The Journal of Pain
Volume 6, Issue 9 , Pages 569-580 , September 2005

Comparison of Fos Expression Within the Ferret’s Spinal Trigeminal Nuclear Complex Evoked by Electrical or Noxious-Thermal Pulpal Stimulation

  • Siriporn Chattipakorn

      Affiliations

    • Department of Odontology and Oral Pathology, Faculty of Dentistry, Chiang Mai University, Chiang Mai, Thailand
    • Corresponding Author InformationAddress reprint requests to Siriporn C. Chattipakorn, DDS, PhD, Department of Odontology and Oral Pathology, Faculty of Dentistry, Chiang Mai University, Chiang Mai, 50200, Thailand
  • ,
  • Nipon Chattipakorn

      Affiliations

    • Department of Cardiac Electrophysiology Research and Training Center, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
  • ,
  • Alan R. Light

      Affiliations

    • Department of Cell and Molecular Physiology, UNC-Chapel Hill, Chapel Hill, North Carolina
  • ,
  • Matti Narhi

      Affiliations

    • Institute of Dentistry, University of Turku, Turku, Finland
  • ,
  • William Maixner

      Affiliations

    • Department of Comprehensive Center for Inflammatory Disorders, UNC-Chapel Hill, Chapel Hill, North Carolina

Received 22 June 2004 ,Revised 13 February 2005 ,Accepted 15 February 2005.

References 

  1. Ahlquist ML , Franzen OG , Edwall GA , Fors UG , Haegerstam GAT . The relation between intradental nerve activity and pulpal pain after heat stimulation . Acta Physiol Scand . 1986;127;:1–7
  2. Arvidsson J , Gobel S . An HRP study of the central projections of primary trigeminal neurons which innervate tooth pulps in the cat . Brain Res . 1981;210;:1–16
  3. Bereiter DA , Benetti AP . Excitatory amino release within spinal trigeminal nucleus after mustard oil injection into the temporomandibular joint regions of the rats . Pain . 1996;67;:451–459
  4. Bereiter DA , Plotsky PM , Gann DS . Tooth pulp stimulation potentiates the adrenocorticotropin response to hemorrhage in cats . Endocrinology . 1982;111;:1127–1132
  5. Boissonade FM , Sharkey KA , Lucier GE . Trigeminal nuclear complex of the ferret (anatomical and immunohistochemical studies) . J Comp Neurol . 1993;93;:291–312
  6. Bossut DF , Whitsel EA , Maixner W . A parametric analysis of the effects of cardiopulmonary vagal electrostimulation on the digastric reflex in cats . Brain Res . 1992;579;:253–260
  7. Bullitt E . Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat . J Comp Neurol . 1990;296;:517–530
  8. Bullitt E . Somatotopy of spinal nociceptive processing . J Comp Neurol . 1991;312;:279–290
  9. Bullitt E , Lee CL , Light AR , Willcockson H . Time course and effect of stimulus duration on noxious stimulus induced c-Fos expression in the rodent spinal cord . Brain Res . 1992;580;:172–179
  10. Byers MR . Dental sensory receptors . Int Rev Neurobiol . 1984;25;:39–93
  11. Campbell NC , Clarke RW , Matthews B . Convergent inputs to neurons responding to tooth-pulp stimulation in the trigeminal nuclei of the rostral brainstem of the minimally traumatized cat . Adv Pain Res Ther . 1985;9;:233–244
  12. Chattipakorn SC , Light AR , Narhi M , Maixner W . The effects of noxious dental heating on the jaw-opening reflex and trigeminal Fos expression in the ferret . J Pain . 2001;2;:345–353
  13. Chattipakorn SC , Light AR , Willcockson HH , Narhi M , Maixner W . The effect of fentanyl on c-fos expression in the trigeminal brainstem complex produced by pulpal heat stimulation in the ferret . Pain . 1999;82;:207–215
  14. Coimbra F , Coimbra A . Dental noxious stimulation reaches the subnucleus caudalis of the trigeminal complex in the rat, as shown by c-fos expression upon thermal or mechanical stimulation . Neurosci Lett . 1994;173;:201–204
  15. Dallel R , Raboisson P , Auroy P , Woda A . The rostral part of the trigeminal sensory complex is involved in orofacial nociception . Brain Res . 1988;448;:7–19
  16. Dong WK , Chudler EH , Kawakami Y . Tooth pulp-evoked potentials in the trigeminal brainstem nuclear complex . Brain Res . 1990;529;:131–142
  17. Dostrovsky JO , Sessle BJ , Hu JW . Presynaptic excitability changes produced in brain stem endings of tooth pulp afferents by raphe and other central and peripheral influences . Brain Res . 1981;218;:141–160
  18. Dragunow M , Faull R . The use of c-fos as a metabolic marker in neuronal pathway tracing . J Neurosci Methods . 1989;29;:261–265
  19. Dubner R . Interaction of peripheral and central input in the main sensory trigeminal nucleus of the cat . Exp Neurol . 1967;17;:186–202
  20. Dubner R . Research on pain mechanisms in animals . J Am Vet Med Assoc . 1987;191;:1273–1276
  21. Erickson JT , Millhorn DE . Fos-like protein is induced in neruons of the medulla oblongata after stimulation of the carotid sinus nerve in awake and anestheiszed rats . Brain Res . 1991;567;:11–24
  22. Gracely RH , Dubner R , McGrath P , Heft H . New methods of pain measurement and their application to pain control . Int Dent J . 1978;28;:52–65
  23. Greenwood F . An electrophysiological study of the central connections of primary afferent nerve fibres from the dental pulp of the cat . Arch Oral Biol . 1973;18;:771–785
  24. Hathaway CB , Hu JW , Bereiter DA . Distribution of Fos-like immunoreactivity in the caudal brainstem of the rat following noxious chemical stimulation of the temporomandibular joint . J Comp Neurol . 1995;356;:444–456
  25. Hu JW , Sessle BJ . Comparison of responses of cutaneous nociceptive and nonnociceptive brain stem neurons in trigeminal subnucleus caudalis (medullary dorsal horn) and subnucleus oralis to natural and electrical stimulation of tooth pulp . J Neurophysiol . 1984;52;:39–53
  26. Hunt SP , Pini A , Evan G . Induction of c-fos-like protein in spinal cord neurons following sensory stimulation . Nature . 1987;328;:632–634
  27. Jacquin MF , Semba K , Rhoades RW , Egger MD . Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vagal nuclei . Brain Res . 1982;246;:285–291
  28. Jyvasjarvi E , Kniffki KD . Cold stimulation of teeth (A comparison between the responses of cat intradental A delta and C fibres and human sensation) . J Physiol . 1987;391;:193–207
  29. Li YW , Dampney RA . Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits . Neuroscience . 1994;61;:13–634
  30. Luna LG . Routine staining procedures . In:  Luna LG editors. Manual of Histological Staining Methods . New York, NY: McGraw-Hill Book Company; 1973;p. 32–46
  31. Maixner W , Dubner R , Kenshalo DR , Bushnell MC , Oliveras JL . Responses of monkey medullary dorsal horn neurons during the detection of noxious heat stimuli . J Neurophysiol . 1989;62;:437–449
  32. Marfurt CF , Rajchert DM . Trigeminal primary afferent projections to “non-trigeminal” areas of the rat central nervous system . J Comp Neurol . 1991;303;:489–511
  33. McGrath PA , Gracely RH , Dubner R , Heft MW . Non-pain and pain sensations evoked by tooth pulp stimulation . Pain . 1983;15;:377–388
  34. Menetrey D , Gannon A , Levine JD , Basbaum AI . Expression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation . J Comp Neurol . 1989;285;:177–195
  35. Meng ID , Bereiter DA . Differential distribution of Fos-like immunoreactivity in the spinal trigeminal nucleus after noxious and innocuous thermal and chemical stimulation of rat cornea . Neuroscience . 1996;72;:243–254
  36. Meng ID , Hu JW , Benetti AP , Bereiter DA . Encoding of corneal input in two distinct regions of the spianl trigeminal nucleus in the rat (Cutaneous receptive Field properites, responses to thermal and chemical stimulation, modulation by diffuse noxious inhibitory controls and projections to parabrachial area) . J Neurophysiol . 1997;77;:43–56
  37. Meng ID , Hu JW , Bereiter DA . Differential effects of morphine on corneal-responsive neurons in rostral versus caudal regions of spinal trigeminal nucleus in the rat . J Neurophysiol . 1998;79;:2593–2602
  38. Mumford JM , Stanley SJ . Sensations on stimulating the pulps of human teeth, thresholds and tolerance ratio . Pain . 1981;10;:391–398
  39. Narhi M . Activation of dental pulp nerves of the cat and the dog with hydrostatic pressure . Proc Finn Dent Soc . 1978;74;:1–64
  40. Narhi M . The neurophysiology of the teeth . Dent Clin North Am . 1990;34;:439–448
  41. Narhi M , Haegerstam G . Intradental nerve activity induced by reduced pressure applied to exposed dentine in the cat . Acta Physiol Scand . 1983;119;:381–386
  42. Narhi M , Jyvasjarvi E , Hirvonen T , Huopaniemi T . Activation of heat-sensitive nerve fibres in the dental pulp of the cat . Pain . 1982;14;:317–326
  43. Narhi M , Jyvasjarvi E , Virtanen A , Huopaniemi T , Ngassapa D , Hirvonen T . Role of intradental A- and C-type fibers in dental pain mechanisms . Proc Finn Dent Soc . 1992;88(Suppl 1):507–516
  44. Narhi MVO . The characteristics of intradental sensory units and their responses to stimulation . J Dent Res . 1985;64;:564–571
  45. Narhi MVO , Hirvonen TJ . The response of dog intradental nerves to hypertonic solutions of CaCl2 and NaCl and other stimuli applied to exposed dentine . Arch Oral Biol . 1987;32;:781–786
  46. Narhi MVO , Hirvonen TJ , Hakumaki MOK . Responses of intradental nerve fibres to stimulation of dentine and pulp . Acta Physiol Scand . 1982;115;:173–178
  47. Nord SG . Bilateral projection of the canine tooth pulp to bulbar trigeminal neurons . Brain Res . 1976;113;:517–525
  48. Olgart L , Gazelius B , Brodin E , Nilsson G . Release of substance P-like immunoreactivity from the dental pulp . Acta Physiol Scand . 1977;101;:510–512
  49. Oliveras JL , Hosobuchi Y , Guilbaud G , Besson JM . Analgesic electrical stimulation of the feline nucleus raphe magnus (Development of tolerance and its reversal by 5-HTP) . Brain Res . 1978;146;:404–409
  50. Oliveras JL , Woda A , Guilbaud G , Besson JM . Inhibition of the jaw-opening reflex by electrical stimulation of the periaqueductal gray matter in the awake, unrestrained cat . Brain Res . 1974;72;:328–331
  51. Panopoulos P , Gazelius B , Olgart L . Responses of feline intradental sensory nerves to hyperosmotic stimulation of dentin . Acta Odontol Scand . 1983;41;:369–375
  52. Peppel P , Anton F . Responses of rat medullary dorsal horn neurons following intranasal noxious chemical stimulation (Effects of stimulus intensity, duration, and interstimulus interval) . J Neurophysiol . 1993;70;:2260–2275
  53. Pertovaara A , Huopaniemi T , Aukee K . Tooth pulp-evoked jaw-opening reflex in the cat (Evidence for central facilitation induced by noxious discharge in the intradental nerve fibers) . Exp Neurol . 1986;92;:207–219
  54. Pertovaara A , Huopaniemi T , Carlson S , Jyvasjarvi E . Response characteristics of tooth pulp-driven postsynaptic neurons in the spinal trigeminal subnucleus interpolaris of the cat (Comparison with primary afferent fiber, subnucleus caudalis, reflex, and sensory responses) . Brain Res . 1987;422;:205–217
  55. Phelan KD , Falls WM . An analysis of the cyto- and myeloarchitectonic organization of trigeminal nucleus interpolaris in the rat . Somatosens Mot Res . 1989;6;:333–366
  56. Presley RW , Menetrey D , Levine JD , Basbaum AI . Systemic morphine suppresses noxious stimulus-evoked Fos protein- like immunoreactivity in the rat spinal cord . J Neurosci . 1990;10;:323–335
  57. Sagar SM , Sharp FR , Curran T . Expression of c-fos protein in brain (Metabolic mapping at the cellular level) . Science . 1988;240;:1328–1331
  58. Sakai A , Sugimoto T , Takemura M , Sugita M . Comparative study of postnatal nerve fiber growth in the inferior alveolar nerve, sensory root of trigeminal nerve, spinal trigeminal tract and inferior incisor tooth pulp of the rat . J Osaka Univ Dent Sch . 1984;24;:41–50
  59. Sessle BJ , Hu JW , Dubner R , Lucier GE . Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). II. Modulation of responses to noxious and nonnoxious stimuli by periaqueductal gray, nucleus raphe magnus, cerebral cortex, and afferent influences, and effect of naloxone . J Neurophysiol . 1981;45;:193–207
  60. Shigenaga Y, Suemune S, Nishimura M, Nishimori T, Sato H, Ishidori H, et al. Topographic representation of lower and upper teeth within the trigeminal sensory nuclei of adult cat as demonstrated by the transganglionic transport of horseradish peroxidase . J Comp Neurol . 1986;251;:299–316
  61. Smith JC , Morrison DE , Ellenberger HH , Otto MR , Feldman JL . Brainstem projections to the major respiratory neuron populations in the medulla of the cat . J Comp Neurol . 1989;281;:69–96
  62. Virtanen ASJ . Electrical stimulation of pulp nerves-comparison of monopolar and bipolar electrode coupling . Pain . 1985;23;:279–288
  63. Willcockson HH , Taylor-Blake B , Light AR . Induction of fos-like immunoreactivity by electrocutaneous stimulation of the rat hindpaw . Somatosens Mot Res . 1995;12;:151–161
  64. Yokota T . Excitation of units in marginal rim of trigeminal subnucleus caudalis elicited by tooth pulp stimulation . Brain Res . 1975;95;:154–158

 Supported by Thailand Research Fund TRF-MRG 4680144 (S.C.), TRF-RSA4680010 (N.C.), NIDR grant DE 11661 (W.M.), and NINDS grant NS 16433 (A.R.L.).

PII: S1526-5900(05)00453-0

doi: 10.1016/j.jpain.2005.02.006

The Journal of Pain
Volume 6, Issue 9 , Pages 569-580 , September 2005