Lesion of the dopaminergic nigrostriatal pathway induces trigeminal dynamic mechanical allodynia

Brain and Behavior

Volumn 4, Issue 3, 2014, Pages 368-380

  Dieb, Wisam ^a   Ouachikh, Omar ^a   Durif, Franck ^a,b   Hafidi, Aziz ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

Atypical facial algia; Basal ganglia; Burning mouth syndrome; Orofacial pain; Parkinson disease; Trigeminal subnucleus caudalis (Sp5C)

Indexed keywords

BROMOCRIPTINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE C; SULPIRIDE; MITOGEN ACTIVATED PROTEIN KINASE; OXIDOPAMINE;

ADULT; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN DAMAGE; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MOTOR PERFORMANCE; NEUROPATHIC PAIN; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEAR LAMINA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TRIGEMINAL NERVE; ANIMAL; CHEMICALLY INDUCED; CORPUS STRIATUM; DISEASE MODEL; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; HYPERALGESIA; METABOLISM; NERVE TRACT; PAIN MEASUREMENT; PARKINSON DISEASE; PATHOPHYSIOLOGY; PHOSPHORYLATION; SPRAGUE DAWLEY RAT; STIMULATION; SUBSTANTIA NIGRA; TRIGEMINUS NEURALGIA;

ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HYPERALGESIA; MALE; NEURAL PATHWAYS; OXIDOPAMINE; PAIN MEASUREMENT; PARKINSON DISEASE, SECONDARY; PHOSPHORYLATION; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TRIGEMINAL NEURALGIA;

EID: 84900405611     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.214     Document Type: Article

References (58)

1. Altier, N., and J. Stewart. 1999. The role of dopamine in the nucleus accumbens in analgesia. Life Sci. 65:2269-2287.
2. Alvarez, P., W. Dieb, A. Hafidi, D. L. Voisin, and R. Dallel. 2009. Insular cortex representation of dynamic mechanical allodynia in trigeminal neuropathic rats. Neurobiol. Dis. 33:89-95.
3. Ansah, O. B., H. Leite-Almeida, H. Wei, and A. Pertovaara. 2007. Striatal dopamine D2 receptors attenuate neuropathic hypersensitivity in the rat. Exp. Neurol. 205:536-546.
4. Barceló, A. C., B. Fillipini, and J. H. Pazo. 2010. Study of the neural basis of striatal modulation of the jaw-opening reflex. J. Neural. Transm. 117:171-181.
5. Borsook, D. 2012. Neurological diseases and pain. Brain 135:320-344.
6. Calne, D. B., P. F. Teychenne, P. N. Leigh, A. N. Bamji, and J. K. Greenacre. 1974. Treatment of Parkinsonism with bromocriptine. Lancet 2:1355-1356.
7. Campbell, J. N., S. N. Raja, R. A. Meyer, and S. E. Mackinnon. 1988. Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32:89-94.
8. Cassell, M. D., L. J. Freedman, and C. Shi. 1999. The intrinsic organization of the central extended amygdala. Ann. N. Y. Acad. Sci. 877:217-241.
9. Chassain, C., G. Bielicki, J. P. Donnat, J. P. Renou, A. Eschalier, and F. Durif. 2005. Cerebral glutamate metabolism in Parkinson's disease: an in vivo dynamic (13)C NMS study in the rat. Exp. Neurol. 191:276-284.
10. Chieng, B., and M. J. Christie. 2010. Somatostatin and nociceptin inhibit neurons in the central nucleus of amygdala that project to the periaqueductal grey. Neuropharmacology 59:425-430.
11. Chudler, E. H., and W. K. Dong. 1995. The role of the basal ganglia in nociception and pain. Pain 60:3-38.
12. Chudler, E. H., and Y. Lu. 2008. Nociceptive behavioral responses to chemical, thermal and mechanical stimulation after unilateral, intrastriatal administration of 6-hydroxydopamine. Brain Res. 1213:41-47.
13. Clifford, T. J., M. J. Warsi, C. A. Burnett, and P. J. Lamey. 1998. Burning mouth in Parkinson's disease sufferers. Gerodontology 15:73-78.
14. Cobacho, N., J. L. De la Calle, J. R. González-Escalada, and C. L. Paíno. 2010. Levodopa analgesia in experimental neuropathic pain. Brain Res. Bull. 83:304-309.
15. Dieb, W., and A. Hafidi. 2013. Astrocytes are involved in Trigeminal Dynamic Mechanical Allodynia: potential Role of D-serine. J. Dent. Res. 92:808-813.
16. Fischer, L., C. A. Parada, and C. H. Tambeli. 2005. A novel method for subarachnoid drug delivery in the medullary region of rats. J. Neurosci. Methods 148:108-112.
17. Gauriau, C., and J. F. Bernard. 2002. Pain pathways and parabrachial circuits in the rat. Exp. Physiol. 87:251-258.
18. Goetz, C. G. 2011. The history of Parkinson's disease: early clinical descriptions and neurological therapies. Cold Spring Harb. Perspect. Med. 1(1):a008862.
19. Ha, A. D., and J. Jankovic. 2012. Pain in Parkinson's disease. Mov. Disord. 27:485-491.
20. Hagelberg, N., S. K. Jääskeläinen, I. K. Martikainen, H. Mansikka, H. Forssell, H. Scheinin, et al. 2004. Striatal dopamine D2 receptors in modulation of pain in humans: a review. Eur. J. Pharmacol. 500:187-192.
21. Ji, R. R., H. Baba, G. J. Brenner, and C. J. Woolf. 1999. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat. Neurosci. 2:1114-1119.
22. Kato, G., Y. Kawasaki, K. Koga, D. Uta, M. Kosugi, T. Yasaka, et al. 2009. Organization of intralaminar and translaminar neuronal connectivity in the superficial spinal dorsal horn. J. Neurosci. 29:5088-5099.
23. Koltzenburg, M., H. E. Torebjork, and L. K. Wahren. 1994. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117:579-591.
24. Koszewicz, M., M. Mendak, T. Konopka, E. Koziorowska-Gawron, and S. Budrewicz. 2012. The characteristics of autonomic nervous system disorders in burning mouth syndrome and Parkinson disease. J. Orofac. Pain 26:315-320.
25. Lin, M. T., J. J. Wu, A. Chandra, and B. L. Tsay. 1981. Activation of striatal dopamine receptors induces pain inhibition in rats. J. Neural. Transm. 51:213-222.
26. Magnusson, J. E., and K. Fisher. 2000. The involvement of dopamine in nociception: the role of D (1) and D (2) receptors in the dorsolateral striatum. Brain Res. 855:260-266.
27. Malmberg, A. B., C. Chen, S. Tonegawa, and A. I. Basbaum. 1997. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 278:279-283.
28. Martin, W. J., H. Liu, H. Wang, A. B. Malmberg, and A. I. Basbaum. 1999. Inflammation-induced up-regulation of protein kinase Cgamma immunoreactivity in rat spinal cord correlates with enhanced nociceptive processing. Neuroscience 88:1267-1274.
29. Melo, C. T., A. M. de Carvalho, B. A. Moura, C. P. Teixeira, L. F. Vasconcelos, M. L. Feitosa, et al. 2013. Evidence for the involvement of the serotonergic, noradrenergic, and dopaminergic systems in the antidepressant-like action of riparin III obtained from Aniba riparia (Nees) Mez (Lauraceae) in mice. Fundam. Clin. Pharmacol. 27:104-112.
30. Meshul, C. K., N. Emre, C. M. Nakamura, C. Allen, M. K. Donohue, and J. F. Buckman. 1999. Time-dependent changes in striatal glutamate synapses following a 6-hydroxydopamine lesion. Neuroscience 88:1-16.
31. Michael-Titus, A., R. Bousselmame, and J. Costentin. 1990. Stimulation of dopamine D2 receptors induces an analgesia involving an opioidergic but non enkephalinergic link. Eur. J. Pharmacol. 187:201-207.
32. Miletic, V., K. K. Bowen, and G. Miletic. 2000. Loose ligation of the rat sciatic nerve is accompanied by changes in the subcellular content of protein kinase C beta II and gamma in the spinal dorsal horn. Neurosci. Lett. 288:199-202.
33. Millan, M. J. 2002. Descending control of pain. Prog. Neurobiol. 66:355-474.
34. Miraucourt, L. S., X. Moisset, R. Dallel, and D. L. Voisin. 2009. Glycine inhibitory dysfunction induces a selectively dynamic, morphine-resistant, and neurokinin 1 receptor- independent mechanical allodynia. J. Neurosci. 29:2519-2527.
35. Morgan, M. J., and K. B. Franklin. 1990. 6-Hydroxydopamine lesions of the ventral tegmentum abolish D-amphetamine and morphine analgesia in the formalin test but not in the tail flick test. Brain Res. 519:144-149.
36. Nakajima, A., Y. Tsuboi, I. Suzuki, K. Honda, M. Shinoda, M. Kondo, et al. 2011. PKCgamma in Vc and C1/C2 is involved in trigeminal neuropathic pain. J. Dent. Res. 90:777-781.
37. Ochoa, J. L., and D. Yarnitsky. 1993. Mechanical hyperalgesias in neuropathic pain patients: dynamic and static subtypes. Ann. Neurol. 33:465-472.
38. Ohsawa, M., M. Narita, H. Mizoguchi, E. Cheng, and L. F. Tseng. 2001. Reduced hyperalgesia induced by nerve injury, but not by inflammation in mice lacking protein kinase C gamma isoform. Eur. J. Pharmacol. 429:157-160.
39. Okada-Ogawa, A., I. Suzuki, B. J. Sessle, C. Y. Chiang, M. W. Salter, J. O. Dostrovsky, et al. 2009. Astroglia in medullary dorsal horn (trigeminal spinal subnucleus caudalis) are involved in trigeminal neuropathic pain mechanisms. J. Neurosci. 29:11161-11171.
40. Ouachikh, O., W. Dieb, F. Durif, and A. Hafidi. 2013. Differential behavioral reinforcement effects of dopamine receptor agonists in the rat with bilateral lesion of the posterior ventral tegmental area. Behav. Brain Res. 252:24-31.
41. Paillé, V., V. Henry, L. Lescaudron, P. Brachet, and P. Damier. 2007. Rat model of Parkinson's disease with bilateral motor abnormalities, reversible with levodopa, and dyskinesias. Mov. Disord. 22:533-539.
42. Pertovaara, A., I. K. Martikainen, N. Hagelberg, H. Mansikka, K. Någren, J. Hietala, et al. 2004. Striatal dopamine D2/D3 receptor availability correlates with individual response characteristics to pain. Eur. J. Neurosci. 20:1587-1592.
43. Polgár, E., J. H. Fowler, M. M. McGill, and A. J. Todd. 1999. The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res. 833:71-80.
44. Reyes, S., and J. Mitrofanis. 2008. Patterns of FOS expression in the spinal cord and periaqueductal grey matter of 6OHDA-lesioned rats. Int. J. Neurosci. 118:1053-1079.
45. Rizvi, T. A., M. Ennis, M. M. Behbehani, and M. T. Shipley. 1991. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J. Comp. Neurol. 303:121-131.
46. Saadé, N. E., S. F. Atweh, N. B. Bahuth, and S. J. Jabbur. 1997. Augmentation of nociceptive reflexes and chronic deafferentation pain by chemical lesions of either dopaminergic terminals or midbrain dopaminergic neurons. Brain Res. 751:1-12.
47. Sandkühler, J. 2009. Models and mechanisms of hyperalgesia and allodynia. Physiol. Rev. 89:707-758.
48. Sogabe, S., Y. Yagasaki, K. Onozawa, and Y. Kawakami. 2013. Mesocortical dopamine system modulates mechanical nociceptive responses recorded in the rat prefrontal cortex. BMC Neurosci. 14:65.
49. Takazawa, T., and A. B. MacDermott. 2010. Synaptic pathways and inhibitory gates in the spinal cord dorsal horn. Ann. N. Y. Acad. Sci. 1198:153-158.
50. Takeda, R., T. Ikeda, F. Tsuda, H. Abe, H. Hashiguchi, Y. Ishida, et al. 2005. Unilateral lesions of mesostriatal dopaminergic pathway alters the withdrawal response of the rat hindpaw to mechanical stimulation. Neurosci. Res. 52:31-36.
51. Torsney, C., and A. B. MacDermott. 2006. Disinhibition opens the gate to pathological pain signaling in superficial neurokinin 1 receptor-expressing neurons in rat spinal cord. J. Neurosci. 26:1833-1843.
52. Vautier, S., A. Milane, C. Fernandez, H. Chacun, L. Lacomblez, and R. Farinotti. 2009. Role of two efflux proteins, ABCB1 and ABCG2 in blood-brain barrier transport of bromocriptine in a murine model of MPTP-induced dopaminergic degeneration. J. Pharm. Pharm. Sci. 12:199-208.
53. Vos, B. P., A. M. Strassman, and R. J. Maciewicz. 1994. Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J. Neurosci. 14:2708-2723.
54. Wang, S., G. Lim, Q. Zeng, B. Sung, L. Yang, and J. Mao. 2005. Central glucocorticoid receptors modulate the expression and function of spinal NMDA receptors after peripheral nerve injury. J. Neurosci. 25:488-495.
55. Wasner, G., and G. Deuschl. 2012. Pains in Parkinson disease-many syndromes under one umbrella. Nat. Rev. Neurol. 8:284-294.
56. Wood, P. B. 2006. Mesolimbic dopaminergic mechanisms and pain control. Pain 120:230-234.
57. Woolf, C. J., and R. J. Mannion. 1999. Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet 353:1959-1964.
58. Zengin-Toktas, Y., N. Authier, H. Denizot, C. Chassain, A. Hafidi, P. M. Llorca, et al. 2013. Motivational properties of D2 and D3 dopamine receptors agonists and cocaine, but not with D1 dopamine receptors agonist and l-dopa, in bilateral 6-OHDA-lesioned rat. Neuropharmacology 70:74-82.