. Wise, P.M. Matthews, J.N. Rawlins, and I. Tracey Exacerbation of pain by anxiety is associated with activity in a hippocampal network J. Neurosci. 21 2001 9896 9903
37. J.D. Power, K.A. Barnes, A.Z. Snyder, B.L. Schlaggar, and S.E. Petersen Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion Neuroimage 59 2012 2142 2154 10.1016/j.neuroimage.2011.10.018 (S1053-8119(11)01181-5 [pii])
38. E.M. Roos, H.P. Roos, L.S. Lohmander, C. Ekdahl, and B.D. Beynnon Knee Injury and Osteoarthritis Outcome Score (KOOS) - development of a self-administered outcome measure J. Orthop. Sports Phys. Ther. 28 1998 88 96 10.2519/jospt.1998.28.2.88
39. M. Roy, D. Shohamy, N. Daw, M. Jepma, G.E. Wimmer, and T.D. Wager Representation of aversive prediction errors in the human periaqueductal gray Nat. Neurosci. 17 2014 10.1038/nn.3832
40. T.V. Salomons, T. Johnstone, M.-M. Backonja, A.J. Shackman, and R.J. Davidson Individual differences in the effects of perceived controllability on pain perception: critical role of the prefrontal cortex J. Cogn. Neurosci. 19 2007 993 1003 10.1162/jocn.2007.19.6.993
41. H.P. Scharf, U. Mansmann, K. Streitberger, S. Witte, J. Kramer, C. Maier, H.J. Trampisch, and N. Victor Acupuncture and knee osteoarthritis: a three-armed randomized trial Ann. Intern. Med. 145 2006 12 20
42. R.B. Spaeth, S. Camhi, J.A. Hashmi, M. Vangel, A.D. Wasan, R.R. Edwards, R.L. Gollub, and J. Kong A longitudinal study of the reliability of acupuncture deqi sensations in knee osteoarthritis Evid. Based Complement Altern. Med. 2013 204259 10.1155/2013/204259
43. G. Stux Technique of acupuncture G. Stux, B. Pomeranz, Basics of Acupuncture 1997 Springer-Verlag Berlin 202 213
44. I. Tracey, A. Ploghaus, J.S. Gati, S. Clare, S. Smith, R.S. Menon, and P.M. Matthews Imaging attentional modulation of pain in the periaqueductal gray in humans J. Neurosci. 22 2002 2748 2752 (doi:20026238)
45. E. Vachon-Presseau, M. Roy, M.O. Martel, E. Caron, M.F. Marin, J. Chen, G. Albouy, I. Plante, M.J. Sullivan, S.J. Lupien, and P. Rainville The stress model of chronic pain: evidence from basal cortisol and hippocampal structure and function in humans Brain 136 2013 815 827 10.1093/brain/aws371
46. M. Valet, T. Sprenger, H. Boecker, F. Willoch, E. Rummeny, B. Conrad, P. Erhard, and T.R. Tolle Distraction modulates connectivity of the cingulo-frontal cortex and the midbrain during pain - an fMRI analysis Pain 109 2004 399 408 10.1016/j.pain.2004.02.033
47. M.T.R. Van Kesteren, M. Rijpkema, D.J. Ruiter, and G. Fernández Retrieval of associative information congruent with prior knowledge is related to increased medial prefrontal activity and connectivity J. Neurosci. 30 2010 15888 15894 10.1523/JNEUROSCI.2674-10.2010
48. A.J. Vickers, and K. Linde Acupuncture for chronic pain JAMA 311 2014 955 956 10.1001/jama.2013.285478 (1835483 [pii])
49. T.D. Wager, D.J. Scott, and J.-K.K. Zubieta Placebo effects on human mu-opioid activity during pain Proc. Natl. Acad. Sci. U. S. A. 104 2007 11056 11061 10.1073/pnas.0702413104
50. A. White Western medical acupuncture: a definition Acupunct. Med. 27 2009 33 35 10.1136/aim.2008.000372
51. S. Whitfield-Gabrieli, and A. Nieto-Castanon Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks Brain Connect. 2 2012 125 141 10.1089/brain.2012.0073
52. C. Witt, B. Brinkhaus, S. Jena, K. Linde, A. Streng, S. Wagenpfeil, J. Hummelsberger, H.U. Walther, D. Melchart, and S.N. Willich Acupuncture in patients with osteoarthritis of the knee: a randomised trial Lancet 366 2005 136 143
53. M. Yi, and H. Zhang Nociceptive memory in the brain: cortical mechanisms of chronic pain J. Neurosci. 31 2011 13343 13345 10.1523/JNEUROSCI.3279-11.2011
54. M. Yi, H. Zhang, L. Lao, G.-G. Xing, and Y. Wan Anterior cingulate cortex is crucial for contra- but not ipsi-lateral electro-acupuncture in the formalin-induced inflammatory pain model of rats Mol. Pain 7 2011 61 10.1186/1744-8069-7-61
55. R.J. Yu, R.L. Gollub, R. Spaeth, V. Napadow, A. Wasan, J. Kong, R. Spaetha, V. Napadowa, A. Wasana, and J. Kong Disrupted functional connectivity of the periaqueductal gray in chronic low back pain Neuroimage (Amst) 6 2014 100 108 10.1016/j.nicl.2014.08.019
56. C.E. Zyloney, K. Jensen, G. Polich, R.E. Loiotile, A. Cheetham, P.S. LaViolette, P. Tu, T.J. Kaptchuk, R.L. Gollub, and J. Kong Imaging the functional connectivity of the Periaqueductal Gray during genuine and sham electroacupuncture treatment Mol. Pain 6 2010 80 10.1186/1744-8069-6-80