MRI structural brain changes associated with sensory and emotional function in a rat model of long-term neuropathic pain

NeuroImage

Volumn 47, Issue 3, 2009, Pages 1007-1014

  Seminowicz, David A ^a   Laferriere, Audrey L ^a   Millecamps, Magali ^a   Yu, Jon S C ^a   Coderre, Terence J ^a,b   Bushnell, M Catherine ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN SIZE; CINGULATE GYRUS; CONTROLLED STUDY; DISEASE DURATION; EMOTIONALITY; ENTORHINAL CORTEX; EXPLORATORY BEHAVIOR; FRONTAL CORTEX; HEAT SENSITIVITY; HYPERALGESIA; LOCOMOTION; MALE; MAZE TEST; MECHANICAL STRESS; NEUROANATOMY; NEUROPATHIC PAIN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; SENSORY SYSTEM;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; HYPERALGESIA; MAGNETIC RESONANCE IMAGING; MALE; NEURALGIA; RATS; RATS, LONG-EVANS;

EID: 67651045815     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.05.068     Document Type: Article

References (97)

1. Apkarian A.V., Sosa Y., Krauss B.R., Thomas P.S., Fredrickson B.E., Levy R.E., Harden R.N., and Chialvo D.R. Chronic pain patients are impaired on an emotional decision-making task. Pain 108 1-2 (2004) 129-136
2. Apkarian A.V., Sosa Y., Sonty S., Levy R.M., Harden R.N., Parrish T.B., and Gitelman D.R. Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J. Neurosci. 24 46 (2004) 10410-10415
3. Apkarian A.V., Bushnell M.C., Treede R.D., and Zubieta J.K. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 9 4 (2005) 463-484
4. Baliki M.N., Chialvo D.R., Geha P.Y., Levy R.M., Harden R.N., Parrish T.B., and Apkarian A.V. Chronic pain and the emotional brain: specific brain activity associated with spontaneous fluctuations of intensity of chronic back pain. J. Neurosci. 26 47 (2006) 12165-12173
5. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 1 (1988) 87-107
6. Bentley D.E., Derbyshire S.W., Youell P.D., and Jones A.K. Caudal cingulate cortex involvement in pain processing: an inter-individual laser evoked potential source localisation study using realistic head models. Pain 102 3 (2003) 265-271
7. Bushnell M.C., Duncan G.H., Hofbauer R.K., Ha B., Chen J.I., and Carrier B. Pain perception: is there a role for primary somatosensory cortex?. Proc. Natl. Acad. Sci. U. S. A. 96 14 (1999) 7705-7709
8. Calejesan A.A., Kim S.J., and Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur. J. Pain 4 1 (2000) 83-96
9. Campbell L.C., Clauw D.J., and Keefe F.J. Persistent pain and depression: a biopsychosocial perspective. Biol. Psychiatry 54 3 (2003) 399-409
10. Cao Z., Wu X., Chen S., Fan J., Zhang R., Owyang C., and Li Y. Anterior cingulate cortex modulates visceral pain as measured by visceromotor responses in viscerally hypersensitive rats. Gastroenterology 134 2 (2008) 535-543
11. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53 1 (1994) 55-63
12. Choi Y., Yoon Y.W., Na H.S., Kim S.H., and Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59 3 (1994) 369-376
13. Chung M.K., Worsley K.J., Paus T., Cherif C., Collins D.L., Giedd J.N., Rapoport J.L., and Evans A.C. A unified statistical approach to deformation-based morphometry. Neuroimage 14 3 (2001) 595-606
14. Coderre T.J., Kumar N., Lefebvre C.D., and Yu J.S. A comparison of the glutamate release inhibition and anti-allodynic effects of gabapentin, lamotrigine, and riluzole in a model of neuropathic pain. J. Neurochem. 100 5 (2007) 1289-1299
15. Collins D.L., Neelin P., Peters T.M., and Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 18 2 (1994) 192-205
16. Cryan J.F., Markou A., and Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci. 23 5 (2002) 238-245
17. Daniel H.C., Narewska J., Serpell M., Hoggart B., Johnson R., and Rice A.S.C. Comparison of psychological and physical function in neuropathic pain and nociceptive pain: implications for cognitive behavioral pain management programs. Eur. J. Pain 12 6 (2008) 731-741
18. Danziger N., Faillenot I., and Peyron R. Can we share a pain we never felt? Neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 61 2 (2009) 203-212
19. DaSilva A.F.M., Granziera C., Snyder J., and Hadjikhani N. Thickening in the somatosensory cortex of patients with migraine. Neurology 69 21 (2007) 1990-1995
20. Davis K.D., Pope G., Chen J., Kwan C.L., Crawley A.P., and Diamant N.E. Cortical thinning in IBS: implications for homeostatic, attention, and pain processing. Neurology 70 2 (2008) 153-154
21. de Gier M., Peters M.L., and Vlaeyen J.W. Fear of pain, physical performance, and attentional processes in patients with fibromyalgia. Pain 104 1-2 (2003) 121-130
22. Decosterd I., and Woolf C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87 2 (2000) 149-158
23. Dick B.D., Verrier M.J., Harker K.T., and Rashiq S. Disruption of cognitive function in Fibromyalgia Syndrome. Pain 139 3 (2008) 610-616
24. Draganski B., Moser T., Lummel N., GSnssbauer S., Bogdahn U., Haas F., and May A. Decrease of thalamic gray matter following limb amputation. Neuroimage 31 3 (2006) 951-957
25. Frare M., Axia G., and Battistella P.A. Quality of life, coping strategies, and family routines in children with headache. Headache: J. Head Face Pain 42 10 (2002) 953-962
26. Geha P.Y., Baliki M.N., Harden R.N., Bauer W.R., Parrish T.B., and Apkarian A.V. The brain in chronic CRPS pain: abnormal gray-white matter interactions in emotional and autonomic regions. Neuron 60 4 (2008) 570-581
27. Genovese C.R., Lazar N.A., and Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15 4 (2002) 870-878
28. Hama A.T., Sagen J., and Pappas G.D. Morphological characterization of dorsal horn spinal neurons in rats with unilateral constriction nerve injury: a preliminary study. Neurol. Res. 16 4 (1994) 297-304
29. Hamani C., Schwalb J.M., Rezai A.R., Dostrovsky J.O., Davis K.D., and Lozano A.M. Deep brain stimulation for chronic neuropathic pain: long-term outcome and the incidence of insertional effect. Pain 125 1-2 (2006) 188-196
30. Harman K., and Ruyak P. Working through the pain: a controlled study of the impact of persistent pain on performing a computer task. Clin. J. Pain 21 3 (2005) 216-222
31. Hasnie F.S., Wallace V.C.J., Hefner K., Holmes A., and Rice A.S.C. Mechanical and cold hypersensitivity in nerve-injured C57BL/6J mice is not associated with fear-avoidance- and depression-related behaviour. Br. J. Anaesth. 98 6 (2007) 816-822
32. Haythornthwaite J.A., and rud-Larson L.M. Psychological aspects of neuropathic pain. Clin. J. Pain 16 2 Suppl (2000) S101-S105
33. Hofbauer R.K., Rainville P., Duncan G.H., and Bushnell M.C. Cortical representation of the sensory dimension of pain. J. Neurophysiol. 86 1 (2001) 402-411
34. Hutchison W.D., Davis K.D., Lozano A.M., Tasker R.R., and Dostrovsky J.O. Pain-related neurons in the human cingulate cortex. Nat. Neurosci. 2 (1999) 403-405
35. Janke A.L., de Z.G., Rose S.E., Griffin M., Chalk J.B., and Galloway G.J. 4D deformation modeling of cortical disease progression in Alzheimer's dementia. Magn. Reson. Med. 46 4 (2001) 661-666
36. Jasmin L., Burkey A.R., Granato A., and Ohara P.T. Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J. Comp. Neurol. 468 3 (2004) 425-440
37. Kalaydjian A., Zandi P.P., Swartz K.L., Eaton W.W., and Lyketsos C. How migraines impact cognitive function: findings from the Baltimore ECA. Neurology 68 17 (2007) 1417-1424
38. Kawamura T., Akira T., Watanabe M., and Kagitani Y. Prostaglandin E1 prevents apoptotic cell death in superficial dorsal horn of rat spinal cord. Neuropharmacology 36 8 (1997) 1023-1030
39. Kewman D.G., Vaishampayan N., Zald D., and Han B. Cognitive impairment in musculoskeletal pain patients. Int. J. Psychiatry Med. 21 3 (1991) 253-262
40. Kim J.H., Suh S.I., Seol H.Y., Oh K., Seo W.K., Yu S.W., Park K.W., and Koh S.B. Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia 28 6 (2008) 598-604
41. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 3 (1992) 355-363
42. Kontinen V.K., Kauppila T., Paananen S., Pertovaara A., and Kalso E. Behavioural measures of depression and anxiety in rats with spinal nerve ligation-induced neuropathy. Pain 80 1-2 (1999) 341-346
43. Kovacevic N., Henderson J.T., Chan E., Lifshitz N., Bishop J., Evans A.C., Henkelman R.M., and Chen X.J. A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb. Cortex 15 5 (2005) 639-645
44. Kuchinad A., Schweinhardt P., Seminowicz D.A., Wood P.B., Chizh B.A., and Bushnell M.C. Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain?. J. Neurosci. 27 15 (2007) 4004-4007
45. Kulkarni B., Bentley D.E., Elliott R., Youell P., Watson A., Derbyshire S.W.G., Frackowiak R.S.J., Friston K.J., and Jones A.K.P. Attention to pain localization and unpleasantness discriminates the functions of the medial and lateral pain systems. Eur. J. Neurosci. 21 11 (2005) 3133-3142
46. Labuda C.J., and Fuchs P.N. Attenuation of negative pain affect produced by unilateral spinal nerve injury in the rat following anterior cingulate cortex activation. Neuroscience 136 1 (2005) 311-322
47. LaGraize S.C., Labuda C.J., Rutledge M.A., Jackson R.L., and Fuchs P.N. Differential effect of anterior cingulate cortex lesion on mechanical hypersensitivity and escape/avoidance behavior in an animal model of neuropathic pain. Exp. Neurol. 188 1 (2004) 139-148
48. Lau J.C., Lerch J.P., Sled J.G., Henkelman R.M., Evans A.C., and Bedell B.J. Longitudinal neuroanatomical changes determined by deformation-based morphometry in a mouse model of Alzheimer's disease. Neuroimage 42 1 (2008) 19-27
49. Lenz F.A., Rios M., Zirh A., Chau D., Krauss G., and Lesser R.P. Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus. J. Neurophysiol. 79 4 (1998) 2231-2234
50. Logan D.E., Simons L.E., Stein M.J., and Chastain L. School impairment in adolescents with chronic pain. J. Pain 9 5 (2008) 407-416
51. Lutz J., Jager L., de Q.D., Krauseneck T., Padberg F., Wichnalek M., Beyer A., Stahl R., Zirngibl B., Morhard D., Reiser M., and Schelling G. White and gray matter abnormalities in the brain of patients with fibromyalgia: a diffusion-tensor and volumetric imaging study. Arthritis. Rheum. 58 12 (2008) 3960-3969
52. Mao J., Mayer D.J., and Price D.D. Patterns of increased brain activity indicative of pain in a rat model of peripheral mononeuropathy. J. Neurosci. 13 6 (1993) 2689-2702
53. Matsuzawa-Yanagida K., Narita M., Nakajima M., Kuzumaki N., Niikura K., Nozaki H., Takagi T., Tamai E., Hareyama N., Terada M., Yamazaki M., and Suzuki T. Usefulness of antidepressants for improving the neuropathic pain-like state and pain-induced anxiety through actions at different brain sites. Neuropsychopharmacology 33 8 (2008) 1952-1965
54. May A. Chronic pain may change the structure of the brain. Pain 137 1 (2008) 7-15
55. Metz A.E., Yau H.J., Centeno M.V., Apkarian A.V., and Martina M. Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. PNAS 106 7 (2009) 2432-2438
56. Miller M.W. The origin of corticospinal projection neurons in rat. Exp. Brain Res. 67 2 (1987) 339-351
57. Mochizuki H., Tashiro M., Kano M., Sakurada Y., Itoh M., and Yanai K. Imaging of central itch modulation in the human brain using positron emission tomography. Pain 105 1-2 (2003) 339-346
58. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., and Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J. Neurosci. 22 15 (2002) 6724-6731
59. Narita M., Kuzumaki N., Narita M., Kaneko C., Hareyama N., Miyatake M., Shindo K., Miyoshi K., Nakajima M., Nagumo Y., Sato F., Wachi H., Seyama Y., and Suzuki T. Chronic pain-induced emotional dysfunction is associated with astrogliosis due to cortical delta-opioid receptor dysfunction. J. Neurochem. 97 5 (2006) 1369-1378
60. Ochsner K.N., Ludlow D.H., Knierim K., Hanelin J., Ramachandran T., Glover G.C., and Mackey S.C. Neural correlates of individual differences in pain-related fear and anxiety. Pain 120 1-2 (2006) 69-77
61. Ochsner K.N., Zaki J., Hanelin J., Ludlow D.H., Knierim K., Ramachandran T., Glover G.H., and Mackey S.C. Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other. Soc. Cogn. Affect Neurosci. 3 2 (2008) 144-160
62. Onyszchuk G., Al-Hafez B., He Y.Y., Bilgen M., Berman N.E.J., and Brooks W.M. A mouse model of sensorimotor controlled cortical impact: characterization using longitudinal magnetic resonance imaging, behavioral assessments and histology. J. Neurosci. Methods 160 2 (2007) 187-196
63. Paxinos G., and Watson R. The Rat Brain in Stereotaxic Coordinates (2005), Elsevier Academic Press, New York
64. Pellow S., Chopin P., File S.E., and Briley M. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14 3 (1985) 149-167
65. Petrak F., Hardt J., Kappis B., Nickel R., and Tiber E.U. Determinants of health-related quality of life in patients with persistent somatoform pain disorder. Eur. J. Pain 7 5 (2003) 463-471
66. Polgar E., Gray S., Riddell J.S., and Todd A.J. Lack of evidence for significant neuronal loss in laminae I-III of the spinal dorsal horn of the rat in the chronic constriction injury model. Pain 111 1-2 (2004) 144-150
67. Polgar E., Hughes D.I., Arham A.Z., and Todd A.J. Loss of neurons from laminas I-III of the spinal dorsal horn is not required for development of tactile allodynia in the spared nerve injury model of neuropathic pain. J. Neurosci. 25 28 (2005) 6658-6666
68. Rainville P., Duncan G.H., Price D.D., Carrier B., and Bushnell M.C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277 (1997) 968-971
69. Roeska K., Doods H., Arndt K., Treede R.D., and Ceci A. Anxiety-like behaviour in rats with mononeuropathy is reduced by the analgesic drugs morphine and gabapentin. Pain 139 2 (2009) 349-357
70. Schlereth T., BaumgSrtner U., Magerl W., Stoeter P., and Treede R.D. Left-hemisphere dominance in early nociceptive processing in the human parasylvian cortex. Neuroimage 20 1 (2003) 441-454
71. Schmidt-Wilcke T., Leinisch E., Straube A., Kampfe N., Draganski B., Diener H., Bogdahn U., and May A. Gray matter decrease in patients with chronic tension type headache. Neurology 65 9 (2005) 1483-1486
72. Schmidt-Wilcke T., Leinisch E., bauer S., Draganski B., Bogdahn U., Altmeppen J., and May A. Affective components and intensity of pain correlate with structural differences in gray matter in chronic back pain patients. Pain 125 1-2 (2006) 89-97
73. Schweinhardt P., Kuchinad A., Pukall C.F., and Bushnell M.C. Increased gray matter density in young women with chronic vulvar pain. Pain 140 3 (2008) 411-419
74. Seltzer Z., Dubner R., and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43 2 (1990) 205-218
75. Sikes R.W., and Vogt B.A. Nociceptive neurons in area 24 of rabbit cingulate cortex. J. Neurophysiol. 68 5 (1992) 1720-1732
76. Sikes R.W., Vogt L.J., and Vogt B.A. Distribution and properties of visceral nociceptive neurons in rabbit cingulate cortex. Pain 135 1-2 (2008) 160-174
77. Sled J.G., Zijdenbos A.P., and Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 17 1 (1998) 87-97
78. Sugimoto T., and Gobel S. Dendritic changes in the spinal dorsal horn following transection of a peripheral nerve. Brain Res. 321 2 (1984) 199-208
79. Sugimoto T., Bennett G.J., and Kajander K.C. Transsynaptic degeneration in the superficial dorsal horn after sciatic nerve injury: effects of a chronic constriction injury, transection, and strychnine. Pain 42 2 (1990) 205-213
80. Teutsch S., Herken W., Bingel U., Schoell E., and May A. Changes in brain gray matter due to repetitive painful stimulation. Neuroimage 42 2 (2008) 845-849
81. Urban R., Scherrer G., Goulding E., Tecott L., and Basbaum A. Dissociation of mechanical hypersensitivity from influences on daily life activities or emotional behaviors in a mouse model of neuropathic pain. 12th IASP World Congress on Pain, Glasgow (2008)
82. Villemure C., and Bushnell M.C. Mood influences supraspinal pain processing separately from attention. J. Neurosci. 29 3 (2009) 705-715
83. Vogt B.A. Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 6 7 (2005) 533-544
84. Vogt B.A., Vogt L.J., and Farber N.B. Cingulate cortex and disease models. In: Paxinos G. (Ed). The Rat Nervous System. Third edition (2004), Elsevier, San Diego, CA 705-727
85. Wager T.D., Rilling J.K., Smith E.E., Sokolik A., Casey K.L., Davidson R.J., Kosslyn S.M., Rose R.M., and Cohen J.D. Placebo-induced changes in fMRI in the anticipation and experience of pain. Science 303 5661 (2004) 1162-1167
86. Walf A.A., and Frye C.A. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2 2 (2007) 322-328
87. Wallace V.C.J., Blackbeard J., Pheby T., Segerdahl A.R., Davies M., Hasnie F., Hall S., McMahon S.B., and Rice A.S.C. Pharmacological, behavioural and mechanistic analysis of HIV-1 gp120 induced painful neuropathy. Pain 133 1-3 (2007) 47-63
88. Wallace V.C.J., Blackbeard J., Segerdahl A.R., Hasnie F., Pheby T., McMahon S.B., and Rice A.S.C. Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain. Brain 130 10 (2007) 2688-2702
89. Wallace V.C.J., Segerdahl A.R., Blackbeard J., Pheby T., and Rice A.S.C. Anxiety-like behaviour is attenuated by gabapentin, morphine and diazepam in a rodent model of HIV anti-retroviral-associated neuropathic pain. Neurosci. Lett. 448 1 (2008) 153-156
90. Watson C.P.N., Deck J.H., Morshead C., Van der Kooy D., and Evans R.J. Post-herpetic neuralgia: further post-mortem studies of cases with and without pain. Pain 44 2 (1991) 105-117
91. Whiteside G.T., and Munglani R. Cell death in the superficial dorsal horn in a model of neuropathic pain. J. Neurosci. Res. 64 2 (2001) 168-173
92. Willoch F., Schindler F., Wester H.J., Empl M., Straube A., Schwaiger M., Conrad B., and Tolle T.R. Central poststroke pain and reduced opioid receptor binding within pain processing circuitries: a [11C]diprenorphine PET study. Pain 108 3 (2004) 213-220
93. Worsley K.J., Liao C.H., Aston J., Petre V., Duncan G.H., Morales F., and Evans A.C. A general statistical analysis for fMRI data. Neuroimage 15 1 (2002) 1-15
94. Xu H., Wu L.J., Wang H., Zhang X., Vadakkan K.I., Kim S.S., Steenland H.W., and Zhuo M. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J. Neurosci. 28 29 (2008) 7445-7453
95. Yoon Y.W., Lee D.H., Lee B.H., Chung K., and Chung J.M. Different strains and substrains of rats show different levels of neuropathic pain behaviors. Exp. Brain Res. 129 2 (1999) 167-171
96. Zhang L., Zhang Y., and Zhao Z.Q. Anterior cingulate cortex contributes to the descending facilitatory modulation of pain via dorsal reticular nucleus. Eur. J. Neurosci. 22 5 (2005) 1141-1148
97. Zimmermann M. Pathobiology of neuropathic pain. Eur. J. Pharmacol. 429 1-3 (2001) 23-37