CoChat
Sign Up
Cited by 1,774Pain Mechanisms and TreatmentsPain Management and TreatmentIon Channels and Receptors

The DOI matches its Crossref record; 1,976 of the 1,976 references it cites were found in a registry or an index.

The induction of pain: an integrative review

Millan, Mark J.·1999·Progress in Neurobiology
DOI 10.1016/s0301-0082(98)00048-3
Open this paper in CoChat — free account

Abstract

The highly disagreeable sensation of pain results from an extraordinarily complex and interactive series of mechanisms integrated at all levels of the neuroaxis, from the periphery, via the dorsal horn to higher cerebral structures. Pain is usually elicited by the activation of specific nociceptors ('nociceptive pain'). However, it may also result from injury to sensory fibres, or from damage to the CNS itself ('neuropathic pain'). Although acute and subchronic, nociceptive pain fulfils a warning role, chronic and/or severe nociceptive and neuropathic pain is maladaptive. Recent years have seen a progressive unravelling of the neuroanatomical circuits and cellular mechanisms underlying the induction of pain. In addition to familiar inflammatory mediators, such as prostaglandins and bradykinin, potentially-important, pronociceptive roles have been proposed for a variety of 'exotic' species, including protons, ATP, cytokines, neurotrophins (growth factors) and nitric oxide. Further, both in the periphery and in the CNS, non-neuronal glial and immunecompetent cells have been shown to play a modulatory role in the response to inflammation and injury, and in processes modifying nociception. In the dorsal horn of the spinal cord, wherein the primary processing of nociceptive information occurs, N-methyl-D-aspartate receptors are activated by glutamate released from nocisponsive afferent fibres. Their activation plays a key role in the induction of neuronal sensitization, a process underlying prolonged painful states. In addition, upon peripheral nerve injury, a reduction of inhibitory interneurone tone in the dorsal horn exacerbates sensitized states and further enhance nociception. As concerns the transfer of nociceptive information to the brain, several pathways other than the classical spinothalamic tract are of importance: for example, the postsynaptic dorsal column pathway. In discussing the roles of supraspinal structures in pain sensation, differences between its 'discriminative-sensory' and 'affective-cognitive' dimensions should be emphasized. The purpose of the present article is to provide a global account of mechanisms involved in the induction of pain. Particular attention is focused on cellular aspects and on the consequences of peripheral nerve injury. In the first part of the review, neuronal pathways for the transmission of nociceptive information from peripheral nerve terminals to the dorsal horn, and therefrom to higher centres, are outlined. This neuronal framework is then exploited for a consideration of peripheral, spinal and supraspinal mechanisms involved in the induction of pain by stimulation of peripheral nociceptors, by peripheral nerve injury and by damage to the CNS itself. Finally, a hypothesis is forwarded that neurotrophins may play an important role in central, adaptive mechanisms modulating nociception. An improved understanding of the origins of pain should facilitate the development of novel strategies for its more effective treatment.

Overview

Integrity signals

Registry

Crossref · 10.1016/s0301-0082(98)00048-3

Cites

1976 of 1976 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Items 401–600 of 1,976

Research works printed but not linked: 119

  1. Abrams, 1996, Tutorial 27: the antidepressants, anticonvulsants and less frequently used primary and adjuvant analgesics, Pain Digest., 6, 374
  2. Aguayo, A. J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. In: Synaptic Plasti-ticity, pp. 457–484. Ed. C. W. Cotman. Raven Press, New York
  3. Aldskogius, H., Arvidsson, J. and Grant, G. (1992) Axotomy-induced changes in primary sensory neurons. In: Sensory Neurons: Diversity, Development and Plasticity, pp. 363–383. Ed. S. A. Scott. Oxford University Press, Oxford
  4. Anghinah, 1994, Effect of baclofen on pain in diabetic neuropathy, Muscle and Nerve., 17, 958
  5. Barbour, 1997, Intersynaptic fusion of neurotransmitters, Trends Neurosci., 20, 377
  6. Bennett, 1996, The effect of BDNF on c-fos and NOS expression in dorsal horn neurons of the adult rat spinal cord, Am. Soc. Neurosci., 22, 993
  7. Bernard, J.-F., Bester, H. and Besson, J.-M. (1995) The spino-parabrachio-amygdaloid and -hypothalamic nociceptive pathways. In: Forebrain Areas Involved in Pain Processing, pp. 27–48. Eds. J.-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  8. Berzaghi, 1995, Neurotrophins induce acute transmitter-mediated changes in brain electrical activity, Am. Soc. Neurosci., 21, 545
  9. Bevan, 1993, Protons and capsaicin activate the same ion channels in rat isolated dorsal root ganglion neurones, J. Physiol., 459, 401
  10. Boivie, J. (1994) Central pain. In Textbook of Pain, 3rd edn, pp. 871–902. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  11. Boivie, J. and Östeberg, A. (1995) Central pain syndrome. In: Forebrain Areas Involved in Pain Processing, pp. 239–252, Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  12. Bouhassira, 1997, Reduction of temporal summation of nociceptive flexion (RIII) reflex and pain after low systemic doses of ketamine, Am. Soc. Neurosci., 23, 1015
  13. Bowles, 1994, Nerve growth factor evokes iGGRP release by a phosphorylation-dependent mechanism, Am. Soc. Neurosci., 20, 18
  14. Brewer, 1995, Acute reorganization of rat nucleus gracilis following peripheral denervation: role of GABA in functional plasticity, Am. Soc. Neurosci., 21, 110
  15. Bushnell, M. C. (1995) Thalamic processing of sensory-discriminative and affective-motivational dimensions of pain. In: Forebrain Areas Involved in Pain Processing, pp. 63–78. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  16. Casey, K. L. and Minoshima, S. (1995) The forebrain network for pain: an emerging image. In: Forebrain Areas Involved in Pain Processing, pp. 213–228. Eds. J-M. Besson, O. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  17. Chessel, 1997, Pharmacological characteristics of microglial P2X7 purinoceptors, Br. J. Pharmac., 120, 127P
  18. Coggeshall, R. E. (1994) A possible relationship between neuropathic pain and central sensory sprouting following peripheral nerve lesions. In: Peripheral Neurons in Nociception: Physico-pharmacological Aspects, pp. 201–208, Eds. J.-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  19. Cohen, 1996, Expression of 5-HT1Dβ, 5-HT1F, 5-HT2B, 5-HT2C and 5-HT7 receptor mRNAs in human intraparenchymal microvessels and related cells in cultures, Am. Soc. Neurosci., 22, 1787
  20. Connor, H. E. and Beattie, D. T. (1996) 5-HT receptor subtypes and migraine. In: Migraine: Pharmacology and Genetics, pp. 18–28, Eds. M. Sandler, M. Ferrari and S. Harnett. Chapman and Hall, London
  21. Coyle, 1996, Efficacy of animal models for neuropathic pain, Pain Digest, 6, 7
  22. Craig, A. D. (1994) Emotional aspects of pain. In: Textbook of Pain, 3rd edn, pp. 261–274. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  23. Craig, A. D. (1995) Supraspinal projections of lamina I neurons. In: Forebrain Areas Involved in Pain Processing, pp. 13–26. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  24. Davis, 1997, des Arg BK-induced mechanical hyperalgesia and analgesia in the rat: involvement of IL-1, prostaglandins and peripheral opioids, Br. J. Pharmac., 120, 74P
  25. Davis, 1994, Overexpression of NGF in transgenic mice induces novel sympathetic projections to primary sensory neurons, Am. Soc. Neurosci., 20, 1090
  26. De Groot, 1997, μ-Opioid receptor plasticity in the superficial dorsal horn following sciatic nerve transaction, Am. Soc. Neurosci., 23, 1015
  27. Devor, M (1994) The pathophysiology of damaged peripheral nerves. In: Textbook of Pain, 3rd edn, pp. 79–100. Eds. R. Melzack and P. D. Wall. Churchill-Livingstone, Edinburgh
  28. Devor, 1995, Peripheral and central nervous system mechanisms of sympathetic related pain, Pain Clinic., 8, 5
  29. Dong, W. K. and Chudler, E. H. (1995) Cortical nociceptive mechanisms. A review of neurophysiological and behavioral evidence in the primate. In: Forebrain Areas Involved in Pain Processing, pp. 183–196. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  30. Dostrovsky, J. O., Hutchison, W. D., Davis, K. D. and Lozano, A. (1995) Potential role of orbital and cingulate cortices in nociception. In: Forebrain Areas Involved in Pain Processing, pp. 171–182. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  31. Eaton, S. A. and Salt, T. E. (1995) The role of excitatory amino-acid receptors in thalamic nociception. In: Forebrain Areas Involved in Pain Processing, pp. 131–142. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  32. Fields, H. L. and Basbaum, A. I. (1994) Central nervous system mechanisms of pain modulation. In: Textbook of Pain, 3rd edn, pp. 243–257. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  33. Fields, H. L. and Rowbotham, M. C. (1994) Multiple mechanisms of neuropathic pain: a clinical perspective. In: Proceedings of the 7th World Congress on Pain, Progress in Pain Research and Management, Vol. 2, pp. 437–454. Eds. G. F. Gebhart, D. L. Hammond and T. S. Jensen. IASP Press, Seattle
  34. Frost, S. A., Raja, S. N., Campbell, J. N., Meyer, R. A. and Khan, A. A. (1988) Does hyperalgesia to cooling stimuli characterize patients with sympathetically maintened pain (reflex sympathetic dystrophy)? In: Proceedings of the Vth World Congress on Pain, pp. 151–156. Eds. R. Dubner, G. F. Gebhart and M. R. Bond. Elsevier, Amsterdam
  35. Garland, 1996, Mechanism of desensitization and resensitization of G protein-coupled neurokinin1 and neurokinin2 receptors, Mol. Pharmac., 49, 438
  36. Gentry, 1997, The effects of sympathectomy on the nerve growth factor (NGF)—induced nociceptive responses in normal and neuropathic rats, Br. J. Pharmac., 120, 231P
  37. Giesler, G. J. (1995b) The spino-hypothalamic tract. In: Forebrain Areas Involved in Pain Processing, pp. 49–62. Eds. J.-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  38. Gold, B. G. and Spencer, P. S. (1993) Neurotrophic function in normal nerve and in peripheral neuropathies. In: Neuroregeneration, pp. 101–122. Ed. A. Gorio. Raven Press, New York
  39. Guilbaud, G. (1988) Peripheral and central electrophysiological mechanisms of joint and muscle pain. In: Proceedings of the Vth World Congress on pain, pp. 201–215. Eds. R. Dubner, G. F. Gebhart and M. R. Bond. Elsevier, Amsterdam
  40. Guilbaud, G. and Benoist, J. M. (1995) Thalamic and cortical processing in rat models of clinical pain. In: Forebrain Areas Involved in Pain Processing, pp. 79–92. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  41. Guilbaud, G., Bernard, J.-F. and Besson, J.-M. (1994) Brain areas involved in nociception and pain. In: Textbook of Pain, 3rd edn, pp. 113–128. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  42. Hammond, 1996, Intrathecally administered cyclo-oxygenase-2 inhibitors attenuate carrageenan-induced thermal hyperalgesia in the rat, Am. Soc. Neurosci., 26, 712
  43. Han, 1994, Ectopic discharges from injured afferent fibers in a rat model of neuropathic pain, Am. Soc. Neurosci., 20, 760
  44. Handwerker, H. O. (1991) What peripheral mechanisms contribute to nociceptive transmission and hyperalgesia. In: Towards a New Pharmacotherapy of Pain, pp. 5–20. Eds. A. I. Basbaum and J.-M Besson. Wiley Press, New York
  45. Hargett, 1997, Upregulation of AMPA receptors in laminae III–V following dorsal rhizotomy: evidence for glutamate supersensitivity, Am. Soc. Neurosci., 23, 1015
  46. Heppenstall, 1997, LIF mRNA distribution in lumbar spinal cord and its modification by peripheral inflammaton and nerve injury, J. Physiol., 505P, 42P
  47. Herrero, 1995, Wind-up of spinal cord neurones is influenced by inflammation, spinalization, endogenous opioids and type of stimulation, Am. Soc. Neurosci., 21, 1407
  48. Houghton, 1997, The effect of dorsal column (DC) lesions upon the central actions of pancreatic afferent fibres in the rat, J. Physiol., 505P, 39P
  49. Hua, 1996, Involvement of cytokines in lipopolysaccaride-induced facilitation of CGRP release from capsaicin sensitive nerves in the trachea: studies with IL-1β and TNF-α, J. Neurophysiol., 16, 4742
  50. Hunter, 1996, The role of α and β adrenoceptors in a rodent model of neuropathic pain, Br. J. Pharmac., 117, 237P
  51. Huskisson, 1995, Effects of anti-inflammatory drugs on the progression of osteoarthritis of the knee, J. Rheumatol., 22, 1941
  52. Jänig, W. (1993) Spinal visceral afferents, sympathetic nervous system and referred pain. In: New Trends in Referred Pain and Hyperalgesia, pp. 83–98, Eds. L. Vecchiet, D. Abbe-Fessard, U. Lindblom and M. A. Giamberardino. Elsevier, Amsterdam
  53. Jones, A. K. P. and Derbyshire, S. W. G. (1995) Cortical and thalamic imaging in normal volunteers and patients with chronic pain. In: Forebrain Areas Involved in Pain Processing, pp. 229–238. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  54. Kawaja, 1997, Sympathetic axons invade the brains of mice overexpressing nerve growth factor, J. Comp. Neurol., 383, 60, 10.1002/(SICI)1096-9861(19970623)383:1<60::AID-CNE5>3.0.CO;2-J · DOI
  55. Keele, C. A. and Armstrong, D. (1964) Substances Producing Pain and Itch, p. 271. Arnold Press, London
  56. Kelly, 1997, Indomethacin prevents the IL-1β-induced increase in neural discharge and enhancement of kinin-mediated activation of C-fibre mechanociceptors innervating the rat knee joint, Br. J. Pharmac., 122, 357P
  57. Von Knorring, L. (1989) Serotonin metabolites in the CSF of chronic pain patients. In: Serotonin and Pain. Excerpta Medica, pp. 85–303. Ed. J. M. Besson. Elsevier, Amsterdam
  58. Koltzenburg, 1995, Electrophysiological analysis of cutaneous sensory neurons in neonatal wildtype mice and transgenic animals lacking BNDF, Am. Soc. Neurosci., 21, 1054
  59. Kress, M., Riedl, B., Rödl, J. and Reeh, P. W. (1994) Effects of nitric oxide, methylene blue and cyclic nucleotides on nociceptive nerve endings in rat skin in vitro. In: The Biology of Nitric Oxide: Physiology and Clinical Aspects, Vol. 3, pp. 319-323. Eds. S. Moncada, M. Feelisch, R. Busse and E. A. Higgs. Portlands Press, London
  60. Lawson, S. N. (1992) Morphological and biochemical cell types of sensory neurons. In: Sensory Neurons. Diversity, Development and Plasticity, pp. 27-59. Ed. P. Scott. Oxford University Press, New York
  61. Le Bars, D. (1988) Serotonin and pain, In: Neuronal Serotonin, pp. 171–230. Eds. N. N. Osborne and M. Hamon. Wiley and Sons, London
  62. Lenz, F. A. (1995) The region posterior inferior to the human thalamic principal sensory nucleus (Vc) may contribute to the affective dimension of pain through thalamo-corticolimbic connections. In: Forebrain Areas Involved in Pain Processing, pp. 119–130. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  63. Lenz, 1997, The sensory-limbic model of pain memory, Pain Forum, 6, 22, 10.1016/S1082-3174(97)70002-3 · DOI
  64. Levine, J. D. and Taiwo, Y. (1994) Inflammatory pain. In: Textbook of Pain, 3rd edn, 1524, pp. 45–56. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh.
  65. Lewis, T. (1942) Pain, p. 183. Macmillan Press, New York
  66. Lexin, 1996, Physiology of the neurotrophins, A. Rev. Neurosci., 19, 289, 10.1146/annurev.ne.19.030196.001445 · DOI
  67. Lin, Q., Peng, Y. B. and Willis, W. D. (1996d) The effects of 8-bromo-cGMP on the inhibition of primate spinothalamic neurons produced by stimulation in periaqueductal gray and GABA receptors. In: 8th World Congress on Pain, International Association for the Study of Pain, pp. 473–474
  68. Lindblom, U. (1985) Assessment of abnormal evoked pain in neurological pain patients and its relationship to spontaneous pain: a descriptive and conceptual model with some analytical results. In: Advances in Pain Resarch and Therapy, Vol. 9, pp. 409–424. Eds. H. L. Fields, R. Dubner, F. Cervero and L. E. Jones. Raven Press, New York
  69. Lombard, M.-C. and Larabi, Y. (1983) Electrophysiological study of the cervical dorsal horn cells in partially deafferented rats. In: Advances in Pain Research and Therapy, Vol. 5, p. 147. Eds. J. J. Bonica, U. Lindblom and A. Iggo. Raven Press, New York
  70. Lucaites, 1996, Autoradiographic localization of the serotonin1F (5-HT1F) receptor in rat brain using [3H]LY133,470, a selective 5-HT1F receptor radioligand, Am. Soc. Neurosci., 22, 1331
  71. Mailiani, A., Pagani, M. and Lombardi, F. (1984) Visceral versus somatic mechanisms. In: Textbook of Pain, pp. 100–121. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  72. Marcoux, 1994, Pharmacologic therapeutic window in acute stroke, Drug News Persp., 7, 228
  73. McGiven, 1997, Electrophysiological characterisation of the novel tetrodotoxin-sensitive sodium channel, rPN4, Br. J. Pharmac., 122, 366P
  74. McKenna, 1994, Bilateral VB thalamotomy does not reduce pain in the formalin test, Am. Soc. Neurosci., 20, 1572
  75. McMahon, S. B. (1994) Mechanisms of cutaneous, deep and visceral pain. In: Textbook of Pain, 3rd edn, pp. 129–153. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  76. Mense, S., Light, A. R. and Perl, E. R. (1981) Spinal terminations of subcutaneous high-threshold mechanoreceptors. In: Spinal Cord Sensation, pp. 111–123. Eds. A. G. Brown and M. Rethelyi. Scottish Academic Press, Edinburgh
  77. Meyer, R. A., Campbell, J. N. and Raja, S. N. (1994) Peripheral neural mechanisms of nociception In: Textbook of Pain, pp. 13–44. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  78. Millan, 1997, Autoreceptor and heteroceptor control of 5-HT, dopamine (DA) and noradrenaline (NAD) release in frontal cortex: strategies for improved antidepressant agents, Br. J. Pharmac., 122, 468P
  79. Millan, 1994, Multiple alpha2-adrenergic receptor subtypes. II. Evidence for a role of rat Rα2A-ARs in the control of nociception, motor behaviour and hippocampal synthesis of noradrenaline, J. Pharmac. Exp. Ther., 270, 958
  80. Miller, 1991, Interleukin-1 augments gamma-aminobyturic acidA receptor function in brain, Mol. Pharmac., 39, 105
  81. Monhemius, 1997, Descending influences differentially modulate superficial lamina I and deep multireceptive dorsal horn neurones in the rat, J. Physiol., 505, 43P
  82. Naciff, 1996, Differential expression of annexins I-VI in the rat dorsal root ganglia and spinal cord, J. Comp. Neurol., 368, 356, 10.1002/(SICI)1096-9861(19960506)368:3<356::AID-CNE3>3.0.CO;2-4 · DOI
  83. Nishiyama, 1993, Peripheral nerve injury enhances α2-adrenergic receptor expression by some DRG neurons, Am. Soc. Neurosci., 19, 499
  84. Olesen, J. and Janssen-Olesen, I. (1997) Novel targets for drug development in migraine. In: Headache Treatment: Trial Methodology and New Drugs Vol. 6, pp. 313–320, Eds. J. Olesen and P. Tfelt-Hansen. Lippincott-Raven Publishers, Philadelphia
  85. Paul, 1997, Effect of α2-adrenoceptor agonists on bradykinin-induced plasma protein extravasation in guinea-pig skin, Br. J. Pharmac., 120, 172P
  86. Perl, E. R. (1994) A re-evaluation of mechanisms leading to sympathetically related pain. In: Pharmacological Approaches to the Treatment of Chronic Pain: New Concepts and Critical Issues, pp. 129–150. Eds. H. L. Fields and J. C. Liebeskind. IASP Press, Seattle
  87. Perry, 1993, Macrophage response to central and peripheral nerve injury, Adv. Neurol., 5, 309
  88. Phebus, 1996, Characterization of LY 334,370, a potent and selective 5-HT1F receptor agonist, in the neurogenic dural inflammation model of migraine pain, Am. Soc. Neurosci., 22, 1331
  89. Price, D. D., Mao, J. and Mayer, D. J. (1995) Brain neural images of persistent pain states in rats using 2-DG autoradiography. In: Forebrain Areas Involved in Pain Processing, pp. 143–154. Eds. J. M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  90. Procacci, P. and Zoppi, M. (1983) Pathophysiolology and clinical aspects of visceral and referred pain. In: Proceedings of the Third World Congress on Pain, pp. 643–658. Eds. J. J. Bonica, U. Lindblom and A. Iggo. Raven Press, New York
  91. Procacci, P., Zoppi, M. and Maresca, M. (1994) Heart and vascular pain. In: Textbook of Pain, 3rd edn, pp. 541–554. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  92. Puttick, 1992, Excitatory action of prostaglandin E2 on rat neonatal cultured dorsal root ganglion cells, Br. J. Pharmac., 105, 133
  93. Ralston, H. J., Ohara, P. T. Meng, X. W. and Ralston, D. D. (1995) The organization of spinothalamic tract circuitry in the macaque and the role of GABA information processing. In: Forebrain Areas Involved in Pain Processing, pp. 1–13. Eds. J-M. Besson, G. Guilbaud and H. Ollat. John Libbey Eurotext, Paris
  94. Razzaque, 1997, Pharmacological analysis of 5-HT receptor-mediated vasoconstriction of human middle meningeal arteries: determining the contribution of 5-HT1B and 5-HT1F receptor activation, Br. J. Pharmac., 120, 211P
  95. Riaz, 1997, Stimulation of nerve growth factor levels in control and diabetic rats by treatment with clenbuterol, Br. J. Pharmac., 122, 291P
  96. Salvemini, 1996, New concepts in inflammation and therapy, Drug News Persp., 4, 204
  97. Sang, 1997, Analgesic effects of AMPA/kainate antagonist LY 293558 in human: reduction of capsaicin evoked allodynia and hyperalgesia but not sensations in normal skin, Am. Soc. Neurosci., 23, 1015
  98. Sansum, 1997, Characterisation of purinoceptors mediating responses to ATP on rat dorsal roots, Br. J. Pharmac., 120, 128P
  99. Schmidt, 1971, Pre-synaptic inhibition in the vertebrate nervous systems, Rev. Physiol. Biochem. Pharmac., 63, 21
  100. Sloan, 1991, Changes in PCP binding sites in rat spinal cord in an experimental model of acute, peripheral inflammation, Am. Soc. Neurosci., 17, 435
  101. Southall, 1996, LIF induces GAL but not VIP-immunoreactivity in small diameter rat sensory neurons in vivo, Am. Soc. Neurosci., 22, 769
  102. Sutton, 1997, Kainate receptor antagonist SYM 2081 attenuates mechanical allodynia and thermal hyperalgesia in a rat, Am. Soc. Neurosci., 23, 1015
  103. Szallasi, 1997, Perspectives on vanilloids in clinical practice, Drugs News Perspectives, 10, 522
  104. Tasker, R. R. (1990) Pain resulting from central nervous system pathology (central pain). In: The Management of Pain, Vol. 1, 2nd edn, pp. 266–283. Ed. J. J. Bonica. Lea and Febiger Press, Philadelphia
  105. Thomas, 1993, Nerve growth factor alleviates a painful peripheral neuropathy in rats, Am. Soc. Neurosci., 19, 969
  106. Thompson, 1997, LIF and NGF induce noradrenergic fibre sprouting in the intact dorsal root ganglion of adult rats in vivo, J. Physiol., 505.P, 42P
  107. Towers, 1997, GABAB receptors in spinal cord and dorsal root ganglia of sciatic nerve axotomised and control rats: localization of receptor protein by autoradiography using [3H]-CGP62349, Br. J. Pharmac., 122, 345P
  108. Trezise, 1997, Electrophysiological studies on the effects of lamotrigine on rat dorsal root ganglion neurones in vitro, Br. J. Pharmac., 122, 31P
  109. Vecchiet, L., Dragani, L., de Bigontina, P., Obletter, G. and Giamberardino, M. A. (1993) Experimental referred pain and hyperalgesia from muscles in humans. In: New Trends in Referred Pain in Hyperalgesia, pp. 222–232. Eds. L. Vecchiet, D. Albe-Fessard, U. Lindblom and M. A. Giamberardino. Elsevier, Amsterdam
  110. Verheggen, 1997, A comparison of 5-HT receptor mRNA in human temporal artery and brain, Naunyn-Schmiedberg's Arch. Pharmac., 355, R30
  111. Wang, 1997, The mode of action of bradykinin and other basic secretagogues on histamine release from rat peritoneal mast cells, Br. J. Pharmac., 122, 106P
  112. Weil-Fugazza, J. (1989) Central metabolism and release of serotonin in pain and analgesia. In: Serotonin and Pain, pp. 221–238. Ed. J. M. Besson. Elsevier, Amsterdam
  113. Wilcox, G. L. (1991) Excitatory neurotransmitters and pain. In: Pain Research and Clinical Management. Proc VIth World Congress on Pain, Vol. 4, pp. 97–117. Eds. M. R. Bond, J. E. Charlton and C. J. Woolf. Elsevier, Amsterdam
  114. Willingale, 1996, Evidence that prostaglandins may modulate wind-up in a spinal nociceptive reflex in anaesthetised rats, Br. J. Pharmac., 118, 49
  115. Willis, W. D. (1989) The origin and destination of pathways involved in pain transmission. In: Textbook of Pain, 2nd edn, pp. 112–127. Eds. P. D. Wall and R. Melzack. Churchill-Livingstone, Edinburgh
  116. Willis, W. D. (1994) Central plastic responses to pain. In: Proceeding of the 7th World Congress on Pain, Vol. 2, pp. 301–324. Eds. G. F. Gebhart, D. L. Hammond and T. S. Jensen. IASP Press, Seattle
  117. Yoshida, 1997, Organization of the descending projections from the parabrachial nuclear complex and spinal dorsal horn in the rat, J. Comp. Neurol., 383, 94, 10.1002/(SICI)1096-9861(19970623)383:1<94::AID-CNE8>3.0.CO;2-G · DOI
  118. Young, 1997, Behavioural and electrophysiological evidence supporting a role for group I metabotropic glutamate receptors in the mediation of nociceptive inputs to the rat spinal cord, Brain Res., 777, 161
  119. Zhang, 1994, Verapamil inhibits the spontaneous activities originating in dorsal root ganglion cells after chronic nerve constriction in rats, Am. Soc. Neurosci., 20, 760

Cited by

Sorted by citations

See all 1,774

Related

See all

Metadata

Authors
Millan, M. J.
Affiliations
Institut de Recherches Internationales Servier (France) (FR)
Corresponding author
Millan, Mark J.
ORCID
Millan, Mark J.
Venue
Progress in Neurobiology
Publisher
Elsevier BV
Published
1999-01
Volume
57
Issue
1
Pages
1-164
ISSN
0301-0082 (ISSN-L)
DOI
10.1016/s0301-0082(98)00048-3
OpenAlex
W2123258170
Cited by
1,774
References
1,976
Citations by year
2026: 6 · 2025: 24 · 2024: 22 · 2023: 30 · 2022: 53 · 2021: 40 · 2020: 42 · 2019: 49 · 2018: 61 · 2017: 68 · 2016: 72 · 2015: 66 · 2014: 76 · 2013: 74 · 2012: 93
FWCI
8.64
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Progress in Neurobiology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
  • Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
  • Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Keywords
pain induction, nociception, nociceptors, neuropathic pain, dorsal horn, NMDA receptor, neuronal sensitization, peripheral nerve injury, ATP, cytokines, nitric oxide, neurotrophins, glial modulation, dorsal column pathway, spinothalamic tract, affective pain
MeSH terms
Animals, Brain, Humans, Synaptic Transmission, Nociceptors, Pain, Spinal Cord

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review