Evidence for subnucleus interpolaris in craniofacial muscle pain mechanisms demonstrated by intramuscular injections with hypertonic saline

Brain Research

Volumn 842, Issue 1, 1999, Pages 166-183

  Ro, Jin Y ^a   Capra, Norman F ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Craniofacial; Hypertonic saline; Muscle nociception; Trigeminal; Vi

Indexed keywords

SODIUM CHLORIDE;

ANIMAL CELL; ARTICLE; EVOKED RESPONSE; FACE MUSCLE; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; TRIGEMINAL NERVE;

ANIMALS; CATS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; INJECTIONS, INTRAMUSCULAR; MUSCLE, SKELETAL; MYOFASCIAL PAIN SYNDROMES; NEURONS; NOCICEPTORS; PHYSICAL STIMULATION; POSTERIOR HORN CELLS; SALINE SOLUTION, HYPERTONIC; SKIN; STEREOTAXIC TECHNIQUES; STIMULATION, CHEMICAL; TRIGEMINAL NUCLEI;

EID: 0033581322     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01860-0     Document Type: Article

References (88)

1. Amano N., Hu J.W., Sessle B.J. Response of neurons in feline trigeminal subnucleus caudalis (medullary dorsal horn) to cutaneous, introral, and muscle afferent stimuli. J. Neurophysiol. 55:1986;227-243.
2. Arendt-Nielson L., Graven-Nielson T., Svarrer H., Svensson P. The influence of low back pain on muscle activity and coordination during gait: a clinical and experimental study. Pain. 64:1995;231-240.
3. Ashton-Miller J.A., McGlashen K.M., Herzenberg J.E., Stohler C.S. Cervical muscle myoelectrical response to acute experimental sternocleidomastoid pain. Spine. 15:1990;1006-1012.
4. Azerad J., Woda A., Albe-Fessard D. Physiological properties of neurons in different parts of the cat trigeminal sensory complex. Brain Res. 246:1982;7-21.
5. Basbaum A.I., Fields H.L. Endogenous pain control mechanisms: review and hypothesis. Ann. Neurol. 4:1978;451-462.
6. Basbaum A.I., Fields H.L. Endogenous pain control system: brainstem spinal pathways and endorphine circuitry. Annu. Rev. Neurosci. 7:1984;39-338.
7. Bessou P., Laporte Y. Activation des fibres afferentes myelinisees d'origine muscularie (fibres du groupe III). J. Physiol. 52:1960;19-20.
8. Bouhassira D., Gall O., Chitour D., Le Bars D. Dorsal horn convergent neurones: negative feedback triggered by spatial summation of nociceptive afferents. Pain. 62:1995;195-200.
9. Burstein R., Yamamura H., Malick A., Strassman A. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brainstem trigeminal neurons. J. Neurophysiol. 79:1998;964-982.
10. Capra N.F., Wax T.D. Distribution and central projection of primary afferent neurons that innervate the masseter muscle and mandibular periodontium: a double-label study. J. Comp. Neurol. 279:1989;341-352.
11. Capra N.F., Ro J.Y., Wax T.D. Physiological identification of movement-related neurons in the spinal trigeminal nucleus of cats. Somatosens. Motor Res. 11:1994;77-88.
12. Carpenter D., Engberg I., Lundberg A. Primary afferent depolarization evoked from the brainstem and cerebellum. Arch. Ital. Biol. 104:1966;73-85.
13. Carstens E., Kuenzler N., Handwerker H.O. Activation of neurons in rat trigeminal subnucleus caudalis by different chemicals applied to oral and oral mucosa. J. Neurophysiol. 80:1998;465-492.
14. Chung J.M., Fang Z.R., Hori Y., Lee K.H., Willis W.D. Prolonged inhibition of primates pinothalamic tract cells by peripheral nerve stimulation. Pain. 19:1984;259-275.
15. Chung J.M., Lee K.H., Hori Y., Endo K., Willis W.D. Factors influencing peripheral nerve stimulation produced inhibition of primate spinothalamic tract cells. Pain. 19:1984;277-293.
16. Coghill R., Mayer D., Price D. Wide dynamic range but not nociceptive specific neuron encode multidimensional features of prolonged repetitive heat pain. J. Neurophysiol. 69:1993;703-716.
17. Cook A.J., Woolf C.J., Wall P.D., McMahon S.B. Dynamic receptive field plasticity in rat spinal cord dorsal horn following C-primary afferent input. Nature. 325:1987;151-153.
18. Craig A.D., Kniffki K.-D. Spinothalamic lumbosacral lamina I cells responsive to skin and muscle stimulation in the cat. J. Physiol. 365:1985;197-221.
19. Dallel R., Raboisson P., Auroy P., Woda A. The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res. 448:1988;7-19.
20. Dallel R., Clavelou P., Woda A. Effects of tractotomyon nociceptive relations induced by tooth pulp stimulation in the rat. Exp. Neurol. 106:1989;78-84.
21. Dallel R., Raboisson P., Woda A., Sessle B.J. Properties of nociceptive and noncociceptive neurons in trigeminal subnucleus oralis of the rat. Brain Res. 521:1990;95-106.
22. Dallel R., Luccarini P., Molat J.-L., Woda A. Effects of systemic morphine on the activity of convergent neurons of spinal trigeminal nucleus oralis in the rat. Eur. J. Pharmacol. 314:1996;19-25.
23. Dallel R., Duale C., Molat J.-L. Morphine administered in the substantia gelatinosa of the spinal trigeminal nucleus caudalis inhibits nociceptive activities in the spinal trigeminal nucleus oralis. J. Neurosci. 18:1998;3529-3536.
24. R. Dubner, B.J. Sessle, A. Storey, The Neurological Basis of Oral and Facial Function, Plenum, New York, 1978.
25. Dubner R., Bennet G.J. Spinal and trigeminal mechanisms of nociception. Annu. Rev. Neurosci. 6:1983;381-418.
26. Dubner R., Kenshalo D., Maixner W., Bushnell M., Oliveras J. The correlation of monkey medullary dorsal horn neuronal activity and the perceived intensity of noxious heat stimuli. J. Neurophysiol. 62:1989;450-457.
27. Eisenman J., Landgren 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. 59:1963;5-44.
28. Feinstein B., Langton J.N.K., Jameson R.M., Schiller F. Experiments on pain referred from deep tissues. J. Bone Jt. Surg. 36:1954;981-997.
29. H.L. Fields, A.I. Basbaum, Central nervous system mechanisms of pain modulation, in: P.D. Wall, R. Melzak (Eds.), Textbook of Pain, 1994, pp. 243-257.
30. Graven-Nielson T., Arendt-Nielson L., Svensson P., Jensen T.S. Experimental muscle pain: a quantitative study of local and referred pain in humans following injection of hypertonic saline. J. Musculoskeletal Pain. 5:1997;49-68.
31. Graven-Nielson T., Arendt-Nielson L., Svensson P., Jensen T.S. Stimulus-response functions in areas with experimentally induced referred muscle pain - a psychophysical study. Brain Res. 744:1997;121-128.
32. Graven-Nielson T., Fenger-Gron L.S., Svensson P., Streengaard-Pedersen K., Arendt-Nielson L., Jensen T.S. Quantification of deep and superficial sensibility in saline-induced muscle pain - a psychophysical study. Somatosens. Motor Res. 15:1998;46-53.
33. Hayashi H., Sumino R., Sessle B.J. Functional organization of trigeminal subnucleus interpolaris: nociceptive and innocuous afferent inputs, projections to thalamus, cerebellum and spinal cord, and descending modulation from periaqueductal gray. J. Neurophysiol. 51:1984;890-905.
34. Hentall I.D., Fields H.L. Segmental and descending influences on intraspinal thresholds of single C-fibers. J. Neurophysiol. 42:1979;1527-1537.
35. Hoheisel U., Mense S. Long-term changes in discharge behavior of cat dorsal horn neurones following noxious stimulation of deep tissues. Pain. 36:1989;239-247.
36. Hoheisel U., Mense S. Response behavior of cat dorsal horn neurones receiving input from skeletal muscle and other deep somatic tissues. J. Physiol. 426:1990;265-280.
37. Hu J.W., Dostrovsky J.O., Sessle B.J. Functional properties of neurons in subnucleus caudalis of the cat: I. Responses to oro-facial noxious and non-noxious stimuli and projections to thalamus and subnucleus oralis. J. Neurophysiol. 45:1981;173-192.
38. Hu J.W. Response properties of nociceptive and non-nociceptive neurons in the rat's trigeminal subnucleuscaudalis (Medullary dorsal horn) related to cutaneous and deep craniofacial afferent stimulation and modulation by diffuse noxious inhibitory controls. Pain. 41:1990;331-345.
39. Hu J.W., Sessle B.J., Raboisson P., Dallel R., Woda A. A stimulation of craniofacial afferents induces prolonged facilitatory effects in trigeminal nociceptive brainstem neurones. Pain. 48:1992;53-60.
40. T. Humphrey, The central relations of the trigeminal nerve, in: E.A. Kahn, E.C. Crosby, R.C. Schneider, J.A. Taren (Eds.), The Surgery of Pain from Correlative Neurosurgery, C.C. Thomas, Chicago, 1969, pp. 477-508.
41. Hunt C.C. Relation of function to diameter in afferent fibers of muscle nerves. J. Gen. Physiol. 38:1954;117-131.
42. Hylden J.L.K., Nahin R.L., Traub R.J., Dubner R. Expansion of receptive fields of spinal lamina I projection neurons in rats with unilateral adjuvant-induced inflammation: the contribution of dorsal horn mechanisms. Pain. 37:1989;229-243.
43. Jensen T., Norup M. Experimental pain in human temporal muscle induced by hypertonic saline, potassium and acidity. Cephalagia. 12:1996;101-106.
44. Kellgren J.H. Observations on referred pain arising from muscle. Clin. Sci. 3:1938;175-190.
45. Laird J.M.A., Cervero F. A comparative study of the changes in receptive field properties of multireceptive and nociceptive rat dorsal horn neurons following noxious mechanical stimulation. J. Neurophysiol. 62:1989;854-863.
46. Lloyd D.P.C., Chang H.T. Afferent fibers in muscle nerves. J. Neurophysiol. 11:1948;199-208.
47. Lund J.P., Donga R., Widmer C.G., Stohler C.S. The pain adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can. J. Physiol. Pharmacol. 69:1991;683-694.
48. Lund J.P. Mastication and its control by the brainstem. Crit. Rev. Oral Biol. Med. 2:1991;33-64.
49. Maixner W., Dubner R., Bushnell M., Kenshalo D., Oliveras J. Wide dynamic range dorsal horn neurons participate in the encoding process by which monkeys perceive the intensity of noxious heat stimuli. Brain Res. 374:1986;385-388.
50. Maixner W., Dubner R., Kenshalo D., Bushnell M., Oliveras J. Responses of monkey medullary dorsal horn neurons during detection of noxious heat stimuli. J. Neurophysiol. 62:1989;437-449.
51. McMahon S.B., Koltzenburg M. The changing role of primary afferent neurons in pain. Pain. 43:1990;269-272.
52. Meng I.D., Hu J.W., Bennetti A.P., Bereiter D.A. Differential encoding of corneal input in two distinct regions of the spinal trigeminal nucleus (Vsp) in the rat. J. Neurophysiol. 77:1997;43-56.
53. Meng I.D., Hu J.W., Bereiter D.A. Differential effects of morphine on corneal-responsive neurons in rostral versus caudal regions of spinal trigeminal nucleus in the rat. J. Neurophysiol. 79:1998;2563-2602.
54. Mense S., Meyer H. Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J. Physiol. 363:1985;403-417.
55. Mense S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain. 54:1993;241-289.
56. Nishimori T., Sera M., Suemune S., Yoshida A., Tsuru K., Tsuiki Y., Akisaka T., Okamoto T., Dateoka Y., Shigenaga Y. The distribution of muscle primary afferents from the masseter nerve to the trigeminal sensory nuclei. Brain Res. 372:1986;375-381.
57. Oakden E.L., Boissonade F.M. Fos expression in the ferret trigeminal nuclear complex following tooth pulp stimulation. Neuroscience. 84:1998;1197-1208.
58. Ohya A. Response properties of trigeminal subnucleus interpolaris neurons to afferent inputs from deep oral structures. Brain Res. Bull. 29:1992;773-781.
59. Ohya A., Tsuruoka M., Imai E., Fukunaga H., Shinya A., Furuya R., Kawawa T., Matsui Y. Thalamic- and cerebellar-projecting interpolaris neuron responses to afferent inputs. Brain Res. Bull. 32:1993;615-621.
60. Paintal A.S. Functional analysis of group III afferent fibers of mammalian muscles. J. Physiol. 152:1960;250-270.
61. Parada C.A., Luccarini P., Woda A. Effect of an NMDA receptor antagonist on the wind-up of neurons in the trigeminal oralis subnucleus. Brain Res. 761:1997;313-320.
62. E.R. Perl, Why are selectively responsive and multireceptive neurons both present in somatosensory pathways, in: C.V. Euler, O. Franzen, U. Lindblom, D. Ottoson (Eds.), Wenner-Gren International Symposium Series, Somatosensory Mechanisms, 41, Plenum, New York, 1984, pp. 141-161.
63. Qian J., Brown S.D., Carlton S.M. Systemic ketamine attenuates nociceptive behaviors in a rat model of peripheral neuropathy. Brain Res. 715:1996;51-62.
64. Raboisson P., Bourdiol P., Dallel R., Clavelou P., Woda A. Responses of trigeminal subnucleus oralis nociceptive neurons to subcutaneous formalin in the rat. Neurosci. Lett. 125:1991;179-182.
65. Raboisson P., Dallel R., Clavelou P., Sessle B.J. Effects of subcutaneous formalin on the activity of trigeminal brainstem nociceptive neurons in the rat. J. Neurophysiol. 73:1995;496-505.
66. Ro J.Y., Capra N.F. Encoding of jaw movements by central trigeminal neurons with cutaneous receptive fields. Exp. Brain Res. 104:1995;363-375.
67. J.Y. Ro, N.F. Capra, Physiological evidence for caudal brainstem projections of jaw muscle spindle afferents, Exp. Brain Res. (1999) in press.
68. Sessle B.J., Hu J.W., Amano N., Zhong G. Convergence of cutaneous, tooth pulp, visceral, neck, and muscle afferents onto nociceptive and non-nociceptive neurons in trigeminal subnucleus caudalis (Medullary dorsal horn) and its implications for referred pain. Pain. 27:1986;219-235.
69. Sessle B.J. The neurobiology of facial and dental pain: present knowledge, future directions. J. Musculoskeletal Pain. 66:1987;962-981.
70. Shigenaga Y., Sera M., Nishimori T., Suemune S., Nishimura M., Yoshida A., Tsuru K. The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J. Comp. Neurol. 286:1988;489-507.
71. Stacey M.J. Free nerve endings in skeletal muscle of the cat. J. Anat. 105:1969;231-254.
72. Stohler C.S., Ashton-Miller J.A., Carlson D.S. The effects of pain from the mandibular joint and muscles on masticatory motor behavior in man. Arch. Oral Biol. 33:1988;175-182.
73. C.S. Stohler, X. Zhang, J.A. Ashton-Miller, An experimental model of jaw muscle pain in man, in: Z. Davidovitch (Ed.), The Biological Mechanisms of Tooth Movement and Craniofacial Adaptation, The Ohio State University College of Dentistry, Columbus, 1992, pp. 503-511.
74. Stohler C.S., Kowalski C.J. Spatial and temporal summation of sensory and affective dimensions of deep somatic pain. Pain. 79:1999;165-173.
75. Stubhaug A., Breivik H., Eide P.K., Kreunen M., Foss A. Mapping of punctate hyperalgesia around a surgical incision demonstrates that ketamine is a powerful suppressor of central sensitization to pain following surgery. Acta Anaesthesiol. Scand. 41:1997;1124-1132.
76. 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. 794:1998;353-358.
77. Sugimoto T., He Y.-F., Xiao C., Ichikawa H. c-fos Induction in the subnucleus oralis following trigeminal nerve stimulation. Brain Res. 783:1998;158-162.
78. Svensson P., Arendt-Nielson L., Houe L. Sensory-motor interactions of human experimental unilateral jaw muscle pain: a quantitative analysis. Pain. 64:1995;241-249.
79. Svensson P., Houe L., Arendt-Nielson L. Bilateral experimental muscle pain changes electromyographic activity of human jaw-closing muscles during mastication. Exp. Brain Res. 116:1997;182-185.
80. Svensson P., Arendt-Nielson L., Houe L. Muscle pain modulates mastication: an experimental study in humans. J. Orofacial Pain. 12:1998;7-16.
81. Taber E. The cytoarchitecture of the brainstem of the cat. J. Comp. Neurol. 116:1961;27-69.
82. Traub R.J. Spinal modulation of the induction of central sensitization. Brain Res. 778:1997;34-42.
83. Ujihara H., Sasa M., Fujita Y., Takaori S. Opioid-mediated inhibition from the subnucleus caudalis of spinal trigeminal nucleus to the neurons in the subnucleus oralis. Brain Res. 18:1987;52-57.
84. Vecchiet L., Galletti R., Giamberardino M.A., Dragani L., Marini F. Modifications of cutaneous, subcutaneous and muscular sensory and pain thresholds after the induction of and experimental algogenic focus in the skeletal muscle. Clin. J. Pain. 4:1988;55-59.
85. Westberg K.-G., Clavelou P., Schwartz G., Lund J.P. Effects of chemical stimulation of masseter muscle nociceptors on trigeminal motoneuron activities during fictive mastication in the rabbit. Pain. 73:1997;295-308.
86. W.D. Willis, R.E. Coggeshall, Sensory Mechanisms of the Spinal Cord, Plenum, New York, 1991.
87. Woolf C.J. Evidence for a central component of post injury pain hypersensitivity. Nature. 306:1983;686-688.
88. Young R.F., Perryman K.M. Neuronal responses in rostral trigeminal brainstem nuclei of macaque monkeys after chronic trigeminal tractotomy. J. Orofacial Pain. 65:1986;508-516.