Building up analgesia in humans via the endogenous μ-opioid system by combining placebo and active tDCS: A preliminary report

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  DosSantos, Marcos F ^a   Martikainen, Ilkka K ^a,b   Nascimento, Thiago D ^a   Love, Tiffany M ^b   DeBoer, Misty D ^a   Schambra, Heidi M ^c   Bikson, Marom ^d   Zubieta, Jon Kar ^b   DaSilva, Alexandre F ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c Departments of Neurology and Rehabilitation and Regenerative Medicine Columbia University ^*  (United States)

^d City College of New York   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 11; CARFENTANIL; CARFENTANIL C 11; MU OPIATE RECEPTOR; UNCLASSIFIED DRUG; FENTANYL; NARCOTIC ANALGESIC AGENT;

ADULT; ANALGESIA; ARTICLE; COHORT ANALYSIS; COLD STRESS; CONTINUOUS INFUSION; FEMALE; GRAY MATTER; HEAT STRESS; HUMAN; HUMAN EXPERIMENT; IN VIVO STUDY; LEFT PREFRONTAL CORTEX; MALE; NEUROTRANSMISSION; NORMAL HUMAN; PAIN THRESHOLD; PILOT STUDY; PLACEBO EFFECT; POSITRON EMISSION TOMOGRAPHY; PRECUNEUS; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; THALAMUS; TRANSCRANIAL DIRECT CURRENT STIMULATION; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; CLINICAL TRIAL; METABOLISM; MIDDLE AGED; MOTOR CORTEX; PROCEDURES;

ADULT; ANALGESIA; ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; FEMALE; FENTANYL; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, OPIOID, MU; TRANSCRANIAL DIRECT CURRENT STIMULATION;

EID: 84904297563     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102350     Document Type: Article

References (69)

1. Wager TD, Scott DJ, Zubieta JK (2007) Placebo effects on human mu-opioid activity during pain. Proc Natl Acad Sci U S A 104: 11056-11061. (Pubitemid 47175225)
2. Scott DJ, Stohler CS, Egnatuk CM, Wang H, Koeppe RA, et al. (2008) Placebo and nocebo effects are defined by opposite opioid and dopaminergic responses. Arch Gen Psychiatry 65: 220-231. (Pubitemid 351214321)
3. Zubieta J, Bueller J, Jackson L, Scott D, Xu Y, et al. (2005) Placebo effects mediated by endogenous opioid activity on mu-opioid receptors. J Neurosci 25: 7754-7762. (Pubitemid 41208646)
4. Zubieta JK, Stohler CS (2009) Neurobiological mechanisms of placebo responses. Ann N Y Acad Sci 1156: 198-210.
5. 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. (Pubitemid 43078587)
6. Harris RE, Zubieta JK, Scott DJ, Napadow V, Gracely RH, et al. (2009) Traditional Chinese acupuncture and placebo (sham) acupuncture are differentiated by their effects on mu-opioid receptors (MORs). Neuroimage 47: 1077-1085.
7. Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, et al. (2003) Modulation of cortical excitability by weak direct current stimulation- technical, safety and functional aspects. Suppl Clin Neurophysiol 56: 255-276.
8. DaSilva AF, Volz MS, Bikson M, Fregni F (2011) Electrode positioning and montage in transcranial direct current stimulation. J Vis Exp.
9. Mylius V, Borckardt JJ, Lefaucheur JP (2012) Noninvasive cortical modulation of experimental pain. Pain 153: 1350-1363.
10. Fregni F, Gimenes R, Valle A, Ferreira M, Rocha R, et al. (2006) A randomized, sham-controlled, proof of principle study of transcranial direct current stimulation for the treatment of pain in fibromyalgia. Arthritis Rheum 54: 3988-3998. (Pubitemid 44955903)
11. Fregni F, Boggio P, Lima M, Ferreira M, Wagner T, et al. (2006) A shamcontrolled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain 122: 197-209.
12. DaSilva AF, Mendonca ME, Zaghi S, Lopes M, DosSantos MF, et al. (2012) tDCS-Induced Analgesia and Electrical Fields in Pain-Related Neural Networks in Chronic Migraine. Headache.
13. O'Connell NE, Wand BM, Marston L, Spencer S, Desouza LH (2010) Noninvasive brain stimulation techniques for chronic pain. Cochrane Database Syst Rev: CD008208.
14. O'Connell NE, Cossar J, Marston L, Wand BM, Bunce D, et al. (2013) Transcranial direct current stimulation of the motor cortex in the treatment of chronic nonspecific low back pain: a randomized, double-blind exploratory study. Clin J Pain 29: 26-34.
15. Wrigley PJ, Gustin SM, McIndoe LN, Chakiath RJ, Henderson LA, et al. (2013) Longstanding neuropathic pain after spinal cord injury is refractory to transcranial direct current stimulation: a randomized controlled trial. Pain 154: 2178-2184.
16. Antal A, Polania R, Schmidt-Samoa C, Dechent P, Paulus W (2011) Transcranial direct current stimulation over the primary motor cortex during fMRI. Neuroimage 55: 590-596.
17. Zheng X, Alsop DC, Schlaug G (2011) Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage 58: 26-33.
18. García-Larrea L, Peyron R, Mertens P, Gregoire MC, Lavenne F, et al. (1999) Electrical stimulation of motor cortex for pain control: a combined PET-scan and electrophysiological study. Pain 83: 259-273. (Pubitemid 29479285)
19. de Andrade DC, Mhalla A, Adam F, Texeira MJ, Bouhassira D (2011) Neuropharmacological basis of rTMS-induced analgesia: the role of endogenous opioids. Pain 152: 320-326.
20. Amanzio M, Benedetti F (1999) Neuropharmacological dissection of placebo analgesia: expectation-activated opioid systems versus conditioning-activated specific subsystems. J Neurosci 19: 484-494. (Pubitemid 29028987)
21. Levine JD, Gordon NC, Fields HL (1978) The mechanism of placebo analgesia. Lancet 2: 654-657. (Pubitemid 9048375)
22. DosSantos MF, Love TM, Martikainen IK, Nascimento TD, Fregni F, et al. (2012) Immediate effects of tDCS on the m -opioid system of a chronic pain patient. Front Psychiatry 3: 93.
23. Dannals RF, Ravert HT, Frost JJ, Wilson AA, Burns HD, et al. (1985) Radiosynthesis of an opiate receptor binding radiotracer: [11C]carfentanil. Int J Appl Radiat Isot 36: 303-306. (Pubitemid 15117523)
24. Jewett DM (2001) A simple synthesis of [11C]carfentanil using an extraction disk instead of HPLC. Nucl Med Biol 28: 733-734.
25. Minoshima S, Koeppe RA, Mintun MA, Berger KL, Taylor SF, et al. (1993) Automated detection of the intercommissural line for stereotactic localization of functional brain images. J Nucl Med 34: 322-329. (Pubitemid 23056418)
26. Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, et al. (1996) Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab 16: 834-840. (Pubitemid 26292051)
27. Gandiga PC, Hummel FC, Cohen LG (2006) Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol 117: 845-850.
28. Wagner T, Fregni F, Fecteau S, Grodzinsky A, Zahn M, et al. (2007) Transcranial direct current stimulation: a computer-based human model study. Neuroimage 35: 1113-1124. (Pubitemid 46507817)
29. Chong PS, Cros DP (2004) Technology literature review: quantitative sensory testing. Muscle Nerve 29: 734-747. (Pubitemid 38620017)
30. Hansson P, Backonja M, Bouhassira D (2007) Usefulness and limitations of quantitative sensory testing: clinical and research application in neuropathic pain states. Pain 129: 256-259. (Pubitemid 46778783)
31. Schestatsky P, Stefani LC, Sanches PR, Silva Júnior DP, Torres IL, et al. (2011) Validation of a Brazilian quantitative sensory testing (QST) device for the diagnosis of small fiber neuropathies. Arq Neuropsiquiatr 69: 943-948.
32. Yarnitsky D, Sprecher E (1994) Thermal testing: normative data and repeatability for various test algorithms. J Neurol Sci 125: 39-45. (Pubitemid 24240185)
33. Maarrawi J, Peyron R, Mertens P, Costes N, Magnin M, et al. (2007) Motor cortex stimulation for pain control induces changes in the endogenous opioid system. Neurology 69: 827-834. (Pubitemid 47329581)
34. Taylor JJ, Borckardt JJ, George MS (2012) Endogenous opioids mediate left dorsolateral prefrontal cortex rTMS-induced analgesia. Pain 153: 1219-1225.
35. Ossipov MH, Dussor GO, Porreca F (2010) Central modulation of pain. J Clin Invest 120: 3779-3787.
36. Linnman C, Moulton EA, Barmettler G, Becerra L, Borsook D (2012) Neuroimaging of the periaqueductal gray: state of the field. Neuroimage 60: 505-522.
37. DaSilva A, Granziera C, Tuch D, Snyder J, Vincent M, et al. (2007) Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport 18: 301-305. (Pubitemid 46667957)
38. Mainero C, Boshyan J, Hadjikhani N (2011) Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol 70: 838-845.
39. Wu D, Wang S, Stein JF, Aziz TZ, Green AL (2013) Reciprocal interactions between the human thalamus and periaqueductal gray may be important for pain perception. Exp Brain Res.
40. Maleki N, Brawn J, Barmettler G, Borsook D, Becerra L (2013) Pain response measured with arterial spin labeling. NMR Biomed.
41. Kano M, Farmer AD, Aziz Q, Giampietro V, Brammer MJ, et al. (2013) Sex Differences in Brain Activity to Anticipated and Experienced Visceral Pain in Healthy Subjects. Am J Physiol Gastrointest Liver Physiol.
42. Youssef AM, Gustin SM, Nash PJ, Reeves JM, Petersen ET, et al. (2013) Differential brain activity in subjects with painful trigeminal neuropathy and painful temporomandibular disorder. Pain.
43. Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL, et al. (2004) Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303: 1162-1167. (Pubitemid 38233575)
44. Watson A, El-Deredy W, Iannetti GD, Lloyd D, Tracey I, et al. (2009) Placebo conditioning and placebo analgesia modulate a common brain network during pain anticipation and perception. Pain 145: 24-30.
45. Leppä M, Korvenoja A, Carlson S, Timonen P, Martinkauppi S, et al. (2006) Acute opioid effects on human brain as revealed by functional magnetic resonance imaging. Neuroimage 31: 661-669. (Pubitemid 43776689)
46. Zyloney CE, Jensen K, Polich G, Loiotile RE, Cheetham A, et al. (2010) Imaging the functional connectivity of the Periaqueductal Gray during genuine and sham electroacupuncture treatment. Mol Pain 6: 80.
47. Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci U S A 98: 4259-4264. (Pubitemid 32249932)
48. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43: 897-905. (Pubitemid 39215019)
49. Lorenz J, Cross DJ, Minoshima S, Morrow TJ, Paulson PE, et al. (2002) A unique representation of heat allodynia in the human brain. Neuron 35: 383-393. (Pubitemid 34876739)
50. Porro CA, Baraldi P, Pagnoni G, Serafini M, Facchin P, et al. (2002) Does anticipation of pain affect cortical nociceptive systems? J Neurosci 22: 3206-3214. (Pubitemid 35379207)
51. Apkarian AV, Sosa Y, Sonty S, Levy RM, Harden RN, et al. (2004) Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J Neurosci 24: 10410-10415. (Pubitemid 39552626)
52. Kuchinad A, Schweinhardt P, Seminowicz DA, Wood PB, Chizh BA, et al. (2007) Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain? J Neurosci 27: 4004-4007. (Pubitemid 46597143)
53. Jin C, Yuan K, Zhao L, Yu D, von Deneen KM, et al. (2013) Structural and functional abnormalities in migraine patients without aura. NMR Biomed 26: 58-64.
54. DaSilva AF, Becerra L, Pendse G, Chizh B, Tully S, et al. (2008) Colocalized structural and functional changes in the cortex of patients with trigeminal neuropathic pain. PLoS One 3: e3396.
55. Metz AE, Yau HJ, Centeno MV, Apkarian AV, Martina M (2009) Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. Proc Natl Acad Sci U S A 106: 2423-2428.
56. Boggio PS, Zaghi S, Fregni F (2009) Modulation of emotions associated with images of human pain using anodal transcranial direct current stimulation (tDCS). Neuropsychologia 47: 212-217.
57. Stagg CJ, Lin RL, Mezue M, Segerdahl A, Kong Y, et al. (2013) Widespread Modulation of Cerebral Perfusion Induced during and after Transcranial Direct Current Stimulation Applied to the Left Dorsolateral Prefrontal Cortex. J Neurosci 33: 11425-11431.
58. Taylor JJ, Borckardt JJ, Canterberry M, Li X, Hanlon CA, et al. (2013) Naloxone-Reversible Modulation of Pain Circuitry by Left Prefrontal rTMS. Neuropsychopharmacology.
59. Johnson S, Summers J, Pridmore S (2006) Changes to somatosensory detection and pain thresholds following high frequency repetitive TMS of the motor cortex in individuals suffering from chronic pain. Pain 123: 187-192. (Pubitemid 43816773)
60. Summers J, Johnson S, Pridmore S, Oberoi G (2004) Changes to cold detection and pain thresholds following low and high frequency transcranial magnetic stimulation of the motor cortex. Neurosci Lett 368: 197-200. (Pubitemid 39194871)
61. Moloney TM, Witney AG (2013) Transcranial direct current stimulation (tDCS) priming of 1 Hz repetitive transcranial magnetic stimulation (rTMS) modulates experimental pain thresholds. Neurosci Lett 534: 289-294.
62. Bachmann CG, Muschinsky S, Nitsche MA, Rolke R, Magerl W, et al. (2010) Transcranial direct current stimulation of the motor cortex induces distinct changes in thermal and mechanical sensory percepts. Clin Neurophysiol 121: 2083-2089.
63. Nahmias F, Debes C, de Andrade DC, Mhalla A, Bouhassira D (2009) Diffuse analgesic effects of unilateral repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers. Pain 147: 224-232.
64. Jürgens TP, Schulte A, Klein T, May A (2012) Transcranial direct current stimulation does neither modulate results of a quantitative sensory testing protocol nor ratings of suprathreshold heat stimuli in healthy volunteers. Eur J Pain 16: 1251-1263.
65. Luedtke K, May A, Jürgens TP (2012) No effect of a single session of transcranial direct current stimulation on experimentally induced pain in patients with chronic low back pain-an exploratory study. PLoS One 7: e48857.
66. Essick GK (2004) Psychophysical assessment of patients with posttraumatic neuropathic trigeminal pain. J Orofac Pain 18: 345-354.
67. Rolke R, Baron R, Maier C, Tölle TR, Treede RD, et al. (2006) Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain 123: 231-243.
68. Villamar MF, Volz MS, Bikson M, Datta A, Dasilva AF, et al. (2013) Technique and considerations in the use of 461 ring high-definition transcranial direct current stimulation (HD-tDCS). J Vis Exp: e50309.
69. O'Connell NE, Cossar J, Marston L, Wand BM, Bunce D, et al. (2012) Rethinking clinical trials of transcranial direct current stimulation: participant and assessor blinding is inadequate at intensities of 2 mA. PLoS One 7: e47514.