Cerebral cortex modulation of pain

Acta Pharmacologica Sinica

Volumn 30, Issue 1, 2009, Pages 31-41

  Xie, Yu Feng ^a,b   Huo, Fu Quan ^a   Tang, Jing Shi ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Agranular insular cortex; Anterior cingulate cortex; Motor cortex; Nociception; Periaqueductal gray; Primary and secondary somatosensory cortices; Ventrolateral orbital cortex

Indexed keywords

1 [2 (BENZHYDRYLOXY)ETHYL] 4 (3 PHENYLPROPYL)PIPERAZINE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMANTADINE; BICUCULLINE; CHOLECYSTOKININ; DICLOFENAC; DIZOCILPINE; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; GABOXADOL; LIDOCAINE; METABOTROPIC RECEPTOR 3; MORPHINE; MU OPIATE RECEPTOR; MUSCIMOL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NALOXONE; OPIATE; STRYCHNINE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

BRAIN CORTEX; BRAIN FUNCTION; CINGULATE GYRUS; DRUG RECEPTOR BINDING; DRUG TARGETING; FEEDBACK SYSTEM; GLIA CELL; HUMAN; INSULA; MOTOR CORTEX; NEUROMODULATION; NEUROPATHIC PAIN; NEUROTRANSMISSION; NONHUMAN; ORBITAL CORTEX; PAIN; PERIAQUEDUCTAL GRAY MATTER; REVIEW; SOMATOSENSORY CORTEX; ANIMAL; BRAIN MAPPING; HISTOLOGY; METABOLISM; PAIN ASSESSMENT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN MAPPING; CEREBRAL CORTEX; HUMANS; NEUROTRANSMITTER AGENTS; PAIN; PAIN MEASUREMENT;

EID: 64849088457     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2008.14     Document Type: Review

References (112)

1. Melzack R. From the gate to the neuromatrix. Pain 1999; Suppl 6: S121-S126.
2. Sewards TV, Sewards MA. The medial pain system: neural representations of the motivational aspect of pain. Brain Res Bull 2002: 59: 163-80.
3. Casey KL. Forebrain mechanisms of nociception and pain: analysis through imaging. Proc Natl Acad Sci USA 1999; 96: 7668-74.
4. Ploner M, Schnitzler A. Cortical representation of pain. Nervenarzt 2004: 75: 962-9.
5. 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.
6. Ohara P T, Vit JP, Jasmin L. Cortical modulation of pain. Cell Mol Life Sci 2005; 62: 44-52.
7. Garcia-Larrea L, Peyron R. Motor cortex stimulation for neuropathic pain: From phenomenology to mechanisms. Neuroimage 2007; 37: 71-9.
8. Lima MC, Fregni F. Motor cortex stimulation for chronic pain: systematic review and meta-analysis of the literature. Neurology 2008; 70: 2329-37.
9. Treede RD, Kenshalo DR, Gracely RH, Jones AK. The cortical representation of pain. Pain 1999; 79: 105-11.
10. Vogt BA, Sikes RW. The medial pain system, cingulate cortex, and parallel processing of nociceptive information. Prog Brain Res 2000; 122: 223-35.
11. Tang JS, Xie YF, Huo FQ, Zhao M, Qu CL, Wang J, Wang JY. The Role of Thalamic Nucleus Submedius and Ventrolateral Orbital Cortex in Modulation of Nociception. In: Hu F, editor. Pain research progress: migraine, fibromyalgia and related pain. NOVA Publishers; 2008. p25-69.
12. Lopez-Avila A, Coffeen U, Ortega-Legaspi JM, del Angel R, Pellicer F. Dopamine and NMDA systems modulate long-term nociception in the rat anterior cingulate cortex. Pain 2004; 111: 136-43.
13. Ohara PT, Granato A, Moallem TM, Wang BR, Tillet Y, Jasmin L. Dopaminergic input to GABAergic neurons in the rostral agranular insular cortex of the rat. J Neurocytol 2003; 32: 131-41.
14. Wood PB. Role of central dopamine in pain and analgesia. Expert Rev Neurother 2008; 8: 781-97.
15. Coffeen U, Lopez-Avila A, Ortega-Legaspi JM, del Angel R, Lopez-Munoz FJ, Pellicer F. Dopamine receptors in the anterior insular cortex modulate long-term nociception in the rat. Eur J Pain 2008; 12: 535-43.
16. Price DD. Psychological and neural mechanisms of the affective dimension of pain. Science 2000; 288: 1769-72.
17. Sewards T V, Sewards M. Separate, parallel sensory and hedonic pathways in the mammalian somatosensory system. Brain Res Bull 2002; 58: 243-60.
18. Vogt BA. Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 2005; 6: 533-44.
19. Wang CC, Shyu BC. Differential projections from the mediodorsal and centrolateral thalamic nuclei to the frontal cortex in rats. Brain Res 2004; 995: 226-35.
20. Bingel U, Lorenz J, Schoell E, Weiller C, Buchel C. Mechanisms of placebo analgesia: rACC recruitment of a subcortical antinociceptive network. Pain 2006; 120: 8-15.
21. Svensson P, Minoshima S, Beydoun A, Morrow TJ, Casey KL. Cerebral processing of acute skin and muscle pain in humans. J Neurophysiol 1997; 78: 450-60.
22. Derbyshire SW, Jones AK, Creed F, Starz T, Meltzer CC, Townsend DW, et al. Cerebral responses to noxious thermal stimula tion in chronic low back pain patients and normal controls. Neuroimage 2002; 16: 158-68.
23. 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.
24. Yang JW, Shih HC, Shyu BC. Intracortical circuits in rat anterior cingulate cortex are activated by nociceptive inputs mediated by medial thalamus. J Neurophysiol 2006; 96: 3409-22.
25. Sikes RW, Vogt LJ, Vogt BA. Distribution and properties of visceral nociceptive neurons in rabbit cingulate cortex. Pain 2008; 135: 164-70.
26. Zhang L, Zhang Y, Zhao ZQ. Anterior cingulate cortex contributes to the descending facilitatory modulation of pain via dorsal reticular nucleus. Eur J Neurosci 2005; 22: 1141-8.
27. Calejesan AA, Kim SJ, Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain 2000; 4: 83-96.
28. Cao Z, Wu X, Chen S, Fan J, Zhang R, Owyang C, et al. Anterior cingulate cortex modulates visceral pain as measured by viscero-motor responses in viscerally hypersensitive rats. Gastroenterology 2008; 134: 535-43.
29. Koyama T, Tanaka YZ, Mikami A. Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain. Neuroreport 1998; 9: 2663-7.
30. Iwata K, Kamo H, Ogawa A, Tsuboi Y, Noma N, Mitsuhashi Y, et al. Anterior cingulate cortical neuronal activity during perception of noxious thermal stimuli in monkeys. J Neurophysiol 2005; 94: 1980-91.
31. Valet M, Sprenger T, Boecker H, Willoch F, Rummeny E, Conrad B, et al. Distraction modulates connectivity of the cingulo-frontal cortex and the midbrain during pain - an fMRI analysis. Pain 2004; 109: 399-408.
32. Neto FL, Schadrack J, Platzer S, Zieglgansberger W, Tolle TR, Castro-Lopes JM. Up-regulation of metabotropic glutamate receptor 3 mRNA expression in the cerebral cortex of mono-arthritic rats. J Neurosci Res 2001; 63: 356-67.
33. Wu X, Gao J, Yan J, Fan J, Owyang C, Li Y. Role for NMDA receptors in visceral nociceptive transmission in the anterior cingulate cortex of viscerally hypersensitive rats. Am J Physiol Gastrointest Liver Physiol 2008; 294: G918-G927.
34. Ren WH, Guo JD, Cao H, Wang H, Wang PF, Sha H, et al. Is endogenous D-serine in the rostral anterior cingulate cortex necessary for pain-related negative affect? J Neurochem 2006; 96: 1636-47.
35. Baumgartner U, Buchholz HG, Bellosevich A, Magerl W, Siessmeier T, Rolke R, et al. High opiate receptor binding potential in the human lateral pain system. Neuroimage 2006; 30: 692-9.
36. Jones AK, Watabe H, Cunningham VJ, Jones T. Cerebral decreases in opioid receptor binding in patients with central neuropathic pain measured by [11C]diprenorphine binding and PET. Eur J Pain 2004; 8: 479-85.
37. 11C]diprenorphine PET study. Pain 2004; 108: 213-20.
38. Zubieta JK, Smith YR, Bueller JA, Xu Y, Kilbourn MR, Jewett DM, et al. Regional mu opioid receptor regulation of sensory and afective dimensions of pain. Science 2001; 293: 311-5.
39. Erel U, Arborelius L, Brodin E. Increased cholecystokinin release in the rat anterior cingulate cortex during carrageenan-induced arthritis. Brain Res 2004; 1022: 39-46.
40. Heilborn U, Rost BR, Arborelius L, Brodin E. Arthritis-induced increase in cholecystokinin release in the rat anterior cingulate cortex is reversed by diclofenac. Brain Res 2007; 1136: 51-8.
41. Pellicer F, Lopez-Avila A, Coffeen U, Manuel Ortega-Legaspi J, Angel RD. Taurine in the anterior cingulate cortex diminishes neuropathic nociception: a possible interaction with the glycine(A) receptor. Eur J Pain 2007; 11: 444-51.
42. Kuzumaki N, Narita M, Narita M, Hareyama N, Niikura K, Nagumo Y, et al. Chronic pain-induced astrocyte activation in the cingulate cortex with no change in neural or glial differentiation from neural stem cells in mice. Neurosci Lett 2007; 415: 22-7.
43. Narita M, Kuzumaki N, Narita M, Hareyama N, Miyatake M, Shindo K, et al. Chronic pain-induced emotional dysfunction is associated with astrogliosis due to cortical delta-opioid receptor dysfunction. J Neurochem 2006; 97: 1369-78.
44. Jasmin L, Burkey AR, Granato A, Ohara PT. Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J Comp Neurol 2004; 468: 425-40.
45. Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguiere F. Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb Cortex 2002;12: 376-85.
46. Frot M, Mauguiere F. Dual representation of pain in the operculo-insular cortex in humans. Brain 2003; 126: 438-50.
47. Frot M, Magnin M, Mauguiere F, Garcia-Larrea L. Human SII and posterior insula differently encode thermal laser stimuli. Cereb Cortex 2007; 17: 610-20.
48. Schnitzler A, Ploner M. Neurophysiology and functional neuro-anatomy of pain perception. J Clin Neurophysiol 2000; 17: 592-603.
49. Burkey AR, Carstens E, Wenniger JJ, Tang J, Jasmin L. An opioidergic cortical antinociception triggering site in the agranular insular cortex of the rat that contributes to morphine antinociception. J Neurosci 1996; 16: 6612-23.
50. Xie YF, Wang J, Huo FQ, Jia H, Tang JS. Mu but not delta and kappa opioid receptor involvement in ventrolateral orbital cortex opioid-evoked antinociception in formalin test rats. Neuroscience 2004; 126: 717-26.
51. Maarrawi J, Peyron R, Mertens P, Costes N, Magnin M, Sindou M, et al. Differential brain opioid receptor availability in central and peripheral neuropathic pain. Pain 2007; 127: 183-94.
52. Jasmin L, Rabkin SD, Granato A, Boudah A, Ohara PT. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature 2003; 424: 316-20.
53. Burkey AR, Carstens E, Jasmin L. Dopamine reuptake inhibition in the rostral agranular insular cortex produces antinociception. J Neurosci 1999; 19: 4169-79.
54. Coffeen U, Lopez-Avila A, Ortega-Legaspi JM, del Angel R, Lopez-Munoz FJ, Pellicer F. Dopamine receptors in the anterior insular cortex modulate long-term nociception in the rat. Eur J Pain 2008; 12: 535-43.
55. Kanda M, Nagamine T, Ikeda A, Ohara S, Kunieda T, Fujiwara N, et al. Primary somatosensory cortex is actively involved in pain processing in human. Brain Res 2000; 853: 282-9.
56. Gojyo F, Sugiyo S, Kuroda R, Kawabata A, Varathan V, Shigenaga Y, et al. Efects of somatosensory cortical stimulation on expression of c-Fos in rat medullary dorsal horn in response to formalin-induced noxious stimulation. J Neurosci Res 2002; 68: 479-88.
57. Kuroda R, Kawao N, Yoshimura H, Umeda W, Takemura M, Shigenaga Y, et al. Secondary somatosensory cortex stimulation facilitates the antinociceptive effect of the NO synthase inhibitor through suppression of spinal nociceptive neurons in the rat. Brain Res 2001; 903: 110-6.
58. Youell PD, Wise RG, Bentley DE, Dickinson MR, King TA, Tracey I, et al. Lateralisation of nociceptive processing in the human brain; a functional magnetic resonance imaging study. Neuroimage 2004; 23: 1068-77.
59. Forss N, Raij TT, Seppa M, Hari R. Common cortical network for first and second pain. Neuroimage 2005; 24: 132-42.
60. Peyron R, Laurent B, Garcia-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis (2000). Neurophysiol Clin 2000; 30: 263-88.
61. Mazzola L, Isnard J, Mauguiere F. Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses. Cereb Cortex 2006; 16: 960-8.
62. Wang JY, Chang JY, Woodward DJ, Baccala LA, Han JS, Luo F. Corticofugal influences on thalamic neurons during nociceptive transmission in awake rats. Synapse 2007; 61: 335-42.
63. Coffeld JA, Bowen KK, Miletic V. Retrograde tracing of projections between the nucleus submedius, the ventrolateral orbital cortex, and the midbrain in the rat. J Comp Neurol 1992; 321: 488-99.
64. Craig AD Jr, Wiegand SJ, Price JL. The thalamo-cortical projection of the nucleus submedius in the cat. J Comp Neurol 1982; 206: 28-48.
65. Yoshida A, Dostrovsky JO, Chiang CY. The afferent and efferent connections of the nucleus submedius in the rat. J Comp Neurol 1992; 324: 115-33.
66. Li YQ, Takada M, Matsuzaki S, Shinonaga Y, Mizuno N. Identifcation of periaqueductal gray and dorsal raphe nucleus neurons projecting to both the trigeminal sensory complex and forebrain structures: a fluorescent retrograde double-labeling study in the rat. Brain Res 1993; 623: 267-77.
67. Floyd NS, Price JL, Ferry AT, Keay K, Bandler R. Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 2000; 422: 556-78.
68. Floyd NS, Price JL, Ferry AT, Keay K, Bandler R. Orbitomedial prefrontal cortical projections to hypothalamus in the rat. J Comp Neurol 2001; 432: 307-28.
69. Reep RL, Corwin JV, King V. Neuronal connections of orbital cortex in rats; topography of cortical and thalamic afferents. Exp Brain Res 1996; 111: 215-32.
70. Behbehani MM. Functional characteristics of the midbrain periaqueductal gray. Prog Neurobiol 1995; 46: 575-605.
71. GRNTHAM EG. Prefrontal lobotomy for relief of pain, with a report of a new operative technique. J Neurosurg 1951; 8: 405- 10.
72. Cooper SJ. Anaesthetisation of prefrontal cortex and response to noxious stimulation. Nature 1975; 254: 439-40.
73. Backonja M, Miletic V. Responses of neurons in the rat ventro-lateral orbital cortex to phasic and tonic nociceptive stimulation. Brain Res 1991; 557: 353-5.
74. Backonja M, Wang B, Miletic V. Responses of neurons in the ventrolateral orbital cortex to noxious cutaneous stimulation in a rat model of peripheral mononeuropathy. Brain Res 1994; 639: 337-40.
75. Follet K, Dirks B. Responses of neurons in ventrolateral orbital cortex to noxious visceral stimulation in the rat. Brain Res 1995; 669: 157-62.
76. Snow PJ, Lumb BM, Cervero F. The representation of prolonged and intense, noxious somatic and visceral stimuli in the ventro-lateral orbital cortex of the cat. Pain 1992; 48: 89-99.
77. Yang SW, Follett KA. The effect of morphine on responses of ventrolateral orbital cortex (VLO) neurons to colorectal distension in the rat. Brain Res 1998; 808: 101-5.
78. Zhang S, Tang JS, Yuan B, Jia H. Inhibitory effects of electrical stimulation of ventrolateral orbital cortex on the rat jaw-opening refex. Brain Res 1998; 813: 359-66.
79. Zhang YQ, Tang JS, Yuan B, Jia H. Inhibitory effects of electrically evoked activation of ventrolateral orbital cortex on the tail-flick refex are mediated by periaqueductal gray in rats. Pain 1997; 72: 127-35.
80. Zhao M, Wang JY, Jia H, Tang JS. Roles of different subtypes of opioid receptors in mediating the ventrolateral orbital cortex opioid-induced inhibition of mirror-neuropathic pain in the rat. Neuroscience 2007; 144: 1486-94.
81. Zhao M, Wang JY, Jia H, Tang JS. mu- but not delta- and kappa-opioid receptors in the ventrolateral orbital cortex mediate opioid-induced antiallodynia in a rat neuropathic pain model. Brain Res 2006; 1076: 68-77.
82. Huang X, Tang JS, Yuan B, Jia H. Morphine applied to the ventrolateral orbital cortex produces a naloxone-reversible antino-ciception in the rat. Neurosci Lett 2001; 299: 189-92.
83. Qu CL, Tang JS, Jia H. Involvement of GABAergic modulation of antinociception induced by morphine microinjected into the ventrolateral orbital cortex. Brain Res 2006; 1073-1074: 281-9.
84. Baliki M, Al Amin HA, Atweh SF, Jaber M, Hawwa N, Jabbur SJ, et al. Attenuation of neuropathic manifestations by local block of the activities of the ventrolateral orbito-frontal area in the rat. Neuroscience 2003; 120: 1093-104.
85. Grachev ID, Fredrickson BE, Apkarian AV. Brain chemistry reflects dual states of pain and anxiety in chronic low back pain. J Neural Transm 2002; 109: 1309-34.
86. Zhang S, Tang JS, Yuan B, Jia H. Inhibitory effects of glutamate-induced activation of thalamic nucleus submedius are mediated by ventrolateral orbital cortex and periaqueductal gray in rats. Eur J Pain 1998;2: 153-63.
87. Zhang S, Tang JS, Yuan B, Jia H. Electrically-evoked inhibitory effects of the nucleus submedius on the jaw-opening reflex are mediated by ventrolateral orbital cortex and periaqueductal gray mater in the rat. Neuroscience 1999; 92: 867-75.
88. Zhang S, Tang JS, Yuan B, Jia H. Involvement of the frontal ventrolateral orbital cortex in descending inhibition of nociception mediated by the periaqueductal gray in rats. Neurosci Let. 1997; 224: 142-6.
89. Hutchison WD, Harfa L, Dostrovsky JO. Ventrolateral orbital cortex and periaqueductal gray stimulation-induced effects on on- and off-cells in the rostral ventromedial medulla in the rat. Neuroscience 1996; 70: 391-407.
90. McLean S, Rothman RB, Herkenham M. Autoradiographic localization of mu- and delta-opiate receptors in the forebrain of the rat. Brain Res 1986; 378: 49-60.
91. Huo FQ, Wang J, Li YQ, Chen T, Han F, Tang JS. GABAergic neurons express mu-opioid receptors in the ventrolateral orbital cortex of the rat. Neurosci Lett 2005; 382: 265-8.
92. Huo FQ, Qu CL, Li YQ, Tang JS, Jia H. GABAergic modulation is involved in the ventrolateral orbital cortex 5-HT(1A) receptor activation-induced antinociception in the rat. Pain 2008; doi:10.1016/j.pain.2008.05.013.
93. Heinricher MM, Morgan MM, Tortorici V, Fields HL. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 1994; 63: 279-88.
94. Brown JA, Pilitsis JG. Motor cortex stimulation for central and neuropathic facial pain: a prospective study of 10 patients and observations of enhanced sensory and motor function during stimulation. Neurosurgery 2005; 56: 290-7.
95. Lazorthes Y, Sol JC, Fowo S, Roux FE, Verdie JC. Motor cortex stimulation for neuropathic pain. Acta Neurochir Suppl 2007; 97: 37-44.
96. Lefaucheur JP, Drouot X, Menard-Lefaucheur I, Lefaucheur JP, Drouot X, Menard-Lefaucheur I. Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain. J Neurol Neurosurg Psychiatry 2004; 75: 612-6.
97. Saitoh Y, Hirayama A, Kishima H, Shimokawa T, Oshino S, Hirata M, et al. Reduction of intractable deafferentation pain due to spinal cord or peripheral lesion by high-frequency repetitive transcranial magnetic stimulation of the primary motor cortex. J Neurosurg 2007; 107: 555-9.
98. Peyron R, Faillenot I, Mertens P, Laurent B, Garcia-Larrea L. Motor cortex stimulation in neuropathic pain. Correlations between analgesic effect and hemodynamic changes in the brain. A PET study. Neuroimage 2007; 34: 310-21.
99. Saitoh Y, Osaki Y, Nishimura H, Hirano S, Kato A, Hashikawa K, et al. Increased regional cerebral blood flow in the contralateral thalamus after successful motor cortex stimulation in a patient with poststroke pain. J Neurosurg 2004; 100: 935-9.
100. Passard A, Atal N, Benadhira R, Brasseur L, Saba G, Sichere P, et al. Effects of unilateral repetitive transcranial magnetic stimulation of the motor cortex on chronic widespread pain in fibromyalgia. Brain 2007; 130: 2661-70.
101. Cioni B, Meglio M. Motor cortex stimulation for chronic non-malignant pain: current state and future prospects. Acta Neurochir Suppl 2007; 97: 45-9.
102. Maarrawi J, Peyron R, Mertens P, Costes N, Magnin M, Sindou M, et al. Motor cortex stimulation for pain control induces changes in the endogenous opioid system. Neurology 2007; 69: 827-34.
103. Lefaucheur JP, Drouot X, Menard-Lefaucheur I, Keravel Y, Nguyen JP. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology 2006; 67: 1568-74.
104. Laalou FZ, de Vasconcelos AP, Oberling P, Jeltsch H, Cassel JC, Pain L. Involvement of the basal cholinergic forebrain in the mediation of general (propofol) anesthesia. Anesthesiology 2008; 108: 888-96.
105. Ma J, Leung LS. Limbic system participates in mediating the effects of general anesthetics. Neuropsychopharmacology 2006; 31: 1177-92.
106. Watkins LR, Maier SF. Glia and Pain: Past, Present, and Future. In: Merskey H, Loeser JD, Dubner R (eds) The Paths of Pain 1975-2005. IASP PRESS 2005.
107. Wieseler-Frank J, Maier SF, Watkins LR. Glial activation and pathological pain. Neurochem Int 2004; 45: 389-95.
108. Hansson E. Could chronic pain and spread of pain sensation be induced and maintained by glial activation? Acta Physiol (Oxf) 2006; 187: 321-7.
109. Xie YF, Zhang S, Chiang CY, Hu JW, Dostrovsky JO, Sessle BJ. Involvement of glia in central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). Brain BehavImmun 2007; 21: 634-41.
110. Xie YF. Glial involvement in trigeminal central sensitization. Acta Pharmacol Sin 2008; 29: 641-5.
111. Price JL. Prefrontal cortical networks related to visceral function and mood. Ann NY Acad Sci 1999; 877: 383-96.
112. Zhang F, Vadakkan KI, Kim SS, Wu LJ, Shang Y, Zhuo M. Selective activation of microglia in spinal cord but not higher cortical regions following nerve injury in adult mouse. Mol Pain 2008; 4: 15.