This paper reviews the recent advances in knowledge of brainstem mechanisms related to craniofacial pain. It also draws attention to their clinical implications, and concludes with a brief overview and suggestions for future research directions. It first describes the general organizational features of the trigeminal brainstem sensory nuclear complex (VBSNC), including its input and output properties and intrinsic characteristics that are commensurate with its strategic role as the major brainstem relay of many types of somatosensory information derived from the face and mouth. The VBSNC plays a crucial role in craniofacial nociceptive transmission, as evidenced by clinical, behavioral, morphological, and electrophysiological data that have been especially derived from studies of the relay of cutaneous nociceptive afferent inputs through the subnucleus caudalis of the VBSNC. The recent literature, however, indicates that some fundamental differences exist in the processing of cutaneous vs. other craniofacial nociceptive inputs to the VBSNC, and that rostral components of the VBSNC may also play important roles in some of these processes. Modulatory mechanisms are also highlighted, including the neuro-chemical substrate by which nociceptive transmission in the VBSNC can be modulated. In addition, the long-term consequences of peripheral injury and inflammation and, in particular, the neuroplastic changes that can be induced in the VBSNC are emphasized in view of the likely role that central sensitization, as well as peripheral sensitization, can play in acute and chronic pain. The recent findings also provide new insights into craniofacial pain behavior and are particularly relevant to many approaches currently in use for the management of pain and to the development of new diagnostic and therapeutic procedures aimed at manipulating peripheral inputs and central processes underlying nociceptive transmission and its control within the VBSNC.
References
1.
Allen GV, Pronych SP (1997). Trigeminal autonomic pathways involved in nociception-induced reflex cardiovascular responses. Brain Res754:269-278.
2.
Almond JR, Westrum LE, Henry MA (1996). Post-embedding immunogold labeling of gamma-aminobutyric acid in lamina II of the spinal trigeminal subnucleus pars caudalis: I. A qualitative study. Synapse24:39-47.
3.
Ambalavanar R., Morris R. (1992). The distribution of binding by isolectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat. Neuroscience47:421-429.
4.
Angus-Leppan H., Olausson B., Boers P., Lambert GA (1994). Convergence of afferents from superior sagittal sinus and tooth pulp on cells in the upper cervical spinal cord of the cat. Neurosci Lett182:275-278.
5.
Arvidsson U. Riedi M., Chakrabarti S., Lee J.-H., Nakano AH, Dado RJ, et al. (1995). Distribution and targeting of a μ-opioid receptor (MORI) in brain and spinal cord. I Neurosci15:3328-3341.
6.
Azerad J., Boucher Y., Pollin B. (1992). Occurrence of glutamate in primary sensory trigeminal neurons innervating the rat dental pulp. Comptes Rendus de l'Academie des Sciences Paris, Serie III 314:469-475.
7.
Bakke M., Hu JW, Sessle BJ (1998a). Involvement of NK-1 and NK-2 tachykinin receptor mechanisms in jaw muscle activity reflexly evoked by inflammatory irritant application to the rat temporomandibular joint. Pain75:219-227.
8.
Bakke M., Hu JW, Sessle BJ (1998b). Morphine application to peripheral tissues modulates nociceptive jaw reflex. NeuroReport9:3315-3319.
9.
Barnett EM Evans GD, Sun N., Perlman S., Cassell MD (1995). Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1. J Neurosci15:2972-2984.
10.
Bennett GJ (1994). Neuropathic pain. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 201-224.
11.
Bennett-Clarke CA, Chiaia NL (1992). Normal development and effects of neonatal infraorbital nerve damage upon the innervation of the trigeminal brainstem complex by primary afferent fibers containing calcitonin gene-related peptide. J Comp Neurol342:282-294.
12.
Bereiter DA (1997). Morphine and somatostatin analogue reduce c-fos expression in trigeminal subnucleus caudalis produced by corneal stimulation in the rat. Neuroscience77:863-874.
13.
Bereiter DA, Benetti AP (1996). Excitatory amino release within spinal trigeminal nucleus after mustard oil injection into the temporomandibular joint region of the rat. Pain67:451-459.
14.
Bereiter DA, Bereiter DF (1996). N-methyl-D-aspartate and non-N-methyl-D-aspartate receptor antagonism reduces fos-like immunoreactivity in central trigeminal neurons after corneal stimulation in the rat. Neuroscience73:249-258.
15.
Bereiter DA, Hathaway CB, Benetti AP (1994). Caudal portions of the spinal trigeminal complex are necessary for autonomic responses and display Fos-like immunoreactivity after corneal stimulation in the cat. Brain Res657:73-82.
16.
Bester H., Menendez L., Besson JM, Bernard JF (1995). Spino(trigemino)parabrachiohypothalamic pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol73:568-585.
17.
Boissonade FM, Matthews B. (1993). Responses of trigeminal brain stem neurons and the digastric muscle to tooth-pulp stimulation in awake cats. J Neurophysiol69:174-186.
18.
Bonica JJ (1983). Pain research and therapy: achievements of the past and challenges of the future. In: Advances in pain research and therapy. Vol. 5. Bonica JJ, Lindblom U, Iggo A, editors. New York: Raven Press, pp. 1-36.
19.
Broton JG, Sessle BJ (1988). Reflex excitation of masticatory muscles induced by algesic chemicals applied to the temporomandibular joint of the cat. Arch Oral Biol33:741-747.
20.
Broton JG, Hu JW, Sessle BJ (1988). Effects of temporomandibular joint stimulation on nociceptive and nonnociceptive neurons of the cat's trigeminal subnucleus caudalis (medullary dorsal horn). J Neurophysiol59:1575-1589.
21.
Brown JL, Liu H., Maggio JE, Vigna SR, Mantyh PW, Basbaum AI (1995). Morphological characterization of substance P receptor-immunoreactive neurons in the rat spinal cord and trigeminal nucleus caudalis. J Comp Neurol356:327-344.
22.
Bruce LL, McHaffie JG, Stein BE (1987) The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labeling study with fluorescent dyes. J Comp Neurol262:315-330.
23.
Burstein R., Yamamura H., Malick A., Strassman AM (1998). Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J Neurophysiol79:964-982.
24.
Cadet R., Aigouy L., Woda A. ( 1995). Enhanced nociceptive behaviour following conditioning injection of formalin in the perioral area of the rat. Brain Res676:189-195.
25.
Cairns BE, Sessle BJ, Hu JW (1998). Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J Neurosci18:8056-8064.
26.
Capra NF, Dessem D. (1992). Central connections of trigeminal primary afferent neurons: topographical and functional considerations. Crit Rev Oral Biol Med4:1-52.
27.
Carlsson GE, LeResche L. (1995). Epidemiology of temporomandibular disorders. In: Temporomandibular disorders and related pain conditions. Progress in pain research and management. Vol. 4. Sessle B), Bryant PS, Dionne RA, editors. Seattle: IASP Press, pp. 211-226.
28.
Carstens E., Saxe I., Ralph R. (1995). Brainstem neurons expressing c-fos immunoreactivity following irritant chemical stimulation of the rat's tongue. Neuroscience69:939-953.
29.
Chen L., Huang LY (1992). Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a source of modulation. Nature356:521-523.
30.
Chiang CY, Hu JW, Dostrovsky JO, Sessle BJ (1989). Changes in mechanoreceptive field properties of trigeminal somatosensory brainstem neurons induced by stimulation of nucleus raphe magnus in cats. Brain Res485:371-381.
31.
Chiang CY, Dostrovsky JO, Sessle BJ (1991). Periaqueductal gray matter and nucleus raphe magnus involvement in anterior pretectal nucleus-induced inhibition of jaw-opening reflex in rats. Brain Res544:71-78.
32.
Chiang CY, Hu JW, Sessle BJ (1994). Parabrachial area and nucleus raphe magnus-induced modulation of nociceptive and nonnociceptive trigeminal subnucleus caudalis neurons activated by cutaneous or deep inputs. J Neurophysiol71:2430-2445.
33.
Chiang CY, Hu JW, Sessle BJ (1997). NMDA receptor involvement in neuroplastic changes induced by neonatal capsaicin treatment in trigeminal nociceptive neurons. J Neurophysiol78:2799-2803.
34.
Chiang CY, Park SJ, Kwan CL, Hu JW, Sessle BJ (1998). NMDA receptor mechanisms contribute to neuroplasticity induced in caudalis nociceptive neurons by tooth pulp stimulation. J Neurophysiol80:2621-2631.
35.
Chiang CY, Kwan CL, Hu JW, Sessle BJ (1999). Effects of GABA receptor antagonists on trigeminal subnucleus caudalis nociceptive neurons in normal and neonatally capsaicin-treated adult rats. J Neurophysiol82:2154-2162.
36.
Clavelou P., Pajot J., Dallel R., Raboisson P. (1989). Application of the formalin test to the study of orofacial pain in the rat. Neurosci Lett103:349-353.
37.
Cleland CL, Gebhart GF (1997). Does central nervous system neuroplasticity contribute to hyperalgesia? Behav Brain Sci20:444-445.
38.
Clements JR, Magnusson KR, Hautman J., Beitz AJ (1991). Rat tooth pulp projections to spinal trigeminal subnucleus caudalis are glutamate-like immunoreactive. J Comp Neurol309:281-288.
39.
Coderre TJ, Katz J. ( 1997). Peripheral and central hyperexcitability: differential signs and symptoms in persistent pain. Behav Brain Sci20:404-419.
40.
Coderre TJ, Katz J., Vaccarino AL, Melzack R. (1993). Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain52:259-285.
41.
Coimbra F., Coimbra A. (1994). Dental noxious input reaches the subnucleus caudalis of the trigeminal complex in the rat, as shown by c-fos expression upon thermal or mechanical stimulation. Neurosci Lett173:201-204.
42.
Cooper BY, Sessle BJ (1992). Anatomy, physiology, and pathophysiology of trigeminal system paresthesias and dysesthesias. In: Oral and maxillofacial surgery clinics of North America. Trigeminal nerve injury: diagnosis and management. Vol. 4, No. 2. LaBanc JP, Gregg JM, Saunders WB, editors. Philadelphia: W.B. Saunders, pp. 297-322.
43.
Craig AD, Dostrovsky JO (1997). Processing of nociceptive information at supraspinal levels. In: Anesthesia: biologic foundations. Yaksh TL, Lynch C 111, Zapol WM, Maze M, Biebuyck JF, Saidman LJ, editors. Philadelphia: Lippincott-Raven, pp. 625-642.
44.
Cutrer FM, Schoenfeld D., Limmroth V., Panahian N., Moskowitz M. (1995). Suppression by the sumatriptan analogue, CP-122,288 of c-fos immunoreactivity in trigeminal nucleus caudalis induced by intracisternal capsaicin. Br J Pharmacol114:987-992.
45.
Dallel R., Raboisson P., Auroy P., Woda A. ( 1988). The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res448:7-19.
46.
Dallel R., Clavelou P., Woda A. ( 1989). Effects of tractotomy on nociceptive reactions induced by tooth pulp stimulation in the rat. Exp Neural106:78-84.
47.
Dallel R., Raboisson P., Woda A., Sessle BJ (1990). Properties of nociceptive and nonnociceptive brainstem neurons in trigeminal subnucleus oralis of the rat. Brain Res521:95-106.
48.
Dallel R., Luccarini P., Molat J.-L, Woda A. ( 1996). Effects of systemic morphine on the activity of convergent neurons of spinal trigeminal nucleus oralis in the rat. Eur J Pharmacol314:19-25.
49.
Dallel R., De Chazeron I., Sierralta F., Raboisson P. (1997). Diencephalic projections of the rat spinal trigeminal nucleus oralis studied with the PHA-L method (abstract). Soc Neurosci Abstr23:154.
50.
Dallel R., Duale C., Molat J.-L (1998). Morphine administered in the substantia gelatinosa of the spinal trigeminal nucleus caudalis inhibits nociceptive activities in the spinal trigeminal nucleus oralis. J Neurosci18:3529-3536.
51.
Darian-Smith I. (1966). Neural mechanisms of facial sensation. Int Rev Neurobiol9:301-395.
52.
Denny-Brown D., Yanagisawa N. (1973). The function of the descending root of the fifth nerve. Brain96:783-814.
53.
Dickenson AH (1994). Where and how do opioids act? In: Progress in pain research and management. Vol. 2. Proceedings of the 7th World Congress on Pain, Aug 22-27, 1993, Paris. Gebhart GF, Hammond DL, Jensen TS, editors. Seattle: IASP Press, pp. 525-552.
54.
DiFiglia M., Aronin N. (1990). Synaptic interactions between GABAergic neurons and trigeminothalamic cells in the rat trigeminal nucleus caudalis. Synapse6:358-363.
55.
Ding YQ, Kaneko T., Nomura S., Mizuno N. (1996). Immunohistochemical localization of m-opioid receptors in the central nervous system of the rat. J Comp Neurol367:375-402.
56.
Dohrn CS, Beitz AJ (1994). NMDA receptor mRNA expression in NOS-containing neurons in the spinal trigeminal nucleus of the rat. Neurosci Lett175:28-32.
57.
Dong WK, Chudler EH (1984). Origins of tooth pulp-evoked far-field and early near-field potentials in the cat. J Neurophysiol51:859-889.
58.
Dostrovsky JO, Davis KD, Kawakita K. (1991). Central mechanisms of vascular headaches. Can J Physiol Pharmacol69:652-658.
59.
Duale C., Luccarini P., Cadet R., Woda A. ( 1996). Effects of morphine microinjections into the trigeminal sensory complex on the formalin test in the rat. Exp Neural142:331-339.
60.
Dubner R. (1985). Recent advances in our understanding of pain. In: Oro-facial pain and neuromuscular dysfunction: mechanisms and clinical correlates. Klineberg I, Sessle B, editors. Oxford: Pergamon Press, pp. 3-19.
61.
Dubner R. (1997). Neural basis of persistent pain: sensory specialization, sensory modulation, and neuronal plasticity. In: Progress in pain research and management. Vol. 8. Proceedings of the 8th World Congress on Pain, Aug 17-22, 1996, Vancouver. Jensen TS, Turner JA, Wiesenfeld-Hallin A, editors. Seattle: IASP Press, pp. 243-257.
62.
Dubner R., Basbaum AI (1994). Spinal dorsal horn plasticity following tissue or nerve injury. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 225-241.
63.
Dubner R., Bennett GJ (1983). Spinal and trigeminal mechanisms of nociception. Ann Rev Neurosci6:381-418.
64.
Dubner R., Sessle BJ, Storey AT (1978). The neural basis of oral and facial function. New York: Plenum Press.
65.
Duval P., Lenoir V., Moussaoui S., Garret C., Kerdelhue B. (1996). Substance P and neurokinin A variations throughout the rat estrous cycle; comparison with ovariectomized and male rats: II. Trigeminal nucleus and cervical spinal cord. J Neurosci Res45:610-616.
66.
Eberberger A., Anton F., Tölle TR, Zieglgansberger W. (1995) Morphine, 5-HT2 and 5-HT3 receptor antagonists reduce c-fos expression in the trigeminal nuclear complex following noxious chemical stimulation of the rat nasal mucosa. Brain Res676:336-342.
67.
Eisenberg E., Vos BP, Strassman AM (1996). The peripheral antinociceptive effect of morphine in a rat model of facial pain. Neuroscience72:519-525.
68.
Falls WM (1988). Synaptic organization of primary axons in trigeminal nucleus oral is. J Electron Microsc Tech10:213-227.
69.
Fields HL, Basbaum AI (1994). Central nervous system mechanisms of pain modulation. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 243-257.
70.
Fromm GH, Sessle BJ (1991). Trigeminal neuralgia. Current concepts regarding pathogenesis and treatment. Stoneham: Butterworth-Heinemann.
71.
Fromm GH, Sato K., Nakata M. (1992). The actions of GABAB antagonists in the trigeminal nucleus of the rat. Neuropharmacology31:475-480.
72.
Fukushima T., Kerr FWL (1979). Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections. J Comp Neurol183:169-184.
73.
Ginestal E., Matute C. (1993). Gamma-aminobutyric acid-immunoreactive neurons in the rat trigeminal nuclei. Histochemistry99:49-55.
74.
Goadsby PI, Zagami AS (1991). Stimulation of the superior sagittal sinus increases metabolic activity and blood flow in certain regions of the brainstem and upper cervical spinal cord of the cat. Brain114:1001-1011.
75.
Gobel S., Hockfield S., Ruda MA ( 1981). Anatomical similarities between medullary and spinal dorsal horns. In: Oral-facial sensory and motor functions. Kawamura Y, Dubner R, editors. Tokyo: Quintessence, pp. 211-223.
76.
Gobel S., Bennett GJ, Allen B., Humphrey E., Seltzer Z., Abdelmoumene M., et al. (1982). Synaptic connectivity of substantia gelatinosa neurons with reference to potential termination sites of descending axons. In: Brain stem control of spinal mechanisms. Sjolund B, Bjorklund A, editors. Amsterdam: Elsevier, pp. 135-158.
77.
Graham SH, Sharp FR, Dillon W. (1988). Intraoral sensation in patient with brain stem lesions: role of the rostral spinal trigeminal nuclei in pons. Neurology38:1529.
78.
Grudt TJ Williams IT (1994). mu-opioid agonists inhibit spinal trigeminal substantia gelatinosa neurons in guinea pig and rat. J Neurosci14:1646-1654.
79.
Grudt TJ, Williams IT, Travagli RA (1995). Inhibition by 5-hydroxytryptamine and noradrenaline in the substantia gelatinosa of the guinea-pig spinal trigeminal nucleus. J Physiol485:113-120.
80.
Guilbaud G., Bernard JF, Besson JM (1994). Brain areas involved in nociception and pain. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 113-128.
81.
Hannam AG, Sessle BJ (1994). Temporomandibular neurosensory and neuromuscular physiology. In: Temporomandibular joint and masticatory muscle disorders. Zarb GE, Carlsson G, Sessle BJ, Mohl ND, editors. Copenhagen: Munksgaard, pp. 67-100.
82.
Hargreaves KM, Roszkowski MT, Jackson DL, Bowles W., Richardson JD, Swift JQ (1995). Neuroendocrine and immune response to injury, degeneration, and repair. In: Temporomandibular disorders and related pain conditions. Progress in pain research and management. Vol. 4. Sessle BJ, Bryant PS, Dionne RA, editors. Seattle: IASP Press, pp. 273-292.
83.
Hathaway CB, Hu JW, Bereiter DA (1995). Distribution of fos-like immunoreactivity in the caudal brainstem of the rat following noxious chemical stimulation of the temporomandibular joint. J Comp Neurol356:444-456.
84.
Hayashi H. (1985). Morphology of terminations of small and large myelinated trigeminal primary afferent fibers in the cat. J Comp Neurol240:71-89.
85.
Hayashi H. (1992). Somatosensory pathways from the trigeminal nucleus to the mesencephalic parabrachial area. In: Processing and inhibition of nociceptive information. Inoki R, Shigenaga Y, Tohyama M, editors. Amsterdam: Elsevier, pp. 109-114.
86.
Henderson TA, lacquin MF (1995). What makes subcortical barrels? Requisite trigeminal circuitry and developmental mechanisms. In: Cerebral cortex. Vol. 11. lones EG, Diamond IT, editors. New York: Plenum Press, pp. 123-187.
87.
Henry JL, Sessle BJ, Lucier GE, Hu JW (1980). Effects of substance P on nociceptive and non-nociceptive trigeminal brain stem neurons. Pain8:33-45.
88.
Henry MA, Johnson LR, Nousek-Goebl N., Westrum LE (1996). Light microscopic localization of calcitonin gene-related peptide in the normal feline trigeminal system and following retrogasserian rhizotomy. J Comp Neurol365:526-540.
89.
Hoskin KL, Kaube H., Goadsby PJ (1996). Sumatriptan can inhibit trigeminal afferents by an exclusively neural mechanism. Brain119:1419-1428.
90.
Hu JW (1990). 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. Pain41:331-345.
91.
Hu JW, Sessle BJ (1984). 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 Neurophysiol52:39-53.
92.
Hu JW, Sessle BJ (1988). Properties of functionally identified nociceptive and nonnociceptive facial primary afferents and presynaptic excitability changes induced in their brainstem endings by raphe and orofacial stimuli in cats. Exp Neurol101:385-399.
93.
Hu JW, Sessle BJ (1989). Effects of tooth pulp deafferentation on nociceptive and non-nociceptive neurons of the feline trigeminal subnucleus caudalis (medullary dorsal horn). J Neurophysiol61:1197-1206.
94.
Hu JW, Sharav Y., Sessle BJ (1990). Effects of one or two-staged deafferentation of mandibular and maxillary tooth pulps on the functional properties of trigeminal brainstem neurones. Brain Res516:271-279.
95.
Hu JW, Sessle BJ, Raboisson P., Dallel R., Woda A. ( 1992a). Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brainstem neurones. Pain48:53-60.
96.
Hu JW, Shohara E., Sessle BJ (1992b). Patterns and plasticity of dental afferent inputs to trigeminal (V) brainstem neurons in kittens. Proc Finn Dent Soc88(Suppl 1):563-569.
97.
Hu JW, Tsai CM, Bakke M., Seo K., Tambeli CH, Vernon H., et al. (1997). Deep craniofacial pain: involvement of trigeminal subnucleus caudalis and its modulation. In: Progress in pain research and management. Vol. 8. Proceedings of the 8th World Congress on Pain, Aug 17-22, 1996, Vancouver. Jensen TS, Turner JA, Wiesenfeld-Hallin A, editors. Seattle: IASP Press, pp. 497-506.
98.
Hu JW, Woda A., Sessle BJ (1999). Pre-emptive local anaesthesia does not prevent tooth pulp deafferentation-induced neuroplastic changes in cat trigeminal brainstem neurones. Arch Oral Biol44:287-293.
99.
lwata K., Kanda K., Tsuboi Y., Kitajima K., Sumino R. (1995). Fos induction in the medullary dorsal horn and C1 segment of the spinal cord by acute inflammation in aged rats. Brain Res678:127-139.
100.
Jacquin MF, Stennett RA, Renehan WE, Rhoades RW (1988). Structure-function relationships in the rat brainstem subnucleus interpolaris: II. Low and high threshold trigeminal primary afferents. J Comp Neurol267:107-130.
101.
Jacquin MF, Chiaia NL, Haring JH, Rhoades RW (1990). lntersubnuclear connections within the rat trigeminal brainstem complex. Somatosens Motor Res7:399-420.
102.
Jasmin L., Burkey AR, Card JP, Basbaum AI (1997). Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-)parabrachio-amygdaloid, in the rat. J Neurosci17:3751-3765.
103.
Jensen TS, Turner JA, Wiesenfeld-Hallin A, editors (1997). Progress in pain research and management. Vol. 8. Proceedings of the 8th World Congress on Pain, Aug 17-22, 1996, Vancouver. Seattle: IASP Press.
104.
Johnson LR, Westrum LE, Henry MA (1991). Anatomic organization of the trigeminal system and the effects of deafferentation. In: Trigeminal neuralgia. Current concepts regarding pathogenesis and treatment. Fromm GH, Sessle BJ, editors. Stoneham: Butterworth-Heinemann, pp. 27-69.
105.
Kato J., Wakisaka S., Tabata MJ, Itotagawa T., Kurisu K. (1995). Appearance of dynorphin in the spinal trigeminal nucleus complex following experimental tooth movement in the rat. Arch Oral Biol40:79-81.
106.
Katz ) J. (1995). Pre-emptive analgesia: evidence, current status and future directions. Eur J Anaesthesiol12(Suppl 10):8-13.
107.
Kemplay S., Webster KE (1989). A quantitative study of the projections of the gracile, cuneate and trigeminal nuclei and of the medullary reticular formation to the thalamus in the rat. Neuroscience32:153-167.
108.
Kobayashi Y., Matsumura G. (1996). Central projections of primary afferent fibers from the rat trigeminal nerve labeled with isolectin B4-HRP. Neurosci Lett217:89-92.
109.
Kojima Y. (1990). Convergence patterns of afferent information from the temporomandibular joint and masseter muscle in the trigeminal subnucleus caudalis. Brain Res Bull24:609-616.
110.
Kondo E., Kiyama H., Yamano M., Shida T., Ueda Y., Tohyama M. (1995). Expression of glutamate (AMPA type) and y-aminobutyric acid (GABA)A receptors in the rat caudal trigeminal spinal nucleus. Neurosci Lett186:169-172.
111.
Kruger L., Sternini C., Brecha NC, Mantyh PW (1988). Distribution of calcitonin gene-related peptide immunoreactivity in relation to the rat central somatosensory projection. I Comp Neurol273:149-162.
112.
Kwan CL, Hu JW, Sessle BJ (1993). Effects of tooth pulp deafferentation on brainstem neurons of the rat trigeminal subnucleus oralis. Somatosens Motor Res10:115-131
113.
Kwan CL, Hu JW, Sessle BJ (1996). Neuroplastic effects of neonatal capsaicin treatment on neurons in adult rat trigeminal nuclei principalis and subnucleus oralis. J Neurophysiol75:298-310.
114.
Kwan CL, DeMaro JA, Hu JW, Jacquin MF, Sessle BJ (1999). C-fiber depletion alters response properties of neurons in trigeminal nucleus principalis. J Neurophysiol81:435-446.
115.
Lapa Rcrs, Bauer JA, Lindsey CJ (1996). A comparative and ultrastructural study of synaptic contacts established by primary sensory fibers in the spinal trigeminal nucleus of the rat. Tissue & Cell28:569-576.
116.
Levine J., Taiwo Y. (1994). Inflammatory pain. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 45-56.
117.
Lipton JA, Ship JA, Larach-Robinson D. (1993). Estimated prevalence and distribution of reported orofacial pain in the United States. J Am Dent Assoc124:115-121.
118.
Lu J., Bereiter DA (1995). Acute injection of adrenal steroids reduces cornea-evoked expression of c-fos within the spinal trigeminal nucleus of adrenalectomized rats. Neuroscience66:933-941.
119.
Lund JP ( 1991). Mastication and its control by the brain stem. CRC Crit Rev Oral Biol Med2:33-64.
120.
Lund IP, Donga R., Widmer CG, Stohler CS (1991). The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol69:683-694.
121.
Luo P., Dessem D. (1995). Inputs from identified jaw-muscle spindle afferents to trigeminothalamic neurons in the rat: a double-labelling study using retrograde HRP and intracellular biotinamide. J Comp Neurol353:50-66.
122.
Magnusson KR, Clements JR, Larson AA, Madl JE, Beitz AJ (1987). Localization of glutamate in trigeminothalamic projection neurons: a combined retrograde transport-immunohistochemical study. Somatosens Res4:177-190.
123.
Maillou P., Cadden SW (1997). Effects of remote deep somatic noxious stimuli on a jaw reflex in man Arch Oral Biol42:323-327.
124.
Maixner W., Sigurdsson A., Fillingim RB, Lundeen T., Booker DK (1995). Regulation of acute and chronic orofacial pain. In: Orofacial pain and temporomandibular disorders. Advances in pain research and therapy. Vol. 21. Fricton JR, Dubner R, editors. New York: Raven Press, pp. 85-102.
125.
Mansour A., Fox CA, Burke S., Meng F., Thompson RC, Akil H., et al. (1994). Mu, delta and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol350:412-438.
126.
Martinez S., Belmonte C. (1996). c-fos expression in trigeminal nucleus neurons after chemical irritation of the cornea: reduction by selective blockade of nociceptor chemosensitivity. Exp Brain Res109:56-62.
127.
Mason P., Strassman A., Maciewicz R. (1985). Is the jaw-opening reflex a valid model of pain? Brain Res10:137-146.
128.
Matthews MA, Hoffman KD, Hernandez TV (1989). Ulex europaeus agglutinin-1 binding to dental primary afferent projections in the spinal trigeminal complex combined with double immunolabeling of substance P and GABA elements using peroxidase and colloidal gold. Somatosens Motor Res6:513-536.
129.
McHaffie JG, Larson MA, Stein BE (1994). Response properties of nociceptive and low-threshold neurons in rat trigeminal pars caudalis. J Comp Neurol347:409-425.
130.
McQuay HJ (1994). Do preemptive treatments provide better pain control? In: Progress in pain research and management. Vol. 2. Proceedings of the 7th World Congress on Pain, Aug 22-27, 1993, Paris. Gebhart GF, Hammond DL, Jensen TS, editors. Seattle: IASP Press, pp. 709-723.
131.
Meller ST, Gebhart GF (1993). Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain52:235-240.
132.
Melzack R. (1994). Folk medicine and the sensory modulation of pain. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 1209-1217.
133.
Meng ID, Hu JW, Benetti AP, Bereiter DA (1997). Encoding of corneal input in two distinct regions of the spinal trigeminal nucleus in the rat: cutaneous receptive field properties, responses to thermal and chemical stimulation, modulation by diffuse noxious inhibitory controls, and projections to the parabrachial area. J Neurophysiol77:43-56.
134.
Mense S. (1993). Nociception from skeletal muscle in relation to clinical muscle pain. Pain54:241-289.
135.
Mokha SS (1993). Morphine differentially modulates nociceptive input in the superficial versus the deeper dorsal horn of the medulla (trigeminal nucleus caudalis) in the rat. Brain Res626:318-323.
136.
Moskowitz MA (1994). Drug mechanisms in acute migraine. In: Progress in pain research and management. Vol. 2. Proceedings of the 7th World Congress on Pain, Aug 22-27, 1993, Paris. Gebhart GF, Hammond DL, lensen TS, editors. Seattle: IASP Press, pp. 755-764.
137.
Narhi M., Yamamoto H., Ngassapa D., Hirvonen T. (1994). The neurophysiological basis and the role of inflammatory reactions in dentine hypersensitivity. Arch Oral Biol39(Suppl):23S-30S.
138.
Nishida Y., Yokota T. (1991). Corneal representation within the trigeminal subnucleus caudalis and adjacent bulbar lateral reticular formation of the cat. Jpn J Physiol41:551-565.
139.
Nishimori T., Buzzi MG, Chudler EH, Poletti CE, Moskowitz MA, Uhl GR (1990). Preproenkephalin up-regulation in nucleus caudalis: high and low intensity afferent stimulation differentially modulate early and late responses. ) Comp Neurol302:1002-1018.
140.
Nord SG, Ross GS ( 1977). Behavioral and neurophysiological correlates of dental pulp stimulation in the monkey. In: Pain in the trigeminal regions. Anderson DJ. Matthews B, editors. Amsterdam: Elsevier/North Holland, pp. 259-270.
141.
Nozaki K., Moskowitz MA, Boccalini P. (1992). CP-93,129, sumatriptan, dihydroergotamine block c-fos expression within rat trigeminal nucleus caudalis caused by chemical stimulation of the meninges. Br J Pharmacol106:409-415.
142.
Okada K., Oshima M., Kawakita K. (1996). Examination of the afferent fiber responsible for the suppression of jaw-opening reflex in heat, cold, and manual acupuncture stimulation in rats. Brain Res740:201-207.
143.
Panneton WM, Yavari P. (1995). A medullary dorsal horn relay for the cardiorespiratory responses evoked by stimulation of the nasal mucosa in the muskrat Ondatra zibethicus: evidence for excitatory amino acid transmission. Brain Res691:37-45.
144.
Parada CA, Luccarini P., Woda A. ( 1997). Effect of an NMDA receptor antagonist on the wind-up of neurons in the trigeminal oralis subnucleus. Brain Res761:313-320.
145.
Park SJ, Chiang CY, Kishimoto H., Hu JW, Sessle BJ (1998). NMDA involvement in pulp-induced neuroplasticity in trigeminal subnucleus oralis (abstract). J Dent Res77(Spec Iss B):895.
146.
Peppel P., Anton F. (1993). Responses of rat medullary dorsal horn neurons following intranasal noxious chemical stimulation: effects of stimulus intensity, duration, and interstimulus interval. J Neurophysiol70:2260-2275.
147.
Petralia RS, Yokotani N., Wenthold RJ (1994). Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci14:667-696.
148.
Phelan KD, Falls WM (1989). The interstitial system of the spinal trigeminal tract in the rat: anatomical evidence for morphological and functional heterogeneity. Somatosens Motor Res6:367-399.
149.
Pozo MA, Cervero F. (1993). Neurons in the rat spinal trigeminal complex driven by corneal nociceptors: receptive-field properties and effects of noxious stimulation of the cornea. J Neurophysiol70:2370-2378.
150.
Quartu M., Setzu MD, Del Fiacco M. (1996). trk-like immunoreactivity in the human trigeminal ganglion and subnucleus caudalis. NeuroReport7:1013-1019.
151.
Raboisson P., Dallel R., Woda A. ( 1989). Responses of neurones in the ventrobasal complex of the thalamus to orofacial noxious stimulation after large trigeminal tractotomy. Exp Brain Res77:569-576.
152.
Raboisson P., Dallel R., Clavelou P., Sessle BJ, Woda A. ( 1995). Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurons in the rat. J Neurophgsiol73:496-505.
153.
Rhoades RW, Chiaia NL, Hess PR, Miller MW (1988). Effect of neonatal infraorbital nerve transection on substance P- and leucine enkephalin-like immunoreactivities in trigeminal subnucleus caudalis of the rat. J Neurosci8:2234-2247.
154.
Salter MW, De Koninck Y., Henry JL (1993). Physiological roles for adenosine and ATP in synaptic transmission in the spinal dorsal horn. Prog Neurobiol41:125-156.
155.
Schmidt RF, Schaible H-G., Messlinger K., Heppelmann B., Hanesch U., Pawlak M. (1994). Silent and active nociceptor: structure, functions and clinical implications. In: Progress in pain research and management. Vol. 2. Proceedings of the 7th World Congress on Pain, Aug 22-27, 1993, Paris. Gebhart GF, Hammond DL, Jensen TS, editors. Seattle: IASP Press, pp. 213-250.
156.
Sessle BJ (1987). The neurobiology of facial and dental pain: present knowledge, future directions. J Dent Res66:962-981.
157.
Sessle BI (1996). Mechanisms of trigeminal and occipital pain. Pain Rev3:91-116.
158.
Sessle BJ, Hu IW (1991). Mechanisms of pain arising from articular tissues. Can J Physiol Pharmacol69:617-626.
159.
Sessle BJ, Chiang CY, Dostrovsky JO (1992). Interrelationships between sensorimotor cortex, anterior pretectal nucleus and periaqueductal gray in modulation of trigeminal sensorimotor function in the rat. In: Processing and inhibition of nociceptive information. Inoki R, Shigenaga Y, Tohyama M, editors. Amsterdam: Elsevier, pp. 77-82.
160.
Sessle BJ, Hu JW, Yu X-M. (1993). Brainstem mechanisms of referred pain and hyperalgesia in the orofacial and temporomandibular region. In: New trends in referred pain and hyperalgesia. Pain research and clinical management. Vol. 7. Vecchiet L, Albe-Fessard D, Lindblom U, editors. Amsterdam: Elsevier, pp. 59-71.
161.
Shepheard SL, Williamson DJ, Williams J., Hill RG, Hargreaves RJ (1995). Comparison of the effects of sumatriptan and the NK, antagonist CP-99,994 on plasma extravasation in dura mater and c-fos mRNA expression in trigeminal nucleus caudalis of rats. Neuropharmacology34:255-261.
162.
Shortland PJ, Jacquin MF, DeMaro JA, Kwan CL, Hu JW, Sessle BJ (1995). Central projections of identified trigeminal primary afferents after molar pulp deafferentation in adult rats. Somatosens Motor Res12:277-297.
163.
Shyu B.-C, Leung GM, Hu JW, Sessle BJ (1993). Tooth pulp deafferentation is not associated with changes in primary afferent depolarization of facial afferent endings in the brain stem. Exp Neurol123:243-250.
164.
Silverman JD, Kruger L. (1988). Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosens Res5:259-267.
165.
Slugg RM, Light AR (1994). Spinal cord and trigeminal projections to the pontine parabrachial region in the rat as demonstrated with Phaseolus vulgaris leucoagglutinin. J Comp Neurol229:49-61.
166.
Sluka KA, Willis WD, Westlund KN (1994). Inflammation-induced release of excitatory amino acids is prevented by spinal administration of a GABAA but not by a GABAB receptor antagonist in rats. J Pharmacol Exp Ther271:76-82.
167.
Soja PJ, Cairns BE, Christensen MP (1999). Transmission through ascending lumbar and trigeminal sensory pathways: dependence on behavioral state. In: Handbook of behavioral state control: cellular and molecular mechanisms. Lydic R, Baghdoyan HA, editors. Boca Raton, FL: CRC Press, pp. 521-544.
168.
Stein C. (1994). Interaction of immune-competent cells and nociceptors. In: Progress in pain research and management. Vol. 2. Proceedings of the 7th World Congress on Pain, Aug 22-27, 1993, Paris. Gebhart GF, Hammond DL, Jensen TS, editors. Seattle: IASP Press, pp. 285-297.
169.
Stohler CS (1995). Clinical perspectives on masticatory and related muscle disorders. Progress in pain research and management. Vol. 4. Sessle BJ, Bryant PS, Dionne RA, editors. Seattle: IASP Press, pp. 3-29.
170.
Stover JD, Schwab CA, Matthews MA (1992). Selective deafferentation of convergent inputs to trigeminal subnucleus caudalis: effects on calcitonin gene-related peptide distribution. Somatosens Motor Res9:107-130.
171.
Strassman AM, Mineta Y., Vos BP (1994a). Distribution of fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood vessels in the rat. ) Neurosci14:3725-3735.
172.
Strassman AM, Potrebic S., Maciewicz RJ (1994b). Anatomical properties of brainstem trigeminal neurons that respond to electrical stimulation of dural blood vessels. J Comp Neurol346:349-365.
173.
Suarez-Roca H., Maixner W. (1993). Activation of kappa opioid receptors by U50488H and morphine enhances the release of substance P from rat trigeminal nucleus slices. J Pharmacol Exp Ther264:648-653.
174.
Sugimoto T. (1987). Effects of chemical convulsants on chronic transsynaptic destruction of medullary dorsal horn neurons following inferior alveolar neurotomy in adult rats. In: Effects of injury on trigeminal and spinal somatosensory systems. Pubols LM, Sessle BJ, editors. New York: Alan R. Liss, pp. 167-174.
175.
Sugimoto T., Fujiyoshi Y., Xiao C., He YF, Ichikawa H. (1997a). Central projection of calcitonin gene-related peptide (CGRP)- and substance P (SP)-immunoreactive trigeminal primary neurons in the rat. Comp Neurol378:425-442.
176.
Sugimoto T., Fujiyoshi Y., He YF, Xiao C., Ichikawa H. (1997b). 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 Res28:361-371.
177.
Sunakawa M., Chiang CY, Sessle BJ, Hu JW (1999). Jaw electromyographic (EMG) activity induced by application of algesic chemicals to the rat tooth pulp. Pain80:493-501.
178.
Svensson P., Arendt-Neilsen L., Hove L. ( 1998). Muscle pain modulates mastication: an experimental study in humans. J Orofac Pain12:7-16.
179.
Takemura M., Nagase Y., Yoshida A., Yasuda K., Kitamura S., Shigenaga Y., et al. (1993). The central projections of the monkey tooth pulp afferent neurons. Somatosens Motor Res10:217-227.
180.
Tallaksen-Greene SJ, Young AB, Penney JB, Beitz AJ (1992). Excitatory amino acid binding sites in the trigeminal principal sensory and spinal trigeminal nuclei of the rat. Neurosci Lett141:79-83.
181.
Tokunaga A., Senba E., Manabe Y., Shida T., Ueda Y., Tohyama M. (1992). Orofacial pain increases mRNA level for galanin in the trigeminal nucleus caudalis of the rat. Peptides13:1067-1072.
182.
Travagli RA (1996). Muscarine receptor activation in the substantia gelatinosa of the spinal trigeminal nucleus of the guinea pig. J Neurophysiol76:3817-3822.
183.
Travagli RA, Williams JT (1996). Endogenous monoamines inhibit glutamate transmission in the spinal trigeminal nucleus of the guinea-pig. J Physiol (Lond)491:177-185.
184.
Tsuru K., Otani K., Kajiyama K., Suemune S., Shigenaga Y. (1989). Central terminations of periodontal mechanoreceptive and tooth pulp afferents in the trigeminal principal and oral nuclei of the cat. Brain Res485:29-61.
185.
Urban L., Thompson SWN, Dray A. ( 1994). Modulation of spinal excitability: co-operation between neurokinin and excitatory amino acid neurotransmitters. Trends Neurosci17:432-438.
186.
Villanueva L., Bouhassira D., Le Bars D. (1996). The medullary subnucleus reticularis dorsalis (SRD) as a key link in both the transmission and modulation of pain signals. Pain67:231-240.
187.
Vos BP, Strassman AM, Maciewicz RJ (1994). Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. ) Neurosci14:2708-2723.
188.
Wakisaka S., Sasaki Y., Ichikawa H., Matsuo S. (1992). Increase in c-fos-like immunoreactivity in the trigeminal nucleus complex after dental treatment. Proc Finn Dent Soc88(Suppl 1):551-556.
189.
Wang X.-M, Mokha SS (1996). Opioids modulate N-methyl-D-aspartic acid (NMDA)-evoked responses of trigeminothalamic neurons. J Neurophysiol76:2093-2096.
190.
Wang X.-M., Yan J.-Q., Zhang K.-M., Mokha SS (1996). Role of opioid receptors (μ. δ1, 82) in modulating responses of nociceptive neurons in the superficial and deeper dorsal horn of the medulla (trigeminal nucleus caudalis) in the rat. Brain Res739:235-243.
191.
Weinberger NM (1995). Dynamic regulation of receptive fields and maps in the adult sensory cortex. Ann Rev Neurosci18:129-158.
192.
Weng H.-R., Laird JMA, Cervero F., Schouenborg J. (1998). GABAA receptor blockade inhibits Aβ fibre evoked wind-up in the arthritic rat. NeuroReport9:1065-1069.
193.
Woda A., Parada CA, Luccarini P. (1998). Intranuclear injection of MK801 in the trigeminal caudalis subnucleus decreases the wind-up of neurones in the trigeminal oralis subnucleus (abstract). J Dent Res77(Spec Iss B):896.
194.
Woolf CJ (1991). Central mechanisms of acute pain. In: Pain research and clinical management. Vol. 4. Proceedings of the 6th World Congress on Pain, Apr 1-6, 1990, Adelaide. Bond MR, Charlton JE, Woolf CJ, editors. Amsterdam: Elsevier, pp. 25-34.
195.
Woolf CJ (1994). The dorsal horn: state-dependent sensory processing and the generation of pain. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 101-112.
196.
Woolf CJ, Thompson JW (1994). Stimulation fibre-induced analgesia: transcutaneous electrical nerve stimulation (TENS) and vibration. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 1191-1208.
197.
Woolsey TA (1990). Peripheral alteration and somatosensory development. In: Development of sensory systems in mammals. Coleman JR, editor. New York: Wiley, pp. 461-526.
198.
Yaksh TL, Malmberg AB (1994). Central pharmacology of nociceptive transmission. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 165-200.
199.
Yew DT, Luo CB, Shen WZ ( 1992). Immunohistochemical localization of enkephalin and substance P in the nucleus caudalis of the spinal trigeminal V in the medulla oblongata of the human fetus. Neuroscience51:185-190.
200.
Yokota T. (1985). Neural mechanisms of trigeminal pain. In: Advances in pain research and therapy. Vol. 9. Fields HL, Dubner R, Cervero F, editors. New York: Raven Press, pp. 221-232.
201.
Yokota T., Nishikawa Y., Koyama N. (1986). Tooth pulp input to the shell region of nucleus ventralis posteromedialis of the cat thalamus. J Neurophysiol56:80-98.
202.
Yoshida A., Dostrovsky JO, Sessle BJ, Chiang CY (1991). Trigeminal projections to the nucleus submedius of the thalamus in the rat. J Comp Neurol307:609-625.
203.
Young RF, Rinaldi PC (1994). Brain stimulation for relief of chronic pain. In: Textbook of pain. 3rd ed. Wall PD, Melzack R, editors. London: Churchill-Livingstone, pp. 1225-1233.
204.
Yu X-M., Sessle BJ, Hu JW (1993). Differential effects of cutaneous and deep application of inflammatory irritant on mechanoreceptive field properties of trigeminal brain stem nociceptive neurons. I Neurophysiol70:1704-1707.
205.
Yu X-M., Sessle BJ, Vernon H., Hu JW (1994). Administration of opiate antagonist naloxone induces recurrence of increased jaw muscle activities related to inflammatory irritant application to rat temporomandibular joint region. J Neurophysiol72:1430-1433.
206.
Yu X-M., Sessle BJ, Vernon H., Hu JW (1995). Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity. Pain60:143-149.
207.
Yu X-M., Sessle BJ, Haas DA, lzzo A., Vernon H., Hu JW (1996). Involvement of NMDA receptor mechanisms in the jaw electromyographic activity and plasma extravasation induced by inflammatory irritant injection into the temporomandibular joint region. Pain68:169-178.
208.
Zhang KM, Wang XM, Mokha SS (1996). Opioids modulate N-methyl-D-aspartic acid (NMDA)-evoked responses of neurons in the superficial and deeper dorsal horn of the medulla trigeminal nucleus caudalis. Brain Res719:229-233.
