Mechanisms of orofacial pain control in the central nervous system

Archives of Histology and Cytology

Volumn 69, Issue 2, 2006, Pages 79-100

  Takemura, Motohide ^a   Sugiyo, Shinichi ^a   Moritani, Masayuki ^a   Kobayashi, Masayuki ^a   Yonehara, Norifumi ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SEROTONIN; SUBSTANCE P;

ANTERIOR HYPOTHALAMUS; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; CONTROL SYSTEM; FACE PAIN; INTERNEURON; MICROPHOTOGRAPHY; MORPHOLOGY; MOUTH PAIN; NERVE CELL; NOCICEPTIVE RECEPTOR; NONHUMAN; PAIN THRESHOLD; PERINATAL PERIOD; PROTEIN EXPRESSION; REVIEW; SENSORIMOTOR FUNCTION; SENSORY STIMULATION; SENSORY SYSTEM; THALAMUS; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS;

ANIMALS; CENTRAL NERVOUS SYSTEM; FACIAL PAIN; GABA MODULATORS; NOCICEPTORS; TRIGEMINAL NERVE;

EID: 33745685762     PISSN: 09149465     EISSN: 13491717     Source Type: Journal    
DOI: 10.1679/aohc.69.79     Document Type: Review

References (165)

1. Abe T, Shimoda T, Sugiyo S, Ohshita N, Takemura M: Altered effects of systemic bicuculline on intensity-dependent c-Fos expression in rats ablated with NK-1 receptor-bearing neurons in the trigeminal caudal nucleus. 34th Society for Neuroscience (Abstract 294.12) (2004).
2. Abe T, Ohshita N, Sugiyo S, Moritani M, Kobayashi M, Takemura M: Elimination of NK-1 neurons in caudal nucleus reverses the effects of systemic bicuculline on c-fos expression in rat trigeminal sensory nucleus: I. High intensity electrical stimulation of the trigeminal ganglion. Neuroscience 133: 739-747 (2005).
3. Allen GV, Barbrick B, Esser MJ: Trigeminal-parabrachial connections: possible pathway for nociception-induced cardiovascular reflex responses. Brain Res 715:125-135 (1996).
4. Ambalavanar R, Moritani M, Haines A, Hilton T, Dessem D: Chemical phenotypes of muscle and cutaneous afferent neurons in the rat trigeminal ganglion. J Comp Neurol 460: 167-179 (2003).
5. Arvidsson J, Gobel S: An HRP study of the central projections of primary trigeminal neurons which innervate tooth pulps in the cat. Brain Res 210: 1-16 (1981).
6. Åström KE: On the central course of afferent fibers in the trigeminal, facial, glossopharyngeal and vagal nerves and their nuclei in the mouse. Acta Physiol Scand 29 (Suppl 106): 209-320 (1953).
7. Azerad J, Woda A, Albe-Fessard D: Physiological properties of neurons in different parts of the cat trigeminal sensory complex. Brain Res 246: 7-21 (1982).
8. Bae YC, Choi BJ, Lee MG, Lee HJ, Park KP, Zhang LF, Honma S, Fukami H, Yoshida A, Ottersen OP, Shigenaga Y: Quantitative ultrastructural analysis of glycine- and γ -aminobutyric acid-immunoreactive terminals on trigeminal α - and γ-motoneuron somata in the rat. J Comp Neurol 442: 308-319 (2002).
9. Bae YC, Oh JM, Hwang SJ, Shigenaga Y, Valtschanoff JG: Expression of vanilloid receptor TRPV1 in the rat trigeminal sensory nuclei. J Comp Neurol 478: 62-71 (2004).
10. Barbut D, Polak JM, Wall PD: Substance P in spinal cord dorsal horn decreases following peripheral nerve injury. Brain Res 205: 289-298 (1981).
11. Barr GA, Paredes W, Erickson K, Zukin RS: Kappa opioid receptor-mediated analgesia in the developing rat. Dev Brain Res 29: 145-152 (1986).
12. Basbaum AI, Glazer EJ, Oertel W: Immunoreactive glutamic acid decarboxylase in the trigeminal nucleus caudalis of the cat: a light and electron-microscopic analysis. Somatosens Res 4: 77-94 (1986).
13. Bayers SA: Neurogenesis in the rat neostriatum. Int J Dev Neurosci 2: 163-175 (1984).
14. Bereiter DA, Bereiter DF: NMDA and non-NMDA receptor antagonism reduces Fos-like immunoreactivity in central trigeminal neurons after corneal stimulation in the rat. Neuroscience 73: 249-258 (1996).
15. Bowery NG, Brown DA: Depolarizing actions of γ-aminobutyric acid and related compounds on rat superior cervical ganglia in vitro. Br J Pharmac 50: 205-218 (1974).
16. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH: Nitric Oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7: 615-624 (1991).
17. Buritova J, Chapman V, Honore P, Besson JM: The contribution of GABAB receptor-mediated events to inflammatory pain processing: carrageenan oedema and associated spinal c-Fos expression in the rat. Neuroscience 73: 487-496 (1996).
18. A receptors: evidence for peripheral primary afferent depolarization. Neuroscience 93: 713-722 (1999).
19. Carstens E, Saxe I, Ralph R: Brainstem neurons expressing c-Fos immunoreactivity following irritant chemical stimulation of the rat's tongue. Neuroscience 69: 939-953 (1995).
20. Casale EJ, Light AR, Rustioni A: Direct projection of the corticospinal tract to the superficial laminae of the spinal cord in the rat. J Comp Neurol 278: 275-286 (1988).
21. Castro AR, Bowery N, Castro-Lopes JM: Baclofen and midazolam alter c-fos induction by peripheral noxious or innocuous stimulation in the spinal cord of normal and monoarthritic rats. Neuropharmacology 38: 1775-1788 (1999).
22. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D: A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441 (1999).
23. Caudle RM, Isaac L: A novel interaction between dynorphin (1-13) and N-methyl-D-aspartate. Brain Res 443: 329-332 (1988).
24. Chapman V, Buritova J, Honore P, Besson JM: 7-Nitro-indazole, a selective inhibitor of neuronal nitric oxide synthase, reduces formalin evoked c-Fos expression in dorsal horn neurons of the rat spinal cord. Brain Res 697: 258-261 (1995).
25. Chapman V, Besson JM: Pharmacological studies of nociceptive systems using the c-Fos immunohistochemical technique: an indicator of noxiously activated spinal neurones. In: The pharmacology of pain (Dickenson A, Besson JM, ed), Springer, Berlin, 1997 (p. 235-279).
26. Chiang CY, Hu JW, Sessle BJ: Parabrachial area and nucleus raphe magnus- induced modulation of nociceptive and nonnociceptive trigeminal subnucleus caudalis neurons activated by cutaneous or deep inputs. J Neurophysiol 71: 2430-2445 (1994).
27. Chiang CY, Kwan CL, Hu JW, Sessle BJ: Effects of GABA receptor antagonist on trigeminal caudalis nociceptive neurons in normal and neonatally capsaicin-treated rats. J Neurophysiol 82: 2154-2162 (1999).
28. Craig AD: Pain mechanisms: labeled lines versus convergence in central processing. Annu Rev Neurosci 26: 1-30 (2003).
29. Dallel R, Clavelou P, Woda A: Effects of tractotomy on nociceptive reactions induced by tooth pulp stimulation in the rat. Exp Neurol 106: 78-84 (1989).
30. 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 18: 3529-3536 (1998).
31. DiFiglia M, Aronin N: Synaptic interactions between GABAergic neurons and trigeminothalamic cells in the rat trigeminal nucleus caudalis. Synapse 6: 358-363 (1990).
32. Dubner R, Ruda MA: Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15: 96-103 (1992).
33. Dubuisson D, Dennis SG: The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 4: 161-174 (1977).
34. Eisenman J, Langren S, Novin D: Functional organization in the main sensory trigeminal nucleus and in the rostral subdivision of the nucleus of the spinal trigeminal tract in the cat. Acta Physiol Scand 59: 1-44 (1963).
35. Falls WM, Rice RE, Vanwagner JP: The dorsomedial portion of trigeminal nucleus oralis (Vo) in the rat: cytology and projections to the cerebellum. Somatosens Res 3: 89-118 (1985).
36. Fay R, Kubin L: Pontomedullary distribution of 5-HT2A receptor-like protein in the rat. J Comp Neurol 418: 323-345 (2000).
37. Fields HL, Basbaum AI: Brainstem control of spinal pain transmission. Ann Rev Physiol 40: 217-248 (1978).
38. Fields HL, Heinricher MM, Mason P: Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 14: 219-245 (1991).
39. Fried K, Arvidsson J, Robertson B, Brodin E, Theodorsson: Combined retrograde tracing and enzyme/immunohistochemistry of trigeminal ganglion cell bodies innervating tooth pulps in the rat. Neuroscience 33: 101-109 (1989).
40. Fromm GH, Terrence CF, Chattha AS: Baclofen is the treatment of trigeminal neuralgia: double blind study and long-term follow-up. Ann Neurol 15: 240-244 (1984).
41. B antagonists in the trigeminal nucleus of the rat. Neuropharmacology 31: 475-480 (1992).
42. Fukushima T, Kerr FWL: Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections. J Comp Neurol 183: 169-184 (1979).
43. Gilbert SD, Clark TM, Flores CM: Antihyperalgesic activity of epibatidine in the formalin model of facial pain. Pain 89: 159-465 (2001).
44. Ginestal E, Matute C: Gamma-aminobutyric acid-immunoreactive neurons, in the rat trigeminal nuclei. Histochemistry 99: 49-55 (1993).
45. Gobel S, Purvis MB: Anatomical studies of the organization of the spinal V nucleus: the deep bundles and the spinal V tract. Brain Res 48: 27-44 (1972).
46. Gojyo F, Sugiyo S, Kuroda R, Kawabata A, Varathan V, Shigenaga Y, Takemura M: Effects of somatosensory cortical stimulation on expression of c-Fos in rat medullary dorsal horn in response to formalin-induced noxious stimulation. J Neurosci Res 68: 479-488 (2002).
47. González-Hernández T, Conde-Send'n M, González- González B, Montolán-Sarmiento B, Pérez-González H, Meyer G: Postnatal development of NADPH-diaphorase activity in the superior colliculus and the ventral lateral geniculate nucleus of the rat. Dev Brain Res 76: 141-145 (1993).
48. Hammond DL: Inhibitory neurotransmitters and nociception: role of GABA and glycine. In: The pharmacology of pain (Dickenson A, Besson JM, ed), Springer, Berlin, 1997 (p. 361-383).
49. Harper AA, Lawson SN: Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol (Lond) 359: 31-46 (1985).
50. 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 356: 444-456 (1995).
51. He Y-F, Ichikawa H, Sugimoto T: The effect of neonatal capsaicin on the c-Fos-like immunoreactivity induced in subnucleus oralis neurons by noxious intraoral stimulation. Brain Res 860: 203-207 (2000).
52. Henry MA, Westrum LE: Central representation of dental structures in the kitten, including projections to the mesencephalic trigeminal nucleus. Somatosens Mot Res 7: 447-462 (1990).
53. Hökfelt T, Zhang X, Xu Z-Q, Ru-Rong J, Shi T, Corness J, Kerekes N, Landry M, Rydh-Rinder M, Broberger C, Wiesenfeld-Hallin Z, Bartfai T, Elde R, Ju G: Cellular and synaptic mechanisms in transition of pain from acute to chronic. In: Proceedings of the 8th World Congress on Pain (Jensen TS ed), IASP Press, Seattle, WA, 1997 (p.133-153).
54. Hou WY, Shyu BC, Chen TM, Lee JW, Shieh JY, Sun WZ: Intrathecally administrated c-fos antisense oligodeoxynucleotide decreases formalin-induced nociceptive behavior in adult rats. Eur J Pharmacol 329: 17-26 (1997).
55. 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 52: 39-53 (1984).
56. Hunter JC, Woodburn VL, Durieux C, Pettersson EKE, Poat JA, Hughes J: c-fos antisense oligodeoxynucleotide increases formalin-induced nociception and regulates preprodynorphin expression. Neuroscience 65: 485-492 (1995).
57. Hwang JH, Yaksh TL: The effect of spinal GABA receptor agonists on tactile allodynia in a surgically-induced neuropathic pain model in the rat. Pain 70: 5-22 (1997).
58. Hylden JL, Nahin RL, Traub RJ, Dubner R: Effects of spinal kappa-opioid receptors agonists on the resposiveness of nociceptive superficial dorsal horn neurons. Pain 44: 187-193 (1991).
59. Ichikawa H, Sugimoto T: Vanilloid receptor 1-like receptor-immunoreactive primary sensory neurons in the rat trigeminal nervous system. Neuroscience 101: 719-725 (2000).
60. Ichikawa H, Sugimoto T: VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res 890: 184-188 (2001).
61. Ichikawa H, Deguchi T, Nakago T, Jacobowitz DM, Sugimoto T: Parvalbumin- and calretinin-immunoreactive trigeminal neurons innervating the rat molar tooth pulp. Brain Res 679: 205-211 (1995).
62. Ichikawa H, Deguchi T, Fujiyoshi Y, Nakago T, Jacobowitz DM, Sugimoto T: Calbindin D28k-immunoreactivity in the trigeminal ganglion neurons and molar tooth pulp of the rat. Brain Res 715: 71-78 (1996).
63. + channel in the rat molar tooth pulp. Brain Res 1065: 138-141 (2005).
64. Iliakis B, Anderson NI, Irish PS, Henry MA, Westrum LE: Electron microscopy of immunoreactivity patterns for glutamate and γ-aminobutyric acid in synaptic glomeruli of the feline trigeminal nucleus (subnucleus caudalis). J Comp Neurol 366: 465-477 (1996).
65. Ishidori H, Nishimori T, Shigenaga Y, Suemune S, Dateoka Y, Sera M, Nagasaka N: Representation of upper and lower primary teeth in the trigeminal sensory nuclear complex in the young dog. Brain Res 370: 153-158 (1986).
66. Iwase K, Takemura M, Shimada T, Wakisaka S, Nokubi T, Shigenaga Y: Ontogeny of NADPH-diaphorase in rat forebrain and midbrain. Anat Embryol 197: 229-247 (1998).
67. Jacquin MF, Semba K, Egger MD, Rhoades RW: Organization of HRP-labeled trigeminal mandibular primary afferent neurons in the rat. J Comp Neurol 215: 397-420 (1983).
68. A receptors in the spinal cord limits the second but not the first phase response to formalin in the rat. In: Proceedings of the 8th World Congress on Pain, Progress in Pain Research and Management, Vol. 8 (Jensen TS, Turner JA, Wiesenfeld-Hallin Z, ed), IASP Press, Seattle, 1997a (p. 313-322).
69. A receptors in formalin-induced nociception in the rat. J Pharmac Expl Ther 282: 928-938 (1997b).
70. Kangrga I, Jiang M, Randic M: Actions of (-)-baclofen on rat dorsal horn neurons. Brain Res 562: 265-275 (1991).
71. Keay KA, Feil K, Gordon BD, Herbert H, Bandler R: Spinal afferents to functionally distinct periaqueductal gray columns in the rat: an anterograde and retrograde tracing study. J Comp Neurol 385: 207-229 (1997).
72. Khayyat GF, Yu YJ, King RB: Response patterns to noxious and non-noxious stimuli in rostral trigeminal relay nuclei. Brain Res 97: 47-60 (1975).
73. Koerber HR, Brown PB: Somatotopic organization of hindlimb cutaneous nerve projections to cat dorsal horn. J Neurophysiol 48: 481-489 (1982).
74. A receptor antagonists induce both descending antinociception and touch-evoked allodynia. Pain 76: 327-336 (1998).
75. Laing I, Todd AJ, Heizmann CW, Schmidt HH: Subpopulations of GABAergic neurons in laminae I-III of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin. Neuroscience 61: 123-132 (1994).
76. Lao L, Marvizon JCG: GABAA receptor facilitation of neurokinin release from primary afferent terminals in the rat spinal cord. Neuroscience 130: 1013-1027 (2005).
77. Li JL, Ding YQ, Takada M, Shigemoto R, Mizuno N: Distribution of trigeminothalamic and spinothalamic tract neurons showing substance P receptor-like immunoreactivity in the rat. Brain Res 719: 207-212 (1996).
78. Li YQ, Takada M, Kaneko T, Mizuno N: Premotor neurons for trigeminal motor nucleus neurons innervating the jaw-closing and jaw-opening muscles: differential distribution in the lower brainstem of the rat. J Comp Neurol 356: 563-579 (1995).
79. A antagonists reduce the inhibition of primate spinothalamic tract neurons produced by stimulation in periaqueductal gray. Brain Res 654: 286-302 (1994).
80. Lin Q, Peng YB, Willis WD: Role of GABA receptor subtypes in inhibition of primate spinothalamic tract neurons: difference between spinal and periaqueductal gray inhibition. J Neurophysiol 75: 109-122 (1996).
81. B receptor system. Br J Pharmac 113: 1561-1566 (1994).
82. Malcangio M, Bowery NG: GABA and its receptors in the spinal cord. Trends Pharmacol Sci 17: 457-462 (1996).
83. Mantyh PW, Hunt SP: Setting the tone: superficial dorsal horn projection neurons regulate pain sensitivity. Trends Neurosci 27: 582-584 (2004).
84. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, Wiley RG, Simone DA: Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278: 275-279 (1997).
85. Marfurt CF, Turner DF: The central projections of tooth pulp afferent neurons in the rat as determined by the transganglionic transport of horseradish peroxidase. J Comp Neurology 223: 535-547 (1984).
86. Marshall GE, Shehab SAS, Spike RC, Todd AJ: Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat. Neuroscience 72: 255-263 (1996).
87. Massardier D, Hunt PF: A direct nonopiate interaction of dynorphin-(1-13) with the N-methyl-D-aspartate (NMDA) receptor. Eur J Pharmacol 170: 125-126 (1989).
88. Millan MJ: Multiple opioid systems and pain. Pain 27: 303-347 (1986).
89. Mitsikostas DD, Sanchez-del-Rio M: Receptor systems mediating c-fos expression within trigeminal nucleus caudalis in animal models of migraine. Brain Res Rev 35: 20-35 (2001).
90. Molander C, Grant G: Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA-HRP conjugate. J Comp Neurol 237: 476-484 (1985).
91. Morris R, Southam E, Gittins SR, de Vente J, Garthwaite J: The NO-cGMP pathway in neonatal rat dorsal horn. Eur J Neurosci 6: 876-879 (1994).
92. Munekawa N, Sugiyo S, Varathan V, Fukami H, Wakisaka S, Shigenaga Y, Takemura M: NADPH-diaphorase and calcium binding proteins in the trigeminal nucleus oralis of rats. Somatosens Mot Res 19: 173-180 (2002).
93. Narhi M: The neurophysiology of the teeth. Dent Clin North Am 34: 439-448 (1990).
94. Noguchi K, Kowalski K, Traub R, Solodkin A, Iadarola MJ, Ruda MA: Dynorphin expression and Fos-like immunoreactivity following inflammation induced hyperalgesia are colocalized in spinal cord neurons. Mol Brain Res 10: 227-233 (1991).
95. Noguchi K, Kawai Y, Fukuoka T, Senba E, Miki K: Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. . J Neurosci 15: 7633-7643 (1995).
96. Nomura H, Ogawa A, Tashiro A, Morimoto T, Hu JW, Iwata K: Induction of Fos protein-like immunoreactivity in the trigeminal spinal nucleus caudalis and upper cervical cord following noxious and nonnoxious mechanical stimulation of the whisker pad of the rat with an inferior alveolar nerve transection. Pain 95: 225-238 (2002).
97. Nunnemacher RF, Sutherland RM: Fibers in the rat's eighth thoracic nerve. Am Zool 9: 1150 (1969).
98. Olave MJ, Maxwell DJ: Neurokinin-1 projection cells in the rat dorsal horn receive synaptic contacts from axons that possess α 2c-adrenergic receptors. J Neurosci 23: 6846-6837 (2003).
99. Pajot J, Pelissier T, Sierralta F, Raboisson P, Dallel R: Differential effects of trigeminal tractotomy on Adelta-and C-fiber-mediated nociceptive responses. Brain Res 863: 289-292 (2000).
100. Palmer RM, Ferriage AG, Moncada S: Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327: 524-526 (1987).
101. Panneton WM, Burton H: Corneal and periocular representation within the trigeminal sensory complex in the cat studied with transganglionic transport of horseradish peroxidase. J Comp Neurol 199: 327-344 (1981).
102. B receptors present on primary afferent terminals of the spinal cord? Nature 307: 71-74 (1984).
103. Reinis S, Goldman JM: Prenatal and postnatal development of brain function. In: The development of the brain. Biological and functional perspectives. Charles C. Thomas Publisher, Springfield, Illinois, 1980 (p. 223-235).
104. Ren K, Dubner R: Central nervous system plasticity and persistent pain. J Orofac Pain 13: 155-171 (1999).
105. Ren K, Dubner R: Descending modulation in persistent pain: an update. Pain 100: 1-6 (2002).
106. A receptor activation. Neuroscience 103: 725-737 (2001).
107. 3H]serotonin. Brain Res 184: 57-83 (1980).
108. A receptors in the midbrain periaqueductal gray abolishes nociceptive specific dorsal horn neuronal activity. Eur J Pharmac 160: 163-166 (1989).
109. Sawynok J: GABAergic mechanisms of analgesia: An update. Pharmac Biochem Behav 26: 463-474 (1987).
110. Shigenaga Y, Okamoto T, Nishimori T, Suemune S, Nasution ID, Chen IC, Tsura K, Yoshida A, Tabuchi K, Hosoi M, Tsura H: Oral and facial representation in the trigeminal principal and rostral spinal nuclei of the cat. J Comp Neurol 244: 1-18 (1986a).
111. Shigenaga Y, Suemune S, Nishimura M, Nishimori T, Sato H, Ishidori H, Yoshida A, Tsuru K, Tsuiki Y, Dateoka Y, Nasution ID, Hosoi M: Topographic representation of lower and upper teeth within the trigeminal sensory nuclei of adult cat demonstrated by the transganglionic transport of horseradish peroxidase. J Comp Neurol 251: 299-316 (1986b).
112. Shigenaga Y, Nishimura M, Suemune S, Nishimori T, Doe K, Tsuru H: Somatotopic organization of tooth pulp primary afferent neurons in the cat. Brain Res 477: 66-89 (1989).
113. Shimoda T, Abe T, Ohshita N, Sugiyo S, Ishigaki S, Takemura M: Aberrant c-Fos induction in the trigeminal principal, oral, and interpolar nuclei after electrical stimulation of the trigeminal ganglion in nerve transected rat. 34th Society for Neuroscience (Abstract 294.10) (2004)
114. Shukla VK, LeMaire S: Non-opioid effects of dynorphins: possible role of the NMDA receptor. Trends Pharmacol Sci 15: 420-424 (1994).
115. Silverman JD, Kruger L: An interpretation of dental innervation based upon the pattern of calcitonin gene-related peptide (CGRP)-immunoreactive thin sensory axons. Somatosens Res 5: 157-175 (1987).
116. Sivilotti L, Woolf CL: The contribution of GABA-A and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J Neurophysiol 72: 169-179 (1994).
117. Steer JM: Some observations on the fine structure of rat dorsal spinal nerve roots. J Anat 109: 467-485 (1971).
118. Stoyanova II: Gamma-aminobutiric acid immunostaining in trigeminal, nodose and spinal ganglia of the cat. Acta Histochem 106: 309-314 (2004).
119. Strassman AM, Vos BP: Somatotopic and laminar organization of Fos-like immunoreactivity in the medullary and upper dorsal horn induced by noxious facial stimulation in the rat. J Comp Neurol 331: 495-516 (1993).
120. Sugimoto T, Takemura M: Tooth pulp primary neurons : cell size analysis central connection and carbonic anhydrase activity. Brain Res Bull 30: 221-226 (1993).
121. Sugimoto T, Takemura M, Sakai A, Ishimaru M: Cell size analysis of trigeminal primary afferent neurons comprizing individual peripheral branches of the rat mandibular nerve. Exp Neurol 93: 565-573 (1986).
122. Sugimoto T, Takemura M, Wakisaka S: Cell size analysis of primary neurons innervating the cornea and tooth pulp of the rat. Pain 32: 375-381 (1988).
123. Sugimoto T, Wakisaka S, Takemura M, Aoki M: Cell size and Nissl pattern analyses of primary afferent neurons innervating the molar tooth pulp and cornea of the rat. In: Processing of sensory information in the superficial dorsal horn of the spinal cord (Cervero F, Bennett GJ, Headley PM, ed), Plenum Publishing Corp, New York 1989 (p. 95-98).
124. Sugimoto T, Takemura M, Mukai N: Histochemical demonstration of neural carbonic anhydrase activity within the mandibular molar and incisor tooth pulps of the rat. Brain Res. 529: 245-254 (1990a).
125. Sugimoto T, Takemura, M, Wakisaka S, Akai M: Carbonic anhydrase activity in the trigeminal primary afferent neuronal cell bodies with peripheral axons innervating the mandibular molar tooth pulps of the rat. Brain Res 505: 354-357 (1990b).
126. Sugimoto T, Ichikawa H, Hijiya H, Mitani S, Nakago T: c-Fos expression by dorsal horn neurons chronically deafferented by peripheral nerve section in response to spared, somatotopically inappropriate nociceptive primary input. Brain Res 621: 161-166 (1993).
127. Sugimoto T, Hara T, Shirai H, Abe T, Ichikawa H, Sato T: c-Fos induction in the subnucleus caudalis following noxious mechanical stimulation of the oral mucous membrane. Exp Neurol 129: 251-256 (1994).
128. Sugimoto T, Yoshida A, Nishijima K, Ichikawa H: c-Fos induction in the rat spinal dorsal horn partially deafferented by dorsal rhizotomy. Neurosci Lett 178: 239-242 (1994).
129. Sugimoto T, Fujiyoshi Y, He Y-F, Xiao C, Ichikawa H: Trigeminal primary projection to the rat brain stem sensory trigeminal nuclear complex and surrounding structures revealed by anterograde transport of cholera toxin B subunit-conjugated and Bandeiraea simplicifolia isolectin B4-conjugated horseradish peroxidase. Neurosci Res 28: 361-371 (1997a).
130. Sugimoto T, Fujiyoshi Y, Xiao C, He Y-F, Ichikawa H: Central projection of calcitonin gene-related peptide (CGRP)- and Substance P (SP)-immunoreactive trigeminal primary neurons in the rat. J Comp Neurol 378: 425-442 (1997b).
131. Sugimoto T, He Y-F, Funahashi M, Ichikawa H: Induction of immediate-early genes c-fos and zif268 in the subnucleus oralis by noxious tooth pulp stimulation. Brain Res 794: 353-8 (1998a).
132. Sugimoto T, He Y-F, Xiao C, Ichikawa H: c-fos induction in the subnucleus oralis following trigeminal nerve stimulation. Brain Res 783: 158-62 (1998b).
133. Sugiyo S, Yonehara N, Appenteng K, Nokubi T, Shigenaga Y, Takemura M: Effects of intrathecal c-fos antisense olidodeoxynucleotide on adjuvant-induced thermal hyperalgesia. Exp Brain Res 140: 198-205 (2001).
134. Sugiyo S, Satoh F, Asakura D, Kim DW, Abe T, Moritani M, Ohshita N, Yoshida A, Nakatsuka M, Iwai Y, Takemura M: Difference in pain related behavior and c-Fos expression between intra-oral and facial region after formalin injection. 34th Society for Neuroscience (Abstract 293.15) (2004).
135. Sugiyo S, Takemura M, Dubner R, Ren K: Trigeminal transition zone-rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol 493: 510-523 (2005).
136. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH: Superficial NK-1-expressing neurons control spinal excitability through activation of descending pathways. Nature Neurosci 5: 1319-1326 (2002).
137. Szabat E, Soinila S, Happola O, Linnala A, Virtanen I: A new monoclonal antibody against the GABA-protein conjugate shows immunoreactivity in sensory neurons of the rat. Neuroscience 47: 409-420 (1992)
138. B receptor inhibits the excitability of rat small diameter trigeminal root ganglion neurons. Neuroscience 123: 491-505 (2004).
139. Takemura M, Sugimoto T, Sakai A: Topographic organization of central terminal region of different sensory branches of the rat mandibular nerve. Exp Neurol 96: 540-557 (1987).
140. Takemura M, Sugimoto T, Shigenaga Y: Difference in central projection of primary afferents innervating facial and intraoral structures in the rat. Exp Neurol 111: 324-331 (1991).
141. Takemura M, Nagase Y, Yoshida A, Yasuda K, Kitamura S, Shigenaga Y, Matano S: The central projection of the monkey tooth pulp afferent neurons. Somatosens Mot Res 10: 217-227 (1993).
142. Takemura M, Wakisaka S, Yoshida A, Nagase Y, Bae YC, Shigenaga Y: NADPH-diaphorase in the spinal trigeminal nucleus oralis and rostral solitary tract nucleus of rats. Neuroscience 61: 587-595 (1994).
143. Takemura M, Wakisaka S, Iwase K, Yabuta NH, Nakagawa S, Chen K, Bae YC, Yoshida A, Shigenaga Y: NADPH-diaphorase in the developing rat: Lower brainstem and cervical spinal cord with special reference to the trigemino-solitary complex. J Comp Neurol 365: 511-525 (1996).
144. Takemura M, Tsujio A, Iwase K, Shimada T, Shigenaga Y: Central terminals of orofacial primary afferents and NADPH-diaphorase activity in the trigemino-solitary complex of rats. Brain Res 781: 78-90 (1998).
145. A receptor-mediated effects on expression of c-Fos in rat trigeminal nucleus following high- and low-intensity afferent stimulation. Neuroscience 98: 325-332 (2000a).
146. Takemura M, Shimada T, Sugiyo S, Nokubi T, Shigenaga Y: Mapping of c-Fos in the trigeminal sensory nucleus following high- and low-intensity afferent stimulation in the rat. Exp Brain Res 130: 113-123 (2000b).
147. B receptor-mediated effects on expression of c-Fos in rat trigeminal nucleus following high- and low-intensity afferent stimulation. Neuroscience 103: 1051-1058 (2001).
148. Todd AJ, Spike RC, Brodbelt AR, Price RF, Shehab SA: Some inhibitory neurons in the spinal cord develop c-fos-immunoreactivity after noxious stimulation. Neuroscience 63: 805-816 (1994).
149. Todd AJ, Watt C, Spike RC, Sieghart W: Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci 16: 974-982 (1996).
150. 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 12: 689-700 (2000).
151. Todd AJ, Puskár Z, Spike RC, Hughes C, Watt C, Forrest L: Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance P-containing afferents and respond to noxious stimulation. J Neurosci 22: 4103-4113 (2002).
152. Torvik A: Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures. J Comp Neurol 106: 51-141 (1956).
153. Tsuboi Y, Takeda M, Tanimoto T, Ikeda M, Matsumoto S, Kitagawa J, Teramoto K, Simizu K, Yamazaki Y, Shima A, Ren K, Iwata K: Alteration of the second branch of the trigeminal nerve activity following inferior alveolar nerve transection in rats. Pain 111: 323-334 (2004).
154. Turner DF, Marfurt CF: Uptake and transneuronal transport of horseradish peroxidase-wheat germ agglutinin by tooth pulp primary afferent neurons. Brain Res 452: 381-387 (1988).
155. Uhl GR, Takemura M: Gene mechanisms in primary afferent proenkephalin regulation in nucleus caudalis. In: Processing and inhibition of nociceptive information (Inoki R, Shigenaga Y, Tohyama M, ed), Elsevier Science Publishers, Amsterdam, the Netherlands, 1992 (p. 103-108).
156. Urban MO, Gebhart GF: Supraspinal contributions to hyperalgesia. Proc Natl Acad Sci USA 96: 7687-7692 (1999).
157. Vanderah TW, Laughlin T, Lashbrook JM, Nichols ML, Wilcox GL, Ossipov MH, Malan TP Jr, Porreca F: Single intrathecal injections of dynorphin A or des-Tyr-dynorphins produce long-lasting allodynia in rats: blockade by MK-801 but not naloxone. Pain 68: 275-281 (1996).
158. Wakisaka S, Nishikawa S, Ichikawa H, Matsuo S, Takano Y, Akai M: The distribution and origin of substance P-like immunoreactivity in the rat molar pulp and periodontal tissues. Arch Oral Biol 30: 813-818 (1985).
159. Walther D, Takemura M, Uhl GR: Fos family member changes in nucleus caudalis neurons after primary afferent stimulation: enhancement of fos B and c-fos. Mol Brain Res 17: 155-159 (1993).
160. Westrum LE, Canfield RC, O'Connor TA: Projections from dental structures to the brain stem trigeminal complex as shown by transganglionic transport of horseradish peroxidase. Neurosci Lett 20: 31-36 (1980).
161. Westrum LE, Canfield RC, O'Connor TA: Each canine tooth projects to all brain stem trigeminal nuclei in cat. Exp Neurol 74: 787-799 (1981).
162. Yasui Y, Itoh K, Mizuno N, Nomura S, Takada M, Konishi A, Kudo M: The posteromedial ventral nucleus of the thalamus (VPM) of the cat: direct ascending projections to the cytoarchitectonic subdivisions. J Comp Neurol 220: 219-228 (1983).
163. Yonehara N, Takemura M, Yoshimura M, Iwase K, Seo HG, Taniguchi N, Shigenaga Y: Nitric oxide in the rat spinal cord in freund's adjuvant-induced hyperalgesia. Jpn J Pharmacol 75: 327-335 (1997).
164. Young RF, King RB: Fiber spectrum of the trigeminal sensory root of the baboon determined by electron microscopy. J Neurosurg 38: 65-72 (1973).
165. Young RF, Oleson TD, Perryman KM: Effect of trigeminal tractotomy on behavioral response to dental pulp stimulation in the monkey. J Neurosurg 55: 420-430 (1981).