Changes in neuronal activities in the two ventral posterior medial thalamic nuclei in an experimental model of trigeminal pain in the rat by constriction of one infraorbital nerve

Somatosensory and Motor Research

Volumn 17, Issue 2, 2000, Pages 109-122

  Vos, Bart P ^a,c   Benoist, Jean Michel ^a,b   Gautron, Michele ^a   Guilbaud, Gisele ^a  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

New on recordings; Rat chronic infraorbital nerve constriction; Ventral posterior medial thalmic nucleus

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; INFRAORBITAL NERVE; MALE; MECHANICAL STIMULATION; NERVE COMPRESSION; NERVE CONDUCTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; THALAMUS NUCLEUS; TRIGEMINAL NERVE; VIBRISSA;

EID: 0034034375     PISSN: 08990220     EISSN: None     Source Type: Journal    
DOI: 10.1080/08990220050020535     Document Type: Article

References (92)

1. ALBE-FESSARD, D., F. STUTINSKY, and S. LIBOUBAN (1971) Atlas stéréotaxique du diencéphak du rat blanc, CNRS (Editions du Centre National de la Recherche Scientifique), Paris.
2. AMIR, R., and M. DEVOR (1992) Axonal cross-excitation in nerve-end neuromas: comparison of A- and C-fibers. J Neurophysiol 68: 1160-1166.
3. AMIR, R., and M. DEVOR (1996) Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci 16: 4733-4741.
4. ARMSTRONG-JAMES, M., and C.A. CALLAHAN (1991) Thalamo-cortical processing of vibrissal information in the rat. II. Spatiotemporal convergence in the thalamic ventroposterior medial nucleus (VPm) and its relevance to generation of receptive fields of S1 cortical 'barrel' neurones. J Comp Neurol 303: 211-224.
5. ARVIDSSON, J., and K. JOHANSSON (1988) Changes in the central projection pattern of vibrissae innervating primary sensory neurons after a peripheral nerve injury in the rat. Neurosci Lett 84: 120-124.
6. ATTAL, N., G. FILLIATREAU, S. PERROT, F. JAZAT, L. DI GIAMBERARDINO, and G. GUILBAUD (1994) Behavioural pain-related disorders and contribution of the saphenous nerve in crush and chronic constriction injury of the rat sciatic nerve. Pain 59: 301-312.
7. ATTAL, N., F. JAZAT,V. KAYSER, and G. GUILBAUD (1990) Further evidence for 'pain-related' behaviours in a model of unilateral peripheral mononeuropathy. Pain 41: 235-251.
8. BENNETT, G.J. (1994) Animal models of neuropathic pain. In Proceedings of the 7th World Congress on Pain, Progress in Pain Research and Management, Vol. 2, G.F. GEBHART, D.L. HAMMOND, and T.S. JENSEN, eds., pp. 495-510, IASP Press, Seattle.
9. BENNETT, G.J., and Y.K. XIE (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33: 87-107.
10. BENOIST, J.M., M. GAUTRON, and G. GUILBAUD (1999) Experimental model of trigeminal pain in the rat by constriction of one infraorbital nerve: changes in neuronal activities in the somatosensory cortices corresponding to the infraorbital nerve. Exp Brain Res 126: 383-398.
11. BENOIST, J.M., V. KAYSER, M. GAUTRON, and G. GUILBAUD (1984) Letter to Editor. Pain 18: 410-411.
12. BOUHASSIRA, D. (1997) Névralgie du trijumeau et douleurs faciales atypiques. In Douleurs, L. BRASSEUR, M. CHAUVIN, and G. GUILBAUD, eds., pp. 475-492, Maloine, Paris.
13. CAMERON, A.A., K.D. CLIFFER, P.M. DOUGHERTY, C.J. GARRISON, W.D. WILLIS, and S.M. CARLTON (1997) Time course of degenerative and regenerative changes in the dorsal horn in a rat model of peripheral neuropathy. J Comp Neurol 379: 428-442.
14. CARLTON, S.M., P.M. DOUGHERTY, C.M. POVER, and R.E. COGGESHALL (1991) Neuroma formation and numbers of axons in a rat model of experimental peripheral neuropathy. Neurosci Lett 131: 88-92.
15. CARVELL, G.E., and D.J. SIMONS (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638-2648.
16. CHIAIA, N.L., R.W. RHOADES, C.A. BENNETT-CLARKE, S.E. FISH, and H.P. KILLACKEY (1991a) Thalamic processing of vibrissal information in the rat: I. Afferent input to the medial ventral posterior and posterior nuclei. J Comp Neurol 314: 201-216.
17. CHIAIA, N.L., R.W. RHOADES, S.E. FISH, and H.P. KILLACKEY (1991b) Thalamic processing of vibrissal information in the rat: II. Morphological and functional properties of medial ventral posterior nucleus and posterior nucleus neurons. J Comp Neurol 314: 217-236.
18. CHMIELOWSKA, J., G.E. CARVELL, and D.J. SIMONS (1989) Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J Comp Neurol 285: 325-338.
19. CHRISTENSEN, D., M. GAUTRON, G. GUILBAUD, and V. KAYSER (1999) Combined systemic administration of the glycine/NMDA receptor antagonist, (+)-HA966 and morphine attenuates pain-related behaviour in a rat model of trigeminal neuropathic pain. Pain 83: 433-440.
20. COGGESHALL, R.E., P.M. DOUGHERTY, C.M. POVER, and S.M. CARLTON (1993) Is large myelinated fiber loss associated with hyperalgesia in a model of experimental peripheral neuropathy in the rat? Pain 52: 233-242.
21. DEVOR, M. (1994) The pathophysiology of damaged peripheral nerves. InTextbook of Pain, 3rd ed, P.D. WALL, and R. MELZACK, eds., pp. 79-100, Churchill Livingstone, London.
22. DEVOR, M., and P.D. WALL (1990) Cross-excitation in dorsal root ganglia of nerve-injured and intact rats. J Neurophysiol 64: 1733-1746.
23. DIAMOND, M.E., M. ARMSTRONG-JAMES, and F.F. EBNER (1992) Somatic sensory responses in the rostral sector of the posterior group (Pom) and in the ventral posterior medial nucleus (VPM) of the rat thalamus. J Comp Neurol 318: 462-476.
24. ERZURUMLU, R.S., and H.P. KILLACKEY (1980) Diencephalic projections of the subnucleus interpolaris of the brainstem trigeminal complex in the rat. Neuroscience 5: 1891-1901.
25. FELDMAN, S.G., and L. KRUGER (1980) An axonal transport study of the ascending projection of medial lemniscal neurons in the rat. J Comp Neurol 192: 427-454.
26. FROMM, G.H., C.F. TERRENCE, and J.C. MAROON (1984) Trigeminal neuralgia. Current concepts regarding etiology and pathogenesis. Arch Neurol 41: 1204-1207.
27. FUKUSHIMA, T., and F.W.L. KERR (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 Neurol 183: 169-184.
28. GAUTRON, M., F. JAZAT, H. RATINAHIRANA, J.J. HAUW, and G. GUILBAUD (1990) Alterations in myelinated fibres in the sciatic nerve of rats after constriction: possible relationships between the presence of abnormal small myelinated fibres and pain-related behaviour. Neurosci Lett 111: 28-33.
29. GUILBAUD, G., and J.M. BENOIST (1995) Thalamic and cortical processing in rat models of clinical pain. In Forebrain Areas involved in Pain Processing, J.M. BESSON, G. GUILBAUD, and H. OLLAT, eds., pp. 79-92, John Libbey Eurotext, Paris.
30. GUILBAUD, G., J.M. BENOIST, F. JAZAT, and M. GAUTRON (1990) Neuronal responsiveness in the ventrobasal thalamic complex of rats with an experimental peripheral mononeuropathy. J Neurophysiol 64: 1537-1554.
31. GUILBAUD, G., J.M. BENOIST, A. LEVANTE, M. GAUTRON, and J.C. WILLER (1992) Primary somatosensory cortex in rats with pain-related behaviours due to a peripheral mononeuropathy after moderate ligation of one sciatic nerve: neuronal responsiveness to somatic stimulation. Exp Brain Res 92: 227-245.
32. GUILBAUD, G., M. GAUTRON, F. JAZAT, H. RATINAHIRANA, R. HASSIG, and J.J. HAUW (1993) Time course of degeneration and regeneration of myelinated nerve fibres following chronic loose ligatures of the rat sciatic nerve: can nerve lesions be linked to the abnormal pain-related behaviours? Pain 53: 147-158.
33. GUILBAUD, G., M. PESCHANSKI, M. GAUTRON, and D. BINDER (1980) Neurones responding to noxious stimulation in VB complex and caudal adjacent regions in the thalamus of the rat. Pain 8: 303-318.
34. GYBELS, J.M., and W.H. SWEET (1989) Neurosurgical treatment of persisting pain. Physiological and pathological mechanisms of human pain. In Pain and Headache, Vol. 11, 442 pp., Karger, Basel.
35. IBUKI, T., A.T. HAMA, X.T. WANG, G.D. PAPPAS, and J. SAGEN (1997) Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 76: 845-858.
36. IDANPÄÄN-HEIKKILÄ, J., and G. GUILBAUD (1999) Pharmacological studies on a rat model of trigeminal painbaclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behaviour. Pain 79: 281-290.
37. IMAMURA, Y., H. KAWAMOTO, and O. NAKANISHI (1997) Characterization of heat-hyperalgesia in an experimental trigeminal neuropathy in rats. Exp Brain Res 116: 97-103.
38. ITO, M. (1988) Response properties and topography of vibrissa-sensitive VPM neurons in the rat. J Neurophysiol 60: 1181-1197.
39. IWATA, K., D.R. KENSHALO, R. DUBNER, and R.L. NAHIN (1992) Diencephalic projections from the superficial and deep laminae of the medullary dorsal horn in the rat. J Comp Neurol 321: 404-420.
40. JACQUIN, M.F. (1989) Structure-function relationships in rat brainstem subnucleus interpolaris: V. Functional consequences of neonatal infraorbital nerve section. J Comp Neurol 282: 63-79.
41. JACQUIN, M.F., N.L. CHIAIA, and R.W. RHOADES (1990) Trigeminal projections to contralateral dorsal horn: Central extent, peripheral origins, and plasticity. Somatosens Mot Res 7: 153-183.
42. KAJANDER, K.C., and G.J. BENNETT (1992) Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in Aβ and Aδ primary afferent neurons. J Neurophysiol 68: 734-744.
43. KAJANDER, K.C., S. WAKISAKA, and G.J. BENNETT (1992) Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat. Neurosci Lett 138: 225-228.
44. KEMPLAY, S., and K.E. WEBSTER (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. Neuroscience 32: 153-167.
45. KERR, F.W.L. (1967) Evidence for a peripheral etiology of trigeminal neuralgia. J Neurosurg 26: 168-174.
46. KIM, S.H., and J.M. CHUNG (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50: 355-363.
47. KLEIN, B.G. (1991) Chronic functional consequences of adult infraorbital nerve transection for rat trigeminal subnucleus interpolaris. Somatosens Mot Res 8: 175-191.
48. KLEIN, B.G., C.F. WHITE, and J.R. DUFFIN (1998) Rapid shifts in receptive fields of cells in trigeminal subnucleus interpolaris following infraorbital nerve transection in adult rats. Brain Res 779: 136-148.
49. KOERBER, H.R., K. MIRNICS, P.B. BROWN, and L.M. MENDELL (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14: 3655-3671.
50. LAIRD, J.M.A., and G.J. BENNETT (1992) Dorsal root potentials and afferent input to the spinal cord in rats with an experimental peripheral neuropathy. Brain Res 584: 181-190.
51. LEE, S.M., M.H. FRIEDBERG, and F.F. EBNER (1994a)The role of GABA-mediated inhibition in the rat ventral posterior medial thalamus. I. Assessment of receptive field changes following thalamic reticular nucleus lesions. J Neurophysiol 71: 1702-1715.
52. B receptor antagonists on responses of VPM neurons. J Neurophysiol 71: 1716-1726.
53. LEKAN, H.A., S.M. CARLTON, and R.E. COGGESHALL (1996) Sprouting of Aβ fibers into lamina II of the rat dorsal horn in peripheral neuropathy. Neurosci Lett 208: 147-150.
54. LUND, R.D., and K.E. WEBSTER (1967) Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. J Comp Neurol 130: 313-328.
55. MANTLE-ST JOHN, L.A., and D.J. TRACEY (1987) Somatosensory nuclei in the brainstem of the rat: Independent projections to the thalamus and cerebellum. J Comp Neurol 255: 259-271.
56. MUNGER, B.L., G.J. BENNETT, and K.C. KAJANDER (1992) An experimental painful peripheral neuropathy due to nerve constriction I. Axonal pathology in the sciatic nerve. Exp Neurol 118: 204-214.
57. MUNGER, B.L., G.B. BENNETT, and B.P. VOS (1996) Abnormal sensory reinnervation of mystacial guard hairs in long term chronic constrictive injury (CCI) of the infraorbital nerve (IoN) in rats. Soc Neurosci Abstr 22: 1487.
58. MUNGER, B.L., and W.E. RENEHAN (1989) Degeneration and regeneration of peripheral nerve in the rat trigeminal system: III. Abnormal sensory reinnervation of rat guard hairs following nerve transection and crush. J Comp Neurol 283: 169-176.
59. NICOLELIS, M.A.L., and J.K. CHAPIN (1994) Spatio-temporal structure of somatosensory responses of many-neuron ensembles in the rat ventral posterior medial nucleus of the thalamus. J Neurosci 14: 3511-3532.
60. NUYTTEN, D., R. KUPERS, M. LAMMENS, R. DOM, J. VAN HEES, and J. GYBELS (1992) Further evidence for myelinated as well as unmyelinated fibre damage in a rat model of neuropathic pain. Exp Brain Res 91: 73-78.
61. OLAVARRIA, J., R.C. VAN SLUYTERS, and H.P. KILLLACKEY (1984) Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res 291: 364-368.
62. PESCHANSKI, M. (1984) Trigeminal afferents to the diencephalon in the rat. Neuroscience 12: 465-487.
63. RAPPAPORT, Z.H., and M. DEVOR (1994) Trigeminal neuralgia: the role of self-sustaining discharge in the trigeminal ganglion. Pain 56: 127-138.
64. RENEHAN, W.E., M.F. JACQUIN, R.D. MOONEY, and R.W. RHOADES (1986) Structure-function relationships in rat medullary and cervical dorsal horns. II. Medullary dorsal horn cells. J Neurophysiol 55: 1187-1201.
65. RENEHAN, W.E., B.G. KLEIN, N.L. CHIAIA, M.F. JACQUIN, and R.W. RHOADES (1989) Physiological and anatomical consequences of infraorbital nerve transection in the trigeminal ganglion and trigeminal spinal tract of adult rat. J Neurosci 9: 548-557.
66. RENEHAN, W.E., and B.L. MUNGER (1986) Degeneration and regeneration of peripheral nerve in the rat trigeminal system: II. Response to nerve lesions. J Comp Neurol 249: 429-459.
67. RHOADES, R.W., G.R. BELFORD, and H.P. KILLACKEY (1987) Receptive-field properties of rat ventral posteromedial neurons before and after selective kainic acid lesions of the trigeminal brainstem complex. J Neurophysiol 57: 1577-1600.
68. SELTZER, Z., R. DUBNER, and Y. SHIR (1990) A novel behavioral model of neuropathic pain disorders produced in rats by a partial sciatic nerve injury. Pain 43: 205-218.
69. SHERMAN, S.M., and R.W. GUILLERY (1996) Functional organization of thalamocortical relays. J Neurophysiol 76: 1367-1395.
70. SHIGENAGA, Y., M. TAKABATAKE, T. SUGIMOTO, and A. SAKAI (1979) Neurons in marginal layer of trigeminal nucleus caudalis projecting to ventrobasal complex (VB) and posterior nuclear group (PO) demonstrated by retrograde labeling with horseradish peroxidase. Brain Res 166: 391-396.
71. SHIPLEY, M.T. (1974) Response characteristics of single units in the rats's trigeminal nuclei to vibrissae displacements. J Neurophysiol 37: 73-90.
72. SILVERMAN, J.D., and L. KRUGER (1985) Projections of the rat trigeminal sensory nuclear complex demonstrated by multiple fluorescent dye retrograde transport. Brain Res 361: 383-388.
73. SIMONS, D.J., and G.E. CARVELL (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61: 311-330.
74. SMITH, R.L. (1973) The ascending fiber projections from the principal sensory trigeminal nucleus in the rat. J Comp Neurol 148: 423-444.
75. SUGITANI, M., J. YANO, T. SUGAI, and H. OOYAMA (1990) Somatotopic organization and columnar structure of vibrissae representation in the rat ventrobasal complex. Exp Brain Res 81: 346-352.
76. SWEET, W.H. (1985) The history of the development of treatment for trigeminal neuralgia. Clin Neurosurg 32: 294-318.
77. TAL, M., and M. DEVOR (1992) Ectopic discharge in injured nerves: comparison of trigeminal and somatic afferents. Brain Res 579: 148-151.
78. TERRENCE, C.F., and G.H. FROMM (1993) Trigeminal neuralgia and other facial neuralgias. In The Headaches, J. OLESEN, P. TFELT-HANSEN, and M.A. WELCH, eds., pp. 773-785, Raven Press, New York.
79. TOMIE, J., and I.Q. WHISHAW (1990) New paradigms for tactile discrimination studies with the rat: methods for simple, conditional and configurational discriminations. Physiol Behav 48: 225-231.
80. VILLANUEVA, L., D. BOUHASSIRA, and D. LE BARS (1996) The medullary subnucleus reticularis dorsalis (SRD) as a key link in both the transmission and modulation of pain signals. Pain 67: 231-240.
81. VOS, B.P., M. GAUTRON, J.M. BENOIST, and G. GUILBAUD (1994a) Responses of ventral posteromedial thalamic nucleus neurons after chronic constriction injury to the rat's infraorbital nerve. Soc Neurosci Abstr 20: 1572.
82. VOS, B.P., and R.J. MACIEWICZ (1990) Alterations of peripheral nerve morphology and changes in fluoride resistant acid phosphatase and substance P-immunoreactivity in the trigeminal nucleus caudalis in an experimental model of trigeminal neuropathic pain. Am Pain Soc Abstr 9: 56.
83. VOS, B.P., and R.J. MACIEWICZ (1991) Behavioral changes following ligation of the infraorbital nerve in rat: an animal model of trigeminal neuropathic pain. In Lesions of Primary Afferent Fibers as a Tool for the Study of Clinical Pain, J.M. BESSON, and G. GUILBAUD, eds., pp. 147-158, Excerpta Medica, Eisevier, Amsterdam.
84. VOS, B.P., and A.M. STRASSMAN (1995) Fos expression in the medullary dorsal horn of the rat after chronic constriction injury to the infraorbital nerve. J Comp Neurol 357: 362-375.
85. VOS, B.P., A.M. STRASSMAN, and R.J. MACIEWICZ (1994b) Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci 14: 2708-2723.
86. WAITE, P.M.E. (1973) Somatotopic organization of vibrissal responses in the ventro-basal complex of the rat thalamus. J Physiol 228: 527-540.
87. WAITE, P.M.E. (1984) Rearrangement of neuronal responses in the trigeminal system of the rat following peripheral nerve section. J Physiol 352: 425-445.
88. WAITE, P.M.E., and B.G. CRAGG (1982) The peripheral and central changes resulting from cutting or crushing the afferent nerve supply to the whiskers. Proc R Soc Lond B214: 191-211.
89. WOOLF, C.J., P. SHORTLAND, and R.E. COGGESHALL (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355: 75-78.
90. WOOLSTON, D.C., J.R. LA LONDE, and J.M. GIBSON (1982) Comparison of response properties of cerebellar-and thalamic-projecting interpolaris neurons. J Neurophysiol 48: 160-173.
91. XIE, Y.K., and W.H. XIAO (1990) Electrophysiological evidence for hyperalgesia in the peripheral neuropathy. Sci China (Ser B) 33: 663-672.
92. ZIMMERMANN, M. (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110.