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

Experimental Brain Research

Volumn 126, Issue 3, 1999, Pages 383-398

  Benoist, J M ^a,b   Gautron, Michèle ^a   Guilbaud, Gisèle ^a  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cortical pad vibrissa area; Neurone recordings; Rat chronic infraorbital nerve constriction

Indexed keywords

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DEAFFERENTATION; ELECTROPHYSIOLOGY; INFRAORBITAL NERVE; LIGATION; MALE; NERVE CONDUCTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; SOMATOSENSORY SYSTEM; STIMULUS RESPONSE; TRIGEMINAL NERVE; VIBRISSA;

ANIMALS; ELECTROPHYSIOLOGY; MALE; NERVE COMPRESSION SYNDROMES; NERVOUS SYSTEM PHYSIOLOGY; NEURONS, AFFERENT; ORBIT; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; TRIGEMINAL NEURALGIA; VIBRISSAE;

EID: 0032969893     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s002210050745     Document Type: Article

References (95)

1. Albe-Fessard D, Stutinsky F, Libouban S (1971) Atlas stéréotaxique du diencéphale du rat blanc. CNRS (Editions du Centre National de la Recherche Scientifique), Paris
2. Armstrong-James M, Callahan CA (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
3. Armstrong-James M, Fox K (1987) Spatiotemporal convergence and divergence in the rat S1 'barrel' cortex. J Comp Neurol 263:265-281
4. Armstrong-James M, George MJ (1988a) Bilateral receptive fields of cells in rat Sm1 cortex. Exp Brain Res 70:155-165
5. Armstrong-James M, George MJ (1988b) Influence of anesthesia on spontaneous activity and receptive field size of single units in rat Sm1 neocortex. Exp Neurol 99:369-387
6. Armstrong-James M, Callahan CA, Friedman MA (1991) Thalamo-cortical processing of vibrissal information in the rat. I. Intracortical origins of surround but not centre-receptive fields of layer IV neurones in the rat S1 barrel field cortex. J Comp Neurol 303:193-210
7. Armstrong-James M, Fox K, Das-Gupta A (1992) Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol 68:1345-1358
8. Arvidsson J, Johansson K (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
9. Attal N, Jazat F, Kayser V, Guilbaud G (1990) Further evidence for 'pain-related' behaviours in a model of unilateral peripheral mononeuropathy. Pain 41:235-251
10. Belford GR, Killackey HP, Chiaia NL, Rhoades RW (1987) Response characteristics and morphology of vibrissa-sensitive neurons in the ventral posteromedial, thalamic reticular and posterior nuclei of the rat. Soc Neurosci Abstr 13:984
11. Bennett GJ, Xie YK (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107
12. Benoist JM, Kayser V, Gautron M, Guilbaud G (1984) Letter to editor. Pain 18:410-411
13. Benoist JM, Gautron M, Guilbaud G (1997) Alteration of neuronal activity in the cortical projection area of the pad vibrissae in rats with pain-related behaviors from the trigeminal area. In: Jensen TS, Turner JA, Wiesenfield-Hallin Z (eds) Proceedings of the 8th world congress on pain, progress in pain research and management, vol VIII. IASP Press, Seattle, pp 561-573
14. Bouhassira D (1997) Névralgie du trijumeau et douleurs faciales atypiques. In: Brasseur L, Chauvin M, Guilbaud G (eds) Douleurs. Maloine, Paris, pp 475-492
15. Cameron AA, Cliffer KD, Dougherty PM, Garrison CJ, Willis WD, Carlton SM (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
16. Carlton SM, Dougherty PM, Pover CM, Coggeshall RE (1991) Neuroma formation and numbers of axons in a rat model of experimental peripheral neuropathy. Neurosci Lett 131:88-92
17. Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10:2638-2648
18. Chapin JK (1986) Laminar differences in sizes, shapes, and response profiles of cutaneous receptive fields in the rat S1 cortex. Exp Brain Res 62:549-559
19. Chapin JK, Lin CS (1984) Mapping the body representation in the S1 cortex of anesthetized and awake rats. J Comp Neurol 229:199-213
20. Chapin JK, Waterhouse BD, Woodward DJ (1981) Differences in cutaneous sensory response properties of single somatosensory cortical neurones in awake and halothane anesthetized rats. Brain Res Bull 6:63-70
21. Chiaia NL, Rhoades RW, Bennett-Clarke CA, Fish SE, Killackey HP (1991) 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
22. Chmielowska J, Carvell GE, Simons DJ (1989) Spatial organization of thalamocortical and corticothalamic projection systems in the rat Sm1 barrel cortex. J Comp Neurol 285:325-338
23. Coggeshall RE, Dougherty PM, Pover CM, Carlton SM (1993) Is large myelinated fiber loss associated with hyperalgesia in a model of experimental peripheral neuropathy in the rat? Pain 52:233-242
24. Dawson DR, Killackey HP (1987) The organization and mutability of the forepaw and hindpaw representations in the somatosensory cortex of the neonatal rat. J Comp Neurol 256:246-256
25. Diamond ME (1995) Somatosensory thalamus of the rat. In: Jones EG, Diamond IT (eds) Cerebral cortex, vol 11. Plenum Press, New York, pp 189-219
26. Dykes RW, Lamour Y (1988) An electrophysiological study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis. J Neurophysiol 60:703-724
27. Elliot T, Howarth CI, Shadbolt NR (1996) Axonal processes and neural plasticity. II: adult somatosensory maps. Cereb Cortex 6:789-793
28. Gardner WJ, Miklos MV (1959) Response of trigeminal neuralgia to "decompression" of sensory root: discussion of cause of trigeminal neuralgia. J Am Med Assoc 170:1773-1776
29. Gautron M, Jazat F, Ratinahirana H, Hauw JJ, Guilbaud G (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
30. Guilbaud G, Benoist JM (1994) Central transmission of somatosensory inputs in the thalamic ventrobasal complex and somatosensory cortex in rat models of clinical pain. In: Boivie J, Hansson P, Lindblom U (eds) Touch, temperature, and pain in health and disease: mechanisms and assessments, progress in pain research and management, vol III. IASP Press, Seattle, pp 339-354
31. Guilbaud G, Benoist JM (1995) Thalamic and cortical processing in rat models of clinical pain. In: Besson JM, Guilbaud G, Ollat H (eds) Forebrain areas involved in pain processing. John Libbey Eurotext, Paris, pp 79-92
32. Guilbaud G, Peschanski M, Gautron M, Binder D (1980) Neurones responding to noxious stimulation in VB complex and caudal adjacent regions in the thalamus of the rat. Pain 8:303-318
33. Guilbaud G, Peschanski M, Besson JM (1984) Experimental data related to nociception and pain at the supraspinal level. In: Wall PD, Melzack R (eds) Textbook of pain. Churchill Livingstone, Edinburgh, pp 110-118
34. Guilbaud, G, Benoist JM, Jazat F, Gautron M (1990) Neuronal responsiveness in the ventrobasal thalamic complex of rats with an experimental peripheral mononeuropathy. J Neurophysiol 64:1537-1554
35. Guilbaud G, Benoist JM, Levante A, Gautron M, Willer JC (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
36. Guilbaud G, Gautron M, Jazat F, Ratinahirana H, Hassig R, Hauw JJ (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
37. Hendry SHC, Jones EG (1986) Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320:750-753
38. Hoeflinger BF, Bennett-Clarke CA, Chiaia NL, Killackey HP, Rhoades RW (1995) Patterning of local intracortical projections within the vibrissae representation of rat primary somatosensory cortex. J Comp Neurol 354:551-563
39. Idänpään-Heikkilä J, Guilbaud G (1999) Pharmacological studies on a rat model of trigeminal pain - baclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behaviour. Pain 79:281-290
40. Ito M (1985) Processing of vibrissa sensory information within the rat neocortex. J Neurophysiol 54:479-490
41. Ivy GO, Gould HJ, Killackey HP (1984) Variability in the distribution of callosal projection neurons in the adult rat parietal cortex. Brain Res 306:53-61
42. Jablonska B, Gierdalski M, Siucinska E, Skangiel-Kramska J, Kossut M (1995) Partial blocking of NMDA receptors restricts plastic changes in adult mouse barrel cortex. Behav Brain Res 66:207-216
43. Jacquin MF (1989) Structure-function relationships in rat brainstem subnucleus interpolaris: V. functional consequences of neonatal infraorbital nerve section. J Comp Neurol 282:63-79
44. Jacquin MF, Renehan WE, Mooney RD, Rhoades RW (1986) Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. J Neurophysiol 55:1153-1186
45. Jacquin MF, Chiaia NL, Rhoades RW (1990) Trigeminal projections to contralateral dorsal horn: central extent, peripheral origins, and plasticity. Somatosens Mot Res 7:153-183
46. Jannetta PJ (1967) Arterial compression of the trigeminal nerve at the pons in patients with trigeminal neuralgia. J Neurosurg 26:159-162
47. Jannetta PJ (1993) Vascular compression is the cause of trigeminal neuralgia. Am Pain Soc J 2:217-227
48. Jensen KF, Killackey HP (1987) Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J Neurosci 7:3529-3543
49. Kaas JH (1991) Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 14:137-167
50. 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. Neuroscience 32:153-167
51. Killackey HP, Leshlin S (1975) The organization of specific thalamocortical projections to the posteromedial barrel subfield of the rat somatic sensory cortex. Brain Res 86:469-472
52. Killackey HP, Shinder A (1981) Central correlates of peripheral pattern alterations in the trigeminal system of the rat. II. The effect of nerve section. Dev Brain Res 1:121-126
53. Killackey HP, Belford G, Ryugo R, Ryugo DK (1976) Anomalous organization of thalamocortical projections consequent to vibrissae removal in the newborn rat and mouse. Brain Res 104:309-315
54. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363
55. Klein BG (1991) Chronic functional consequences of adult infraorbital nerve transection for rat trigeminal subnucleus interpolaris. Somatosens Mot Res 8:175-191
56. Koerber HR, Mirnics K, Brown PB, Mendell LM (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655-3671
57. Koralek KA, Jensen KF, Killackey HP (1988) Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex. Brain Res 463:346-351
58. Kossut M (1992) Plasticity of the barrel cortex neurons. Prog Neurobiol 39:389-422
59. Kossut M, Stewart MG, Siucinska E, Bourne RC, Gabbot PLA (1991) Loss of γ-aminobutyric acid (GABA) immunoreactivity from mouse first somatosensory cortex following neonatal, but not adult, denervation. Brain Res 538:165-170
60. Lamour Y, Willer JC, Guilbaud G (1983a) Rat somatosensory SmI cortex: I. characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation. Exp Brain Res 49:35-45
61. Lamour Y, Guilbaud G, Willer JC (1983b) Rat somatosensory Sm1 cortex: II. Laminar and columnar organization of noxious and non-noxious inputs. Exp Brain Res 49:46-54
62. A receptors in rat somatosensory cortex and effects of tactile deprivation. Somatosens Mot Res 12:127-141
63. Lekan HA, Carlton SM, Coggeshall RE (1996) Sprouting of Aβ fibers into lamina II of the rat dorsal horn in peripheral neuropathy. Neurosci Lett 208:147-150
64. Mantle-St John LA, Tracey DJ (1987) Somatosensory nuclei in the brainstem of the rat: independent projections to the thalamus and cerebellum. J Comp Neurol 255:259-271
65. Munger BL, Renehan WE (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
66. Munger BL, Bennett GA, Vos BP (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
67. Nuytten D, Kupers R, Lammens M, Dom R, Van Hees J, Gybels J (1992) Further evidence for myelinated as well as unmyelinated fibre damage in a rat model of neuropathic pain. Exp Brain Res 91:73-78
68. Olavarria J, Van Sluyters RC, Killackey HP (1984) Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res 291:364-368
69. Peschanski M (1984) Trigeminal afferents to the diencephalon in the rat. Neuroscience 12:465-487
70. Pidoux B, Verley R (1979) Projections on the cortical somatic I barrel subfield from ipsilateral vibrissae in adult rodents. Electroenceph Clin Neurophysiol 46:715-726
71. Renehan WE, Munger BL (1986) Degeneration and regeneration of peripheral nerve in the rat trigeminal system: II. response to nerve lesions. J Comp Neurol 249:429-459
72. Renehan WE, Jacquin MF, Mooney RD, Rhoades RW (1986) Structure-function relationships in rat medullary and cervical dorsal horns. II. Medullary dorsal horn cells. J Neurophysiol 55:1187-1201
73. Renehan WE, Klein BG, Chiaia NL, Jacquin MF, Rhoades RW (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
74. Renehan WE, Crissman RS, Jacquin MF (1994) Primary afferent plasticity following partial denervation of the trigeminal brainstem nuclear complex in the postnatal rat. J Neurosci 14:721-739
75. Rhoades RW, Crissman RS, Bennett-Clarke CA, Killackey HP, Chiaia NL (1996) Development and plasticity of local intracortical projections within the vibrissae representation of the rat primary somatosensory cortex. J Comp Neurol 370:524-535
76. Riddle DR, Purves D (1995) Individual variation and lateral asymmetry of the rat primary somatosensory cortex. J Neurosci 15:4184-4195
77. Seltzer Z, Dubner R, Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by a partial sciatic nerve injury. Pain 43:205-218
78. Shipley MT (1974) Response characteristics of single units in the rats's trigeminal nuclei to vibrissae displacements. J Neurophysiol 37:73-90
79. Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41:798-820
80. Simons DJ (1985) Temporal and spatial integration in the rat SI vibrissa cortex. J Neurophysiol 54:615-635
81. Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61: 311-330
82. 3H]muscimol in the barrel field of mice after peripheral denervation: transient and long-lasting effects. Exp Brain Res 100:39-46
83. Vos BP, Strassman AM (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
84. Vos BP, Gautron M, Benoist JM, Guilbaud G (1994a) Responses of ventral posteromedial thalamic nucleus neurons after chronic constriction injury to the rat infraorbital nerve. Soc Neurosci Abstr 20:1572
85. Vos BP, Strassman AM, Maciewicz RJ (1994b) Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci 14:2708-2723
86. Waite PME (1984) Rearrangement of neuronal responses in the trigeminal system of the rat following peripheral nerve section. J Physiol 352:425-445
87. Welker C (1971) Microelectrode delineation of fine grain somatotopic organization of SM1 cerebral neocortex in albino rat. Brain Res 26:259-275
88. Welker C (1976) Receptive fields of barrels in the somatosensory neocortex of the rat J Comp Neurol 166:173-190
89. Welker C, Woolsey TA (1974) Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J Comp Neurol 158:437-454
90. Welker E, Soriano E, Van der Loos H (1989) Plasticity in the barrel cortex of the adult mouse: effects of peripheral deprivation on GAD-immunoreactivity. Exp Brain Res 74:441-452
91. Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75-78
92. Woolsey TA, Van Der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex: the description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242
93. Woolston DC., La Londe JR, Gibson JM (1982) Comparison of response properties of cerebellar-and thalamic-projecting interpolaris neurons. J Neurophysiol 48:160-173
94. Zafra F, Castrén E, Thoenen H, Lindholm D (1991) Interplay between glutamate and γ-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc Natl Acad Sci U S A 88:10037-10041
95. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110