Imaging pain: A potent means for investigating pain mechanisms in patients

British Journal of Anaesthesia

Volumn 111, Issue 1, 2013, Pages 64-72

  Lee, M C ^a   Tracey, I ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

chronic pain; neuroimaging, magnetic resonance imaging, functional

Indexed keywords

ANTERIOR CINGULATE; ANXIETY; CEREBROVASCULAR ACCIDENT; CHRONIC PAIN; CONSCIOUSNESS; DEPRESSION; FIBROMYALGIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HOPELESSNESS; HUMAN; INSULA; LIMBIC SYSTEM; NEUROIMAGING; NOCICEPTION; NONHUMAN; PAIN ASSESSMENT; PAIN RECEPTOR; PATHOPHYSIOLOGY; PERSONALITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; REVIEW; SENSORY STIMULATION; SOCIAL ENVIRONMENT; SOMATOSENSORY CORTEX; VISUAL CORTEX; VOXEL BASED MORPHOMETRY;

EID: 84880238757     PISSN: 00070912     EISSN: 14716771     Source Type: Journal    
DOI: 10.1093/bja/aet174     Document Type: Article

References (110)

1. IASP. Part III: Pain terms: a current list with definitions and notes on usage. In: Merskey M, Bogduk N, eds. Classification of Chronic Pain Descriptions of Chronic Pain Syndromes and Definitions of Pain Terms. Seattle: IASP Press, 1994; 209-14
2. Morley S. Psychology of pain. Br J Anaesth 2008; 101: 25-31
3. Adams F. The Law, Oath of Hippocrates, on the Surgery, and on the Sacred Disease. Gloucester, United Kingdom: Dodo Press, 2009
4. Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH. Multiple representations of pain in human cerebral cortex. Science 1991; 251: 1355-8
5. Apkarian AV, Hashmi JA, Baliki MN. Pain and the brain: specificity and plasticity of the brain in clinical chronic pain. Pain 2011; 152: S49-64
6. Tracey I. Can neuroimaging studies identify pain endophenotypes in humans? Nat Rev Neurol 2011; 7: 173-81
7. Apkarian AV, Baliki MN, Geha PY. Towards a theory of chronic pain. Prog Neurobiol 2009; 87: 81-97
8. Tracey I, Mantyh PW. The cerebral signature for pain perception and its modulation. Neuron 2007; 55: 377-91
9. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 2005; 9: 463-84
10. Melzack R. Painandthe neuromatrix in the brain. J Dent Educ 2001; 65: 1378-82
11. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science 2004; 303: 1157-62
12. Kross E, Berman MG, MischelW, Smith EE,Wager TD. Social rejection shares somatosensory representations with physical pain. Proc Natl Acad Sci USA 2011; 108: 6270-5
13. Eisenberger NI, Lieberman MD, Williams KD. Does rejection hurt? An FMRI study of social exclusion. Science 2003; 302: 290-2
14. Raij TT, Numminen J, Narvanen S, Hiltunen J, Hari R. Brain correlates of subjective reality of physically and psychologically induced pain. Proc Natl Acad Sci 2005; 102: 2147-51
15. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997; 277: 968-71
16. Coghill RC, Sang CN, Maisog JM, Iadarola MJ. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol 1999; 82: 1934-43
17. Bingel U, Quante M, Knab R, BrommB,Weiller C, Buchel C. Subcortical structures involved in pain processing: evidence from singletrial fMRI. Pain 2002; 99: 313-21
18. Bornhovd K, Quante M, Glauche V, Bromm B, Weiller C, Buchel C. Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. Brain 2002; 125: 1326-36
19. Berthier M, Starkstein S, Leiguarda R.Asymbolia for pain: a sensorylimbic disconnection syndrome. Ann Neurol 1988; 24: 41-9
20. Ploner M, Freund HJ, Schnitzler A. Pain affect without pain sensation in a patient with a postcentral lesion. Pain 1999; 81: 211-4
21. Wilkinson HA, Davidson KM, Davidson RI. Bilateral anterior cingulotomy for chronic noncancer pain. Neurosurgery 1999; 45: 1129-34; discussion 34-6
22. Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain 1911; 34: 102-254
23. PenfieldW, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937; 60: 389-443
24. Boly M, Faymonville ME, Schnakers C, et al. Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 2008; 7: 1013-20
25. Woolf CJ, Ma Q. Nociceptors-noxious stimulus detectors. Neuron 2007; 55: 353-64
26. Todd AJ. Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 2010; 11: 823-36
27. Frot M, Mauguiere F. Dual representation of pain in the operculo-insular cortex in humans. Brain 2003; 126: 438-50
28. Frot M, Mauguiere F, Magnin M, Garcia-Larrea L. Parallel processing of nociceptive A-delta inputs in SII and midcingulate cortex in humans. J Neurosci 2008; 28: 944-52
29. Craig AD. Pain mechanisms: labeled lines versus convergence in central processing. Annu Rev Neurosci 2003; 26: 1-30
30. Brooks JC, Zambreanu L, Godinez A, Craig AD, Tracey I. Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. Neuroimage 2005; 27: 201-9
31. Albanese MC, Duerden EG, Rainville P, Duncan GH. Memory traces of pain in human cortex. J Neurosci 2007; 27: 4612-20
32. Fairhurst M, Fairhurst K, Berna C, Tracey I. An fMRI study exploring the overlap and differences between neural representations of physical and recalled pain. PLoS ONE 2012; 7: e48711
33. Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguiere F. Representation of pain and somatic sensation in the human insula:astudyof responsesto direct electrical cortical stimulation. Cereb Cortex 2002; 12: 376-85
34. Mazzola L, Isnard J, Peyron R, Mauguiere F. Stimulation of the humancortex and the experience of pain: Wilder Penfield's observations revisited. Brain 2012; 135: 631-40
35. Iannetti GD, Niazy RK, Wise RG, et al. Simultaneous recording of laser-evoked brain potentialsand continuous, high-field functional magnetic resonance imaging in humans. Neuroimage 2005; 28: 708-19
36. Lee MC, Mouraux A, Iannetti GD. Characterizing the cortical activity throughwhichpainemerges fromnociception. J Neurosci 2009; 29: 7909-16
37. Tallon-Baudry C. On the neural mechanisms subserving consciousness and attention. Front Psychol 2011; 2: 397
38. Fell J, Fernandez G, Klaver P, Elger CE, Fries P. Is synchronized neuronal gamma activity relevant for selective attention? Brain Res Brain Res Rev 2003; 42: 265-72
39. Gross J, Schnitzler A, Timmermann L, Ploner M. Gamma oscillations inhumanprimarysomatosensorycortex reflect pain perception. PLoS Biology 2007; 5: e133
40. Zhang ZG, Hu L, Hung YS, Mouraux A, Iannetti GD. Gamma-band oscillations in the primarysomatosensory cortex-a direct and obligatory correlate of subjective pain intensity. J Neurosci 2012; 32: 7429-38
41. Iannetti GD, Hughes NP, Lee MC, Mouraux A. Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? J Neurophysiol 2008; 100: 815-28
42. FastenrathM, Friston KJ, Kiebel SJ.Dynamical causal modelling for M/EEG: spatial and temporal symmetry constraints. Neuroimage 2009; 44: 154-63
43. Friston K. Causal modelling and brain connectivity in functional magnetic resonance imaging. PLoS Biology 2009; 7: e33
44. Friston KJ, Dolan RJ. Computational and dynamic models in neuroimaging. Neuroimage 2010; 52: 752-65
45. Liang M, Mouraux A, Iannetti GD. Parallel processing of nociceptive and non-nociceptive somatosensory information in the human primary and secondary somatosensory cortices: evidence from dynamic causal modeling of functional magnetic resonance imaging data. J Neurosci 2011; 31: 8976-85
46. Wiech K, Kalisch R, Weiskopf N, Pleger B, Stephan KE, Dolan RJ. Anterolateral prefrontal cortex mediates the analgesic effect of expected and perceived control over pain. J Neurosci 2006; 26: 11501-9
47. Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN. Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 2008; 59: 1037-50
48. Ochsner KN, Gross JJ. Cognitive emotion regulation: insights from social cognitive and affective neuroscience. Curr Dir Psychol Sci 2008; 17: 153-8
49. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 2004; 43: 897-905
50. Quirk GJ, Garcia R, Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 2006; 60: 337-43
51. Schiller D, Levy I, Niv Y, LeDoux JE, Phelps EA. From fear to safety and back: reversal of fear in the human brain. J Neurosci 2008; 28: 11517-25
52. Ploghaus A, Narain C, Beckmann CF, et al. Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J Neurosci 2001; 21: 9896-903
53. Kong J, Gollub RL, Polich G, et al. A functional magnetic resonance imaging study on the neural mechanisms of hyperalgesic nocebo effect. J Neurosci 2008; 28: 13354-62
54. Tracey I, Ploghaus A, Gati JS, et al.Imagingattentionalmodulation of pain in the periaqueductal gray in humans. J Neurosci 2002; 22: 2748-52
55. Valet M, Sprenger T, Boecker H, et al. Distraction modulates connectivity of the cingulo-frontal cortex and the midbrain during pain-an fMRI analysis. Pain 2004; 109: 399-408
56. Sprenger C, Eippert F, Finsterbusch J, Bingel U, Rose M, Buchel C. Attention modulates spinal cord responses to pain. Curr Biol 2012; 22: 1019-22
57. Petrovic P, Kalso E, Petersson KM, Ingvar M. Placebo and opioid analgesia-imaging a shared neuronal network. Science 2002; 295: 1737-40
58. Eippert F, Bingel U, Schoell ED, et al. Activation of the opioidergic descending pain control system underlies placebo analgesia. Neuron 2009; 63: 533-43
59. Eippert F, Finsterbusch J, Bingel U, Buchel C. Direct evidence for spinal cord involvement in placebo analgesia. Science 2009; 326: 404
60. Fields H, Basbaum AI, Heinricher MM. Central nervous system mechanisms of pain modulation. In: McMahon S, Koltzenburg M, eds. Textbook of Pain. New York: Churchhill Livingstone, 2006; 125-30
61. Lee MC, Zambreanu L, Menon DK, Tracey I. Identifying brain activity specifically related to the maintenance and perceptual consequence of central sensitization in humans. J Neurosci 2008; 28: 11642-9
62. Luginbuhl M, Gerber A, Schnider TW, Petersen-Felix S, Arendt- Nielsen L, Curatolo M. Modulation of remifentanil-induced analgesia, hyperalgesia, and tolerance by small-dose ketamine in humans. Anesth Analg 2003; 96: 726-32, table of contents
63. Jensen KB, Lonsdorf TB, Schalling M, Kosek E, Ingvar M. Increased sensitivity to thermal pain following a single opiate dose is influenced by the COMT val(158)met polymorphism. PLoS ONE 2009; 4: e6016
64. Wanigasekera V, Lee MC, Rogers R, Hu P, Tracey I. Neural correlates of an injury-free model of central sensitization induced by opioid withdrawal in humans. J Neurosci 2011; 31: 2835-42
65. Petersen KL, Jones B, Segredo V, Dahl JB, Rowbotham MC. Effect of remifentanil on pain and secondary hyperalgesia associated with the heat-capsaicin sensitization model in healthy volunteers. Anesthesiology 2001; 94: 15-20
66. Angst MS, Koppert W, Pahl I, Clark DJ, Schmelz M. Shortterm infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 2003; 106: 49-57
67. Smith SM. The future of FMRI connectivity. Neuroimage 2012; 62: 1257-66
68. Ploner M, Lee MC, Wiech K, Bingel U, Tracey I. Prestimulus functional connectivity determines pain perception in humans. Proc Natl Acad Sci USA 2010; 107: 355-60
69. Fair DA, Dosenbach NUF, Church JA, et al. Development of distinct control networks through segregation and integration. Proc Natl Acad Sci USA 2007; 104: 13507-12
70. Bingel U, Wanigasekera V, Wiech K, et al. The effect of treatment expectation on drug efficacy: imaging the analgesic benefit of the opioid remifentanil. Sci Transl Med 2011; 3: 70ra14
71. Atlas LY, Whittington RA, Lindquist MA, Wielgosz J, Sonty N, Wager TD. Dissociable influences of opiates and expectations on pain. J Neurosci 2012; 32: 8053-64
72. Mayer EA, Berman S, Suyenobu B, et al. Differences in brain responses to visceral pain between patients with irritable bowel syndrome and ulcerative colitis. Pain 2005; 115: 398-409
73. Jones AK, Derbyshire SW. Reduced cortical responses to noxious heat in patients with rheumatoid arthritis. Ann Rheum Dis 1997; 56: 601-7
74. Gundel H, Valet M, Sorg C, et al. Altered cerebral response to noxious heat stimulation in patients with somatoform pain disorder. Pain 2008; 137: 413-21
75. Apkarian AV, Thomas PS, Krauss BR, Szeverenyi NM. Prefrontal cortical hyperactivity in patients with sympathetically mediated chronic pain. Neurosci Lett 2001; 311: 193-7
76. Gracely RH, Geisser ME, Giesecke T, et al. Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain 2004; 127: 835-43
77. BalikiMN, Chialvo DR,GehaPY, et al. Chronic pain andthe emotional brain: specific brain activity associated with spontaneous fluctuations of intensity of chronic back pain. J Neurosci 2006; 26: 12165-73
78. Klega A, Eberle T, Buchholz HG, et al. Central opioidergic neurotransmission in complex regional pain syndrome. Neurology 2010; 75: 129-36
79. Willoch F, Schindler F, Wester HJ, et al. Central poststroke pain and reduced opioid receptor binding within pain processing circuitries: a [11C]diprenorphine PET study. Pain 2004; 108: 213-20
80. Maarrawi J, Peyron R, Mertens P, et al. Differential brain opioid receptor availability in central and peripheral neuropathic pain. Pain 2007; 127: 183-94
81. Harris RE, Clauw DJ, Scott DJ, McLean SA, Gracely RH, Zubieta JK. Decreased central mu-opioid receptor availability in fibromyalgia. J Neurosci 2007; 27: 10000-6
82. Apkarian AV, Sosa Y, Sonty S, et al. Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J Neurosci 2004; 24: 10410-5
83. Baliki MN, Petre B, Torbey S, et al. Corticostriatal functional connectivity predicts transition to chronic back pain. Nat Neurosci 2012
84. Geha PY, Baliki MN, Harden RN, Bauer WR, Parrish TB, Apkarian AV. The brain in chronic CRPS pain: abnormal gray-whitematter interactions in emotional and autonomic regions. Neuron 2008; 60: 570-81
85. Draganski B, Moser T, Lummel N, et al. Decrease of thalamic gray matter following limb amputation. Neuroimage 2006; 31: 951-7
86. Davis KD, Pope G, Chen J, Kwan CL, Crawley AP, Diamant NE. Cortical thinning in IBS: implications for homeostatic, attention, and pain processing. Neurology 2008; 70: 153-4
87. Schmidt-Wilcke T, Luerding R,Weigand T, et al. Striatal greymatter increase in patients suffering from fibromyalgia-a voxel-based morphometry study. Pain 2007; 132 Suppl 1: S109-16
88. Kuchinad A, Schweinhardt P, Seminowicz DA,Wood PB, Chizh BA, Bushnell MC. Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain? J Neurosci 2007; 27: 4004-7
89. Metz AE, Yau HJ, Centeno MV, Apkarian AV, Martina M. Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. Proc Natl Acad Sci USA 2009; 106: 2423-8
90. Seminowicz DA, Laferriere AL, Millecamps M, Yu JS, Coderre TJ, Bushnell MC. MRI structural brain changes associated with sensoryandemotional function inaratmodelof long-termneuropathic pain. Neuroimage 2009
91. Obermann M, Nebel K, Schumann C, et al. Gray matter changes related to chronic posttraumatic headache. Neurology 2009; 73: 978-83
92. Rodriguez-Raecke R, Niemeier A, Ihle K, Ruether W, May A. Brain gray matter decrease in chronic pain is the consequence and not the cause of pain. J Neurosci 2009; 29: 13746-50
93. Gwilym SE, Filippini N, Douaud G, Carr AJ, Tracey I. Thalamic atrophy associated with painful osteoarthritis of the hip is reversible after arthroplasty: a longitudinal voxel-based morphometric study. Arthritis Rheum 2010; 62: 2930-40
94. Seminowicz DA, Wideman TH, Naso L, et al. Effective treatment of chronic low back pain in humans reverses abnormal brain anatomy and function. J Neurosci 2011; 31: 7540-50
95. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motorcortex of resting humanbrain using echo-planar MRI. Magn Reson Med 1995; 34: 537-41
96. Smith K. Neuroscience: idle minds. Nature 2012; 489: 356-8
97. Schwarzkopf DS, Rees G. Neuroscience. Brain activity to rely on? Science 2010; 327: 43-4
98. Boly M, Balteau E, Schnakers C, et al. Baseline brain activity fluctuations predictsomatosensory perception inhumans.Proc NatlAcad Sci USA 2007; 104: 12187-92
99. Fox MD, Snyder AZ, Vincent JL, Raichle ME. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 2007; 56: 171-84
100. Napadow V, Kim J, Clauw DJ, Harris RE. Decreased intrinsic brain connectivity is associated with reduced clinical pain in fibromyalgia. Arthritis Rheum 2012; 64: 2398-403
101. Napadow V, LaCount L, Park K, As-Sanie S, Clauw DJ, Harris RE. Intrinsic brain connectivity in fibromyalgia is associated with chronic pain intensity. Arthritis Rheum 2010; 62: 2545-55
102. Schmelz M, Schmidt R. Microneurographic single-unit recordings to assess receptiveproperties of afferenthumanC-fibers.Neurosci Lett 2010; 470: 158-61
103. Brewer JA, Worhunsky PD, Gray JR, Tang YY, Weber J, Kober H. Meditation experience is associated with differences in default mode network activity and connectivity. Proc Natl Acad Sci USA 2011; 108: 20254-9
104. Gard T, Holzel BK, Sack AT, et al. Pain Attenuation through mindfulness is associated with decreased cognitive control and increased sensory processing in the brain. Cereb Cortex 2012; 22: 2692-702
105. Grant JA, Courtemanche J, Rainville P. A non-elaborative mental stance and decoupling of executive and pain-related cortices predicts low pain sensitivity in Zen meditators. Pain 2011; 152: 150-6
106. Veehof MM, Oskam MJ, Schreurs KM, Bohlmeijer ET. Acceptancebased interventions for the treatment of chronic pain: a systematic review and meta-analysis. Pain 2011; 152: 533-42
107. Owen DG, Bureau Y, Thomas AW, Prato FS, St Lawrence KS. Quantification of pain-induced changes in cerebral bloodflowby perfusion MRI. Pain 2008; 136: 85-96
108. Segerdahl AR, Xie J, Paterson K, Ramirez JD, Tracey I, Bennett DL. Imaging the neural correlates of neuropathic pain and pleasurable relief associated with inherited erythromelalgia in a single subject with quantitative arterial spin labelling. Pain 2012; 153: 1122-7
109. Howard MA, Krause K, Khawaja N, et al. Beyond patient reported pain: perfusion magnetic resonance imaging demonstrates reproducible cerebral representation of ongoing post-surgical pain. PLoS ONE 2011; 6: e17096
110. Brodersen KH, Wiech K, Lomakina EI, et al. Decoding the perception of pain from fMRI using multivariate pattern analysis. Neuroimage 2012; 63: 1162-70