Convergence of cutaneous, musculoskeletal, dural and visceral afferents onto nociceptive neurons in the first cervical dorsal horn

European Journal of Neuroscience

Volumn 26, Issue 1, 2007, Pages 142-154

  Morch C D ^a   Hu, J W ^b   Arendt Nielsen, L ^a   Sessle, B J ^b  

^a AALBORG UNIVERSITY   (Denmark)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Neck; Rat; Sensory integration; Somatotopy

Indexed keywords

ACETIC ACID; CHLORALOSE; GLUTAMIC ACID; URETHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CERVICAL SPINAL CORD; CLUSTER ANALYSIS; CONTROLLED STUDY; CORNEA; DURA MATER; ELECTROSTIMULATION; FACE; FOREFOOT; HYPOGLOSSAL NERVE; LARYNGEAL NERVE; MALE; MASSETER MUSCLE; MICROINJECTION; MUSCLE EXCITATION; MUSCULOSKELETAL SYSTEM; NECK; NERVE EXCITABILITY; NERVE STIMULATION; NOCICEPTIVE RECEPTOR; NOCICEPTIVE STIMULATION; NONHUMAN; PERICARDIUM; PRIORITY JOURNAL; RAT; SENSORY NERVE; SHOULDER; SKIN STIMULATION; SPINAL CORD DORSAL HORN; STIMULUS RESPONSE; TEMPOROMANDIBULAR JOINT; TONGUE; TRIGEMINAL NERVE;

ACETIC ACID; ANIMALS; CLUSTER ANALYSIS; CORNEA; DURA MATER; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; HEAT; HYPOGLOSSAL NERVE; LARYNGEAL NERVES; MALE; MASSETER MUSCLE; MECHANORECEPTORS; MICROINJECTIONS; MUSCLE, SKELETAL; NEURONS, AFFERENT; NOCICEPTORS; PAIN MEASUREMENT; PHYSICAL STIMULATION; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; SKIN; TEMPOROMANDIBULAR JOINT;

EID: 34447130927     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05608.x     Document Type: Article

References (77)

1. Anthony, M. (1992) Headache and the greater occipital nerve. Clin. Neurol. Neurosurg., 94, 297 300.
2. Bartsch, T. Goadsby, P.J. (2002) Stimulation of the greater occipital nerve induces increased central excitability of dural afferent input. Brain, 125, 1496 1509.
3. Bartsch, T. Goadsby, P.J. (2003a) Increased responses in trigeminocervical nociceptive neurons to cervical input after stimulation of the dura mater. Brain, 126, 1801 1813.
4. Bartsch, T. Goadsby, P. (2003b) The trigeminocervical complex and migraine: Current concepts and synthesis. Curr. Pain Headache Rep., 7, 371 376.
5. Bereiter, D.A., Bereiter, D.F., Hirata, H. Hu, J.W. (2000) C-fos expression in trigeminal spinal nucleus after electrical stimulation of the hypoglossal nerve in the rat. Somatosens. Motor Res., 17, 229 237.
6. Bogduk, N. (2001) Cervicogenic headache: Anatomic basis and pathophysiologic mechanisms. Curr. Pain Headache Rep., 5, 382 386.
7. Boor, C.D. (1978) A practical guide to splines. In Antmann, S.S., Marsden, J.E. Sirovich, L. (Eds), Applied Mathematical Sciences. Springer, New York, pp. 291 313.
8. Burstein, R. (2001) Deconstructing migraine headache into peripheral and central sensitization. Pain, 89, 107 110.
9. Burstein, R., Yamamura, H., Malick, A. Strassman, A.M. (1998) Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J. Neurophysiol., 79, 964 982.
10. Cairns, B.E., Sessle, B.J. Hu, J.W. (2001a) Temporomandibular-evoked jaw muscle reflex: role of brain stem NMDA and non-NMDA receptors. Neuroreport, 12, 1875 1878.
11. Cairns, B.E., Hu, J.W., Arendt-Nielsen, L., Sessle, B.J. Svensson, P. (2001b) Sex-related differences in human pain and rat afferent discharge evoked by injection of glutamate into the masseter muscle. J. Neurophysiol., 86, 782 791.
12. Cairns, B.E., Sessle, B.J. Hu, J.W. (2001c) Characteristics of glutamate-evoked temporomandibular joint afferent activity in the rat. J. Neurophysiol., 85, 2446 2454.
13. Chandler, M.J., Zhang, J.H. Foreman, R.D. (1996) Vagal, sympathetic and somatic sensory inputs to upper cervical (C-1-C-3) spinothalamic tract neurons in monkeys. J. Neurophysiol., 76, 2555 2567.
14. Chandler, M.J., Zhang, J.H. Foreman, R.D. (1998) Phrenic nerve inputs to upper cervical (C1-C3) spinothalamic tract neurons in monkeys. Brain Res., 798, 93 100.
15. Chandler, M.J., Qin, C., Yuan, Y. Foreman, R.D. (1999) Convergence of trigeminal input with visceral and phrenic inputs on primate C1-C2 spinothalamic tract neurons. Brain Res., 829, 204 208.
16. Chiang, C.Y., Hu, J.W. Sessle, B.J. (1994) 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.
17. Chiang, C.Y., Park, S.J., Kwan, C.L., Hu, J.W. Sessle, B.J. (1998) NMDA receptor mechanisms contribute to neuroplasticity induced in caudalis nociceptive neurons by tooth pulp stimulation. J. Neurophysiol., 80, 2621 2631.
18. Chudler, E.H., Foote, W.E. Poletti, C.E. (1991) Responses of cat C1 spinal cord dorsal and ventral horn neurons to noxious and non-noxious stimulation of the head and face. Brain Res., 555, 181 192.
19. Clement, C.I., Keay, K.A., Podzebenko, K., Gordon, B.D. Bandler, R. (2000) Spinal sources of noxious visceral and noxious deep somatic afferent drive onto the ventrolateral periaqueductal gray of the rat. J. Comp. Neurol., 425, 323 344.
20. Corbett, E.K.A., Saha, S., Deuchars, J., McWilliam, P.N. Batten, T.F.C. (2003) Ionotropic glutamate receptor subunit immunoreactivity of vagal preganglionic neurones projecting to the rat heart. Auton. Neurosci., 105, 105 117.
21. Davis, K.D. Dostrovsky, J.O. (1988) Responses of feline trigeminal spinal tract nucleus neurons to stimulation of the middle meningeal artery and sagittal sinus. J. Neurophysiol., 59, 648 666.
22. Dubner, R. Bennett, G.J. (1983) Spinal and trigeminal mechanisms of nociception. Annu. Rev. Neurosci., 6, 381 418.
23. Dubner, R., Sessle, B.J. Storey, A.T. (1978) The Neutral Basis of Oral and Facial Function. Plenum Press, New York.
24. Foreman, R.D. (1999) Mechanisms of cardiac pain. Annu. Rev. Physiol., 61, 143 167.
25. Foreman, R.D. (2000) Integration of viscerosomatic sensory input at the spinal level. Prog. Brain Res., 122, 209 221.
26. Goadsby, P.J. (2003) Migraine: diagnosis and management. J. Int. Med., 33, 436 442.
27. Goadsby, P.J., Knight, Y.E. Hoskin, K.L. (1997) Stimulation of the greater occipital nerve increases metabolic activity in the trigeminal nucleus caudalis and cervical dorsal horn of the cat. Pain, 73, 23 28.
28. Gobel, S., Falls, W.M. Humphrey, E. (1981) Morphology and synaptic connections of ultrafine primary axons in lamina-I of the spinal dorsal horn - Candidates for the terminal axonal arbors of primary neurons with unmyelinated (C) axons. J. Neurosci., 1, 1163 1179.
29. van Ham, J.J. Yeo, C.H. (1996) The central distribution of primary afferents from the external eyelids, conjunctiva, and cornea in the rabbit, studied using WGA-HRP and B-HRP as transganglionic tracers. Exp. Neurol., 142, 217 225.
30. Hathaway, C.B., Hu, J.W. Bereiter, D.A. (1995) Distribution of Fos-like immunoreactivity in the caudal brain-stem of the rat following noxious chemical-stimulation of the temporomandibular-joint. J. Comp. Neurol., 356, 444 456.
31. Hirata, H., Hu, J.W. Bereiter, D.A. (1999) Responses of medullary dorsal horn neurons to corneal stimulation by CO2 pulses in the rat. J. Neurophysiol., 82, 2092 2107.
32. Hirata, H., Okamoto, K., Tashiro, A. Bereiter, D.A. (2004) A novel class of neurons at the trigeminal subnucleus interpolaris/caudalis transition region monitors ocular surface fluid status and modulates tear production. J. Neurosci., 24, 4224 4232.
33. Hotelling, H. (1933) Analysis of a complex of statistical variables into principal components. J. Educ. Psych., 24, 417 441.
34. Hu, J.W. (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. Pain, 41, 331 345.
35. Hu, J.W., Dostrovsky, J.O. Sessle, B.J. (1981) Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). I. Responses to oral-facial noxious and nonnoxious stimuli and projections to thalamus and subnucleus oralis. J. Neurophysiol., 45, 173 192.
36. Hu, J.W., Sessle, B.J., Raboisson, P., Dallel, R. Woda, A. (1992) Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brain-stem neurones. Pain, 48, 53 60.
37. Hu, J.W., Sun, K.Q., Vernon, H. Sessle, B.J. (2005) Craniofacial inputs to upper cervical dorsal horn: Implications for somatosensory information processing. Brain Res., 1044, 93 106.
38. Imbe, H., Dubner, R. Ren, K. (1999) Masseteric inflammation-induced Fos protein expression in the trigeminal interpolaris/caudalis transition zone: contribution of somatosensory-vagal-adrenal integration. Brain Res., 845, 165 175.
39. Kalezic, I., Pilyavskii, A.I., Maisky, V.A., Kostyukov, A.I., Windhorst, U. Johansson, H. (2004) Distinctive pattern of c-fos expression in the feline cervico-lumbar spinal cord after stimulation of vanilloid receptors in dorsal neck muscles. Neurosci. Lett., 364, 94 97.
40. Kaube, H., Keay, K.A., Hoskin, K.L., Bandler, R. Goadsby, P.J. (1993) Expression of c-Fos-like immunoreactivity in the caudal medulla and upper cervical spinal cord following stimulation of the superior sagittal sinus in the cat. Brain Res., 629, 95 102.
41. Kerr, F.W.L. (1972) Central relationships of trigeminal and cervical primary afferents in the spinal cord and medulla. Brain Res., 43, 561 572.
42. Levy, D. Strassman, A.M. (2002) Mechanical response properties of A and C primary afferent neurons innervating the rat intracranial dura. J. Neurophysiol., 88, 3021 3031.
43. Lu, J., Hathaway, C.B. Bereiter, D.A. (1993) Adrenalectomy enhances Fos-like immunoreactivity within the spinal trigeminal nucleus induced by noxious thermal stimulation of the cornea. Neuroscience, 54, 809 818.
44. Malick, A., Strassman, A.M. Burstein, R. (2000) Trigeminohypothalamic and reticulohypothalamic tract neurons in the upper cervical spinal cord and caudal medulla of the rat. J. Neurophysiol., 84, 2078 2112.
45. Mardia, K.V., Kent, J.T. Bibby, J.M. (1979) Multivariate analysis. In Birnbaum, Z.W. Lukacs, E. (Eds), Probability and Mathematical Statistics. Academic Press, London.
46. Martin, J.A. (1996) Neuroanatomy. Appleton & Lange, Stamford.
47. Meng, I.D. Bereiter, D.A. (1996) Differential distribution of Fos-like immunoreactivity in the spinal trigeminal nucleus after noxious and innocuous thermal and chemical stimulation of rat cornea. Neuroscience, 72, 243 254.
48. Meng, I.D., Hu, J.W., Benetti, A.P. Bereiter, D.A. (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. Neurophysiol., 77, 43 56.
49. Molander, C., Xu, Q., Riveromelian, C. Grant, G. (1989) Cytoarchitectonic organization of the spinal-cord in the rat. 2. The cervical and upper thoracic cord. J. Comp. Neurol., 289, 375 385.
50. Mørch, C.D., Sessle, B.J., Arendt-Nielsen, L. Hu, J.W. (2004) Convergence of cutaneous, visceral and muscle afferents onto nociceptive dorsal horn neurons at the level of the medullary/spinal cord junction. Abstract Viewer/Itinerary Planner. Program no. 293.9. Society for Neuroscience, Washington, DC.
51. Ness, T.J., Follett, K.A., Piper, J. Dirks, B.A. (1998) Characterization of neurons in the area of the medullary lateral reticular nucleus responsive to noxious visceral and cutaneous stimuli. Brain Res., 802, 163 174.
52. Nomura, S. Mizuno, N. (1983) Central distribution of efferent and afferent components of the cervical branches of the vagus nerve. Anat. Embryol., 166, 1 18.
53. Ota, K., Yanagidani, T., Kishikawa, K., Yamamori, Y. Collins, J.G. (1998) Cutaneous responsiveness of lumbar spinal dorsal horn neurons is reduced by general anesthesia, an effect dependent in part on GABAA mechanisms. J. Neurophysiol., 80, 1383 1390.
54. Pfaller, K. Arvidsson, J. (1988) Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J. Comp. Neurol., 268, 91 108.
55. Piovesan, E.J., Kowacs, P.A., Tatsui, C.E., Lange, M.C., Ribas, L.C. Werneck, L.C. (2001) Referred pain after painful stimulation of the greater occipital nerve in humans: evidence of convergence of cervical afferences on trigeminal nuclei. Cephalalgia, 21, 107 109.
56. Piovesan, E., Kowacs, P. Oshinsky, M. (2003) Convergence of cervical and trigeminal sensory afferents. Curr. Pain Headache Rep., 7, 377 383.
57. Price, D.D., Dubner, R. Hu, J.W. (1976) Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal, and nociceptive stimulation of monkey's face. J. Neurophysiol., 39, 936 953.
58. Qin, C., Chandler, M.J., Miller, K.E. Foreman, R.D. (2001) Responses and afferent pathways of superficial and deeper C1-C2 spinal cells to intrapericardial algogenic chemicals in rats. J. Neurophysiol., 85, 1522 1532.
59. Qin, C., Chandler, M.J., Jou, C.J. Foreman, R.D. (2004) Responses and afferent pathways of C1-C2 spinal neurons to cervical and thoracic esophageal stimulation in rats. J. Neurophysiol., 91, 2227 2235.
60. Ralston, H.J. (1968) Fine structure of neurons in dorsal horn of cat spinal cord. J. Comp. Neurol., 132, 275 301.
61. Razook, J.C., Chandler, M.J. Foreman, R.D. (1995) Phrenic afferent input excites C1-C2 spinal neurons in rats. Pain, 63, 117 125.
62. Renehan, W.E., Jacquin, M.F., Mooney, R.D. Rhoades, R.W. (1986) Structure-function relationships in rat medullary and cervical dorsal horns. II. Medullary dorsal horn cells. J. Neurophysiol., 55, 1187 1201.
63. Sessle, B.J. (1999) The neural basis of temporomandibular joint and masticatory muscle pain. J. Orofacial Pain, 13, 238 245.
64. Sessle, B.J. (2000) Acute and chronic craniofacial pain: Brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit. Rev. Oral Biol. Med., 11, 57 91.
65. Sessle, B.J., Hu, J.W., Amano, N. Zhong, G. (1986) Convergence of cutaneous, tooth pulp, visceral, neck and muscle afferents onto nociceptive and non-nociceptive neurones in trigeminal subnucleus caudalis (medullary dorsal horn) and its implications for referred pain. Pain, 27, 219 235.
66. Shigenaga, Y., Chen, I.C., Suemune, S., Nishimori, T., Nasution, I.D., Yoshida, A., Sato, H., Okamoto, T., Sera, M. Hosoi, M. (1986) Oral and facial representation within the medullary and upper cervical dorsal horns in the cat. J. Comp. Neurol., 243, 388 408.
67. Shigenaga, Y., Sera, M., Nishimori, T., Suemune, S., Nishimura, M., Yoshida, A. Tsuru, K. (1988) The central projection of masticatory afferent-fibers to the trigeminal sensory nuclear-complex and upper cervical spinal-cord. J. Comp. Neurol., 268, 489 507.
68. Smith, M.V., Apkarian, A.V. Hodge, C.J. Jr. (1991) Somatosensory response properties of contralaterally projecting spinothalamic and nonspinothalamic neurons in the second cervical segment of the cat. J. Neurophysiol., 66, 83 102.
69. Strassman, A.M. Vos, B.P. (1993) Somatotopic and laminar organization of Fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J. Comp. Neurol., 331, 495 516.
70. Strassman, A.M., Mineta, Y. Vos, B.P. (1994) Distribution of Fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood-vessels in the rat. J. Neurosci., 14, 3725 3735.
71. Tsai, C.-M., Chiang, C.Y., Yu, X.-M. Sessle, B.J. (1999) Involvement of trigeminal subnucleus caudalis (medullary dorsal horn) in craniofacial nociceptive reflex activity. Pain, 81, 115 128.
72. 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. Pain, 67, 231 240.
73. Yamamura, H., Malick, A., Chamberlin, N.L. Burstein, R. (1999) Cardiovascular and neuronal responses to head stimulation reflect central sensitization and cutaneous allodynia in a rat model of migraine. J. Neurophysiol., 81, 479 493.
74. Yanagidani, T., Ota, K. Collins, J.G. (1998) Complex effects of general anesthesia on sensory processing in the spinal dorsal horn. Brain Res., 812, 301 304.
75. Yezierski, R.P. Broton, J.G. (1991) Functional properties of spinomesencephalic tract (SMT) cells in the upper cervical spinal cord of the cat. Pain, 45, 187 196.
76. Yu, X.-M., Sessle, B.J., Haas, D.A., Izzo, A., Vernon, H. Hu, J.W. (1996) Involvement of NMDA receptor mechanisms in jaw electromyographic activity and plasma extravasation induced by inflammatory irritant application to temporomandibular joint region of rats. Pain, 68, 169 178.
77. Zhou, Q.Q., Imbe, H., Dubner, R. Ren, K. (1999) Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: Implications for persistent orofacial pain. J. Comp. Neurol., 412, 276 291.