Lesion of the rostral anterior cingulate cortex eliminates the aversiveness of spontaneous neuropathic pain following partial or complete axotomy

Pain

Volumn 152, Issue 7, 2011, Pages 1641-1648

  Qu, Chaoling ^a,c   King, Tamara ^a   Okun, Alec ^a   Lai, Josephine ^a   Fields, Howard L ^b   Porreca, Frank ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^c MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Anterior cingulate cortex; Axotomy; Negative reinforcement; Nerve injury; Spontaneous pain

Indexed keywords

CLONIDINE; LIDOCAINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; AVERSIVE BEHAVIOR; BRAIN DAMAGE; CONDITIONING; MALE; NERVE FIBER TRANSECTION; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; REINFORCEMENT; REWARD; SAPHENOUS NERVE; SCIATIC NERVE;

ANALGESICS; ANIMALS; AVOIDANCE LEARNING; AXOTOMY; CLONIDINE; COCAINE; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; GYRUS CINGULI; HYPERALGESIA; MALE; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT (PSYCHOLOGY); SCIATIC NERVE; SPINAL NERVES;

EID: 79958740719     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2011.03.002     Document Type: Article

References (59)

1. + channel currents of rat dorsal root ganglion neurons. J Neurophysiol 2001;85:644-58.
2. 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. (Pubitemid 40836040)
3. Burgess SE, Gardell LR, Ossipov MH, Malan Jr TP, Vanderah TW, Lai J, Porreca F. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 2002;22:5129-36. (Pubitemid 37465626)
4. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 2000;4:215-22. (Pubitemid 30332147)
5. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006;52:77-92. (Pubitemid 44466361)
6. Casey KL. Forebrain mechanisms of nociception and pain: analysis through imaging. Proc Natl Acad Sci USA 1999;96:7668-74. (Pubitemid 29328338)
7. Casey KL, Minoshima S, Morrow TJ, Koeppe RA. Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. J Neurophysiol 1996;76:571-81. (Pubitemid 26255295)
8. Casey KL, Morrow TJ, Lorenz J, Minoshima S. Temporal and spatial dynamics of human forebrain activity during heat pain: analysis by positron emission tomography. J Neurophysiol 2001;85:951-9. (Pubitemid 32147792)
9. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994;53:55-63. (Pubitemid 24238751)
10. Craig AD, Reiman EM, Evans A, Bushnell MC. Functional imaging of an illusion of pain. Nature 1996;384:258-60. (Pubitemid 26396973)
11. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain 1995;118:279-306.
12. Devor M. Sensory basis of autotomy in rats. Pain 1991;45:109-10.
13. Devor M. Neuropathic pain: what do we do with all these theories? Acta Anaesthesiol Scand 2001;45:1121-7.
14. Devor M. Sodium channels and mechanisms of neuropathic pain. J Pain 2006;7:S3-S12. (Pubitemid 43106683)
15. Devor M. Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp Brain Res 2009;196:115-28.
16. Dixon WJ. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 1980;20:441-62.
17. Donahue RR, LaGraize SC, Fuchs PN. Electrolytic lesion of the anterior cingulate cortex decreases inflammatory, but not neuropathic nociceptive behavior in rats. Brain Res 2001;897:131-8. (Pubitemid 32244360)
18. Ducreux D, Attal N, Parker F, Bouhassira D. Mechanisms of central neuropathic pain: a combined psychophysical and fMRI study in syringomyelia. Brain 2006;129:963-76.
19. Foltz EL, White Jr LE. Pain "relief" by frontal cingulumotomy. J Neurosurg 1962;19:89-100.
20. Govrin-Lippmann R, Devor M. Ongoing activity in severed nerves: source and variation with time. Brain Res 1978;159:406-10. (Pubitemid 9050975)
21. Gracely RH, Lynch SA, Bennett GJ. Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 1992;51:175-94. (Pubitemid 23000733)
22. Hsieh J-C, Belfrage M, Stone-Elander S, Hansson P, Ingvar M. Central representation of chronic ongoing neuropathic pain studied by positron emission tomography. Pain 1995;63:225-36.
23. Hurt RW, Ballantine Jr HT. Stereotactic anterior cingulate lesions for persistent pain: a report on 68 cases. Clin Neurosurg 1974;21:334-51.
24. Hutchison WD, Davis KD, Lozano AM, Tasker RR, Dostrovsky JO. Pain-related neurons in the human cingulate cortex. Nat Neurosci 1999;2:403-5. (Pubitemid 30491247)
25. Johansen JP, Fields HL. Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat Neurosci 2004;7:398-403. (Pubitemid 38429180)
26. Johansen JP, Fields HL, Manning BH. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci USA 2001;98:8077-82. (Pubitemid 32642689)
27. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992;50:355-63.
28. King T, Vera-Portocarrero L, Gutierrez T, Vanderah TW, Dussor G, Lai J, Fields HL, Porreca F. Unmasking the tonic-aversive state in neuropathic pain. Nat Neurosci 2009;12:1364-6.
29. Koyama T, Kato K, Mikami A. During pain-avoidance neurons activated in the macaque anterior cingulate and caudate. Neurosci Lett 2000;283:17-20. (Pubitemid 30145486)
30. Koyama T, Tanaka YZ, Mikami A. Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain. Neuroreport 1998;9:2663-7. (Pubitemid 28387168)
31. LaGraize SC, Labuda CJ, Rutledge MA, Jackson RL, Fuchs PN. Differential effect of anterior cingulate cortex lesion on mechanical hypersensitivity and escape/avoidance behavior in an animal model of neuropathic pain. Exp Neurol 2004;188:139-48. (Pubitemid 38748812)
32. Li Y, Dorsi MJ, Meyer RA, Belzberg AJ. Mechanical hyperalgesia after an L5 spinal nerve lesion in the rat is not dependent on input from injured nerve fibers. Pain 2000;85:493-502. (Pubitemid 30214178)
33. Lombard MC, Nashold Jr BS, Albe-Fessard D, Salman N, Sakr C. Deafferentation hypersensitivity in the rat after dorsal rhizotomy: a possible animal model of chronic pain. Pain 1979;6:163-74. (Pubitemid 9152801)
34. Moisset X, Bouhassira D. Brain imaging of neuropathic pain. Neuroimage 2007;37:S80-8.
35. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. San Diego: Academic Press; 1986.
36. Petersen KL, Fields HL, Brennum J, Sandroni P, Rowbotham MC. Capsaicin evoked pain and allodynia in post-herpetic neuralgia. Pain 2000;88:125-33.
37. Petrovic P, Ingvar M, Stone-Elander S, Petersson KM, Hansson P. A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy. Pain 1999;83:459-70.
38. Petrovic P, Kalso E, Petersson KM, Ingvar M. Placebo and opioid analgesia - imaging a shared neuronal network. Science 2002;295:1737-40. (Pubitemid 34202913)
39. Peyron R, Garcia-Larrea L, Gregoire MC, Convers P, Lavenne F, Veyre L, Froment JC, Mauguiere F, Michel D, Laurent B. Allodynia after lateral-medullary (Wallenberg) infarct. A PET study. Brain 1998;121:345-56.
40. Pfeiffer A, Brantl V, Herz A, Emrich HM. Psychotomimesis mediated by kappa opiate receptors. Science 1986;233:774-6. (Pubitemid 16016229)
41. 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. (Pubitemid 27366684)
42. Rice AS, Cimino-Brown D, Eisenach JC, Kontinen VK, Lacroix-Fralish ML, Machin I, Mogil JS, Stohr T. Animal models and the prediction of efficacy in clinical trials of analgesic drugs: a critical appraisal and call for uniform reporting standards. Pain 2008;139:243-7.
43. Ringkamp M, Meyer RA. Injured versus uninjured afferents: who is to blame for neuropathic pain? Anesthesiology 2005;103:221-3.
44. Rodin BE, Kruger L. Deafferentation in animals as a model for the study of pain: an alternative hypothesis. Brain Res 1984;319:213-28. (Pubitemid 14039091)
45. Sheen K, Chung JM. Signs of neuropathic pain depend on signals from injured nerve fibers in a rat model. Brain Res 1993;610:62-8. (Pubitemid 23144424)
46. Tracey I. Nociceptive processing in the human brain. Curr Opin Neurobiol 2005;15:478-87. (Pubitemid 41074770)
47. Tracey I, Bushnell MC. How neuroimaging studies have challenged us to rethink: is chronic pain a disease? J Pain 2009;10:1113-20.
48. Treede RD, Kenshalo DR, Gracely RH, Jones AK. The cortical representation of pain. Pain 1999;79:105-11. (Pubitemid 29076744)
49. Tzschentke TM, Schmidt WJ. Functional heterogeneity of the rat medial prefrontal cortex: effects of discrete subarea-specific lesions on drug-induced conditioned place preference and behavioural sensitization. Eur J Neurosci 1999;11:4099-109. (Pubitemid 29537589)
50. Vierck CJ, Hansson PT, Yezierski RP. Clinical and pre-clinical pain assessment: are we measuring the same thing? Pain 2008;135:7-10.
51. Wall JT, Cusick CG. Cutaneous responsiveness in primary somatosensory (S-I) hindpaw cortex before and after partial hindpaw deafferentation in adult rats. J Neurosci 1984;4:1499-515. (Pubitemid 14058668)
52. Wall PD, Devor M, Inbal R, Scadding JW, Schonfeld D, Seltzer Z, Tomkiewicz MM. Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain 1979;7:103-11.
53. Wall PD, Scadding JW, Tomkiewicz MM. The production and prevention of experimental anesthesia dolorosa. Pain 1979;6:175-82. (Pubitemid 9152802)
54. Witting N, Kupers RC, Svensson P, Jensen TS. A PET activation study of brush-evoked allodynia in patients with nerve injury pain. Pain 2006;120:145-54. (Pubitemid 43077177)
55. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 2001;21:1-5.
56. Xie JY, Herman DS, Stiller CO, Gardell LR, Ossipov MH, Lai J, Porreca F, Vanderah TW. Cholecystokinin in the rostral ventromedial medulla mediates opioid-induced hyperalgesia and antinociceptive tolerance. J Neurosci 2005;25:409-16. (Pubitemid 40105611)
57. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 2008;28:7445-53.
58. Yaksh TL, Rudy TA. Chronic catheterization of the spinal subarachnoid space. Physiol Behav 1976;17:1031-6. (Pubitemid 8063691)
59. Yoon YW, Na HS, Chung JM. Contributions of injured and intact afferents to neuropathic pain in an experimental rat model. Pain 1996;64:27-36. (Pubitemid 26062244)