PAIN
Volume 142, Issue 3 , Pages 245-254 , April 2009

NK1 receptor-expressing spinoparabrachial neurons trigger diffuse noxious inhibitory controls through lateral parabrachial activation in the male rat

  • Olivier Lapirot

      Affiliations

    • Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, F-63000 Clermont-Ferrand, France
    • Univ Clermont1, Clermont-Ferrand F-63000, France
  • ,
  • Raja Chebbi

      Affiliations

    • Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, F-63000 Clermont-Ferrand, France
    • Faculté médecine dentaire, Monastir, Tunisia
  • ,
  • Lénaic Monconduit

      Affiliations

    • Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, F-63000 Clermont-Ferrand, France
    • Univ Clermont1, Clermont-Ferrand F-63000, France
  • ,
  • Alain Artola

      Affiliations

    • Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, F-63000 Clermont-Ferrand, France
    • Univ Clermont1, Clermont-Ferrand F-63000, France
  • ,
  • Radhouane Dallel

      Affiliations

    • Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, F-63000 Clermont-Ferrand, France
    • Univ Clermont1, Clermont-Ferrand F-63000, France
    • CHU Clermont-Ferrand, Clermont-Ferrand F-63000, France
    • Corresponding Author InformationCorresponding author. Address: Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, 63000 Clermont-Ferrand, France. Tel.: +33 4 73 17 73 13; fax: +33 4 73 17 73 06.
  • ,
  • Philippe Luccarini

      Affiliations

    • Inserm U929, Neurobiologie de la douleur trigéminale, Faculté de Chirurgie Dentaire, 11 boulevard Charles de Gaulle, F-63000 Clermont-Ferrand, France
    • Univ Clermont1, Clermont-Ferrand F-63000, France

Received 13 October 2008 ,Revised 8 January 2009 ,Accepted 13 January 2009.

References 

  1. Bernard JF, Besson JM. The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol. 1990;63:473–490
  2. Bernard JF, Bester H, Besson JM. Involvement of the spino-parabrachio-amygdaloid and -hypothalamic pathways in the autonomic and affective emotional aspects of pain. Prog Brain Res. 1996;107:243–255
  3. Bernard JF, Dallel R, Raboisson P, Villanueva L, Le Bars D. Organization of the efferent projections from the spinal cervical enlargement to the parabrachial area and periaqueductal gray: a PHA-L study in the rat. J Comp Neurol. 1995;353:480–505
  4. Bester H, Chapman V, Besson JM, Bernard JF. Physiological properties of the lamina I spinoparabrachial neurons in the rat. J Neurophysiol. 2000;83:2239–2259
  5. Bester H, De Felipe C, Hunt SP. The NK1 receptor is essential for the full expression of noxious inhibitory controls in the mouse. J Neurosci. 2001;21:1039–1046
  6. Bester H, Matsumoto N, Besson JM, Bernard JF. Further evidence for the involvement of the spinoparabrachial pathway in nociceptive processes: a c-Fos study in the rat. J Comp Neurol. 1997;383:439–458
  7. Bouhassira D, Bing Z, Le Bars D. Studies of the brain structures involved in diffuse noxious inhibitory controls: the mesencephalon. J Neurophysiol. 1990;64:1712–1723
  8. Bouhassira D, Villanueva L, Bing Z, Le Bars D. Involvement of the subnucleus reticularis dorsalis in diffuse noxious inhibitory controls in the rat. Brain Res. 1992;595:353–357
  9. Brown JL, Liu H, Maggio JE, Vigna SR, Mantyh PW, Basbaum AI. Morphological characterization of substance P receptor-immunoreactive neurons in the rat spinal cord and trigeminal nucleus caudalis. J Comp Neurol. 1995;356:327–344
  10. Callera JC, Oliveira LB, Barbosa SP, Colombari DS, De Luca LA, Menani JV. GABA(A) receptor activation in the lateral parabrachial nucleus induces water and hypertonic NaCl intake. Neuroscience. 2005;134:725–735
  11. Chapman V, Dickenson AH. The effect of intrathecal administration of RP67580, a potent neurokinin 1 antagonist on nociceptive transmission in the rat spinal cord. Neurosci Lett. 1993;157:149–152
  12. Chiang CY, Hu B, Hu JW, Dostrovsky JO, Sessle BJ. Central sensitization of nociceptive neurons in trigeminal subnucleus oralis depends on integrity of subnucleus caudalis. J Neurophysiol. 2002;88:256–264
  13. Coste J, Voisin DL, Luccarini P, Dallel R. A role for wind-up in trigeminal sensory processing: intensity coding of nociceptive stimuli in the rat. Cephalalgia. 2008;28:631–639
  14. Coste J, Voisin DL, Miraucourt LS, Dallel R, Luccarini P. Dorsal horn NK1-expressing neurons control windup of downstream trigeminal nociceptive neurons. Pain. 2008;137:340–351
  15. Coudoré-Civiale M, Courteix C, Boucher M, Fialip J, Eschalier A. Evidence for an involvement of tachykinins in allodynia in streptozocin-induced diabetic rats. Eur J Pharmacol. 2000;401:47–53
  16. Coudoré-Civiale MA, Courteix C, Eschalier A, Fialip J. Effect of tachykinin receptor antagonists in experimental neuropathic pain. Eur J Pharmacol. 1998;361:175–184
  17. Dallel R, Duale C, Luccarini P, Molat JL. Stimulus-function, wind-up and modulation by diffuse noxious inhibitory controls of responses of convergent neurons of the spinal trigeminal nucleus oralis. Eur J Neurosci. 1999;11:31–40
  18. Dallel R, Dualé C, Molat JL. Morphine administered in the substantia gelatinosa of the spinal trigeminal nucleus caudalis inhibits nociceptive activities in the spinal trigeminal nucleus oralis. J Neurosci. 1998;18:3529–3536
  19. Dallel R, Luccarini P, Molat JL, Woda A. Effects of systemic morphine on the activity of convergent neurons of spinal trigeminal nucleus oralis in the rat. Eur J Pharmacol. 1996;314:19–25
  20. Dickenson AH, Le Bars D, Besson JM. Diffuse noxious inhibitory controls (DNIC) effects on trigeminal nucleus caudalis neurones in the rat. Brain Res. 1980;200:293–305
  21. Ding YQ, Takada M, Shigemoto R, Mizumo N. Spinoparabrachial tract neurons showing substance P receptor-like immunoreactivity in the lumbar spinal cord of the rat. Brain Res. 1995;674:336–340
  22. Dubner R, Bennett GJ. Spinal and trigeminal mechanisms of nociception. Annu Rev Neurosci. 1983;6:381–418
  23. Feil K, Herbert H. Topographic organization of spinal and trigeminal somatosensory pathways to the rat parabrachial and Kölliker-Fuse nuclei. J Comp Neurol. 1995;353:506–528
  24. Fields HL, Basbaum AI. Central nervous system mechanisms of pain modulation. In:  McMahon SB,  Koltzenburg M editor. Wall and Melzack’s textbook of pain. Edinburgh: Elsevier Churchill Livingstone; 2006;p. 125–158
  25. Fulwiler CE, Saper CB. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res. 1984;319:229–259
  26. Gear RW, Aley KO, Levine JD. Pain-induced analgesia mediated by mesolimbic reward circuits. J Neurosci. 1999;19:7175–7181
  27. Hermanson O, Blomqvist A. Subnuclear localization of FOS-like immunoreactivity in the parabrachial nucleus after orofacial nociceptive stimulation of the awake rat. J Comp Neurol. 1997;387:114–123
  28. Hirata H, Okamoto K, Tashiro A, Bereiter DA. Novel class of neurons at the trigeminal subnucleus interpolaris/caudalis transition region monitors ocular surface fluid status and modulates tear production. J Neurosci. 2004;24:4224–4232
  29. Hu JW, Sessle BJ, Raboisson P, Dallel R, Woda A. Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brain-stem neurones. Pain. 1992;48:53–60
  30. Hu JW, Woda A, Sessle BJ. Effects of pre-emptive local anaesthesia on tooth pulp deafferentation-induced neuroplastic changes in cat trigeminal brainstem neurones. Arch Oral Biol. 1999;44:287–293
  31. Hu JW. Response properties of nociceptive and non-nociceptive neurons in the rat’s trigeminal subnucleus caudalis (medullary dorsal horn) related to cutaneous and deep craniofacial afferent stimulation and modulation by diffuse noxious inhibitory controls. Pain. 1990;41:331–345
  32. Hua XY, Chen P, Marsala M, Yaksh TL. Intrathecal substance P-induced thermal hyperalgesia and spinal release of prostaglandin E2 and amino acids. Neuroscience. 1999;89:525–534
  33. Hunt SP, Mantyh PW. The molecular dynamics of pain control. Nat Rev Neurosci. 2001;2:83–91
  34. Khasabov SG, Ghilardi JR, Mantyh PW, Simone DA. Spinal neurons that express NK-1 receptors modulate descending controls that project through the dorsolateral funiculus. J Neurophysiol. 2005;93:998–1006
  35. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci. 2002;22:9086–9098
  36. Lantéri-Minet M, Weil-Fugazza J, de Pommery J, Menétrey D. Hindbrain structures involved in pain processing as revealed by the expression of c-Fos and other immediate early gene proteins. Neuroscience. 1994;58:287–298
  37. Le Bars D. The whole body receptive field of dorsal horn multireceptive neurones. Brain Res Brain Res Rev. 2002;40:29–44
  38. Li JL, Wang D, Kaneko T, Shigemoto R, Nomura S, Mizuno N. The relationship between neurokinin-1 receptor and substance P in the medullary dorsal horn: a light and electron microscopic immunohistochemical study in the rat. Neurosci Res. 2000;36:327–334
  39. Li YQ, Li H, Kaneko T, Mizuno N. Substantia gelatinosa neurons in the medullary dorsal horn: an intracellular labeling study in the rat. J Comp Neurol. 1999;411:399–412
  40. Light AR, Kavookjian AM. Morphology and ultrastructure of physiologically identified substantia gelatinosa (lamina II) neurons with axons that terminate in deeper dorsal horn laminae (III–V). J Comp Neurol. 1988;267:172–189
  41. Luccarini P, Childeric A, Gaydier AM, Voisin D, Dallel R. The orofacial formalin test in the mouse: a behavioral model for studying physiology and modulation of trigeminal nociception. J Pain. 2006;7:908–914
  42. Malpeli JG. Reversible inactivation of subcortical sites by drug injection. J Neurosci Methods. 1999;86:119–128
  43. Marshall GE, Shehab SA, Spike RC, Todd AJ. Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat. Neuroscience. 1996;72:255–263
  44. Martin JH, Ghez C. Pharmacological inactivation in the analysis of the central control of movement. J Neurosci Methods. 1999;86:145–159
  45. Mendell LM. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol. 1966;16:316–332
  46. Mestre C, Pélissier T, Fialip J, Wilcox G, Eschalier A. A method to perform direct transcutaneous intrathecal injection in rats. J Pharmacol Toxicol Methods. 1994;32:197–200
  47. Millan MJ. Descending control of pain. Prog Neurobiol. 2002;6:355–474
  48. Parsons AM, Honda CN, Jia YP, Budai D, Xu XJ, Wiesenfeld-Hallin Z, et al. Spinal NK1 receptors contribute to the increased excitability of the nociceptive flexor reflex during persistent peripheral inflammation. Brain Res. 1996;739:263–275
  49. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. London: Academic Press; 1997;
  50. Raboisson P, Dallel R, Clavelou P, Sessle BJ, Woda A. Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurones in the rat. J Neurophysiol. 1995;73:496–505
  51. Raboisson P, Dallel R. The orofacial formalin test. Neurosci Biobehav Rev. 2004;28:219–226
  52. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH. Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci. 2002;5:1319–1326
  53. Takeuchi Y, Hopkins DA. Light and electron microscopic demonstration of hypothalamic projections to the parabrachial nuclei in the cat. Neurosci Lett. 1984;46:53–58
  54. Tambeli CH, Parada CA, Levine JD, Gear RW. Inhibition of tonic spinal glutamatergic activity induces antinociception in the rat. Eur J Neurosci. 2002;16:1547–1553
  55. Todd AJ, McGill MM, Shehab SA. Neurokinin 1 receptor expression by neurons in laminae I, III and IV of the rat spinal dorsal horn that project to the brainstem. Eur J Neurosci. 2000;12:689–700
  56. Villanueva L, Peschanski M, Calvino B, Le Bars D. Ascending pathways in the spinal cord involved in triggering of diffuse noxious inhibitory controls in the rat. J Neurophysiol. 1986;55:34–55
  57. Voisin DL, Doméjean-Orliaguet S, Chalus M, Dallel R, Woda A. Ascending connections from the caudal part to the oral part of the spinal trigeminal nucleus in the rat. Neuroscience. 2002;109:183–193
  58. Woda A, Blanc O, Voisin DL, Coste J, Molat JL, Luccarini P. Bidirectional modulation of windup by NMDA receptors in the rat spinal trigeminal nucleus. Eur J Neurosci. 2004;19:2009–2016
  59. Yoshida A, Chen K, Moritani M, Yabuta NH, Nagase Y, Takemura M, et al. Organization of the descending projections from the parabrachial nucleus to the trigeminal sensory nuclear complex and spinal dorsal horn in the rat. J Comp Neurol. 1997;383:94–111

PII: S0304-3959(09)00044-X

doi: 10.1016/j.pain.2009.01.015

PAIN
Volume 142, Issue 3 , Pages 245-254 , April 2009