Vagal afferent modulation of spinal trigeminal neuronal responses to dural electrical stimulation in rats

Neuroscience

Volumn 222, Issue , 2012, Pages 29-37

  Lyubashina, O A ^a   Sokolov, A Y ^a,b   Panteleev, S S ^a,b  

^a PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

^b PAVLOV FIRST SAINT PETERSBURG STATE MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

Dural electrical stimulation; GABA; Headache; Neuronal activity; STN; Trigeminal pathway; Vagus nerve stimulation; VNS

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED BRAIN STEM RESPONSE; HEADACHE; MALE; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; THERAPY EFFECT; TRIGEMINAL NUCLEUS; VAGUS NERVE STIMULATION;

ANIMALS; DURA MATER; ELECTRIC STIMULATION; MALE; MENINGES; NECK MUSCLES; NEURONS; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SPINAL NERVES; TRIGEMINAL NUCLEUS, SPINAL; VAGUS NERVE; VAGUS NERVE STIMULATION;

EID: 84864935141     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.07.011     Document Type: Article

References (67)

1. Aicher S.A., Lewis S.J., Randich A. Antinociception produced by electrical stimulation of vagal afferents: independence of cervical and subdiaphragmatic branches. Brain Res 1991, 542:63-70.
2. Akerman S., Holland P.R., Goadsby P.J. Cannabinoid (CB1) receptor activation inhibits trigeminovascular neurons. JPET 2007, 320:64-71.
3. Albert G.C., Cook C.M., Prato F.S., Thomas A.W. Deep brain stimulation, vagal nerve stimulation and transcranial stimulation: an overview of stimulation parameters and neurotransmitter release. Neurosci Biobehav Rev 2009, 33:1042-1060.
4. Bajbouj M., Merkl A., Schlaepfer T.E., Frick C., Zobel A., Maier W., O'Keane V., Corcoran C., Adolfsson R., Trimble M., Rau H., Hoff H.J., Padberg F., Muller-Siecheneder F., Audenaert K., van den Abbeele D., Matthews K., Christmas D., Eljamel S., Heuser I. Two-year outcome of vagus nerve stimulation in treatment-resistant depression. J Clin Psychopharmacol 2010, 30:273-281.
5. Benarroch E.E. Pain-autonomic interactions. Neurol Sci 2006, 27:130-133.
6. Ben-Menachem E., Hamberger A., Hedner T., Hammond E.J., Uthman B.M., Slater J., Treig T., Stefan H., Ramsay R.E., Wernicke J.F., Wilder B.J. Effects of vagus nerve stimulation on amino acids and other metabolites in the CSF of patients with partial seizures. Epilepsy Res 1995, 20:221-227.
7. Bohotin C., Scholsem M., Bohotin V., Franzen R., Schoenen J. Vagus nerve stimulation attenuates heat- and formalin-induced pain in rats. Neurosci Lett 2003, 351:79-82.
8. Bohotin C., Scholsem M., Multon S., Martin D., Bohotin V., Schoenen J. Vagus nerve stimulation in awake rats reduces formalin-induced nociceptive behaviour and fos- immunoreactivity in trigeminal nucleus caudalis. Pain 2003, 101:3-12.
9. Bossut D.F., Whitsel E.A., Maixner W. A parametric analysis of the effects of cardiopulmonary vagal electrostimulation on the digastric reflex in cats. Brain Res 1992, 579:253-260.
10. Bossut D.F., Maixner W. Effects of cardiac vagal afferent electrostimulation on the response of trigeminal and trigeminothalamic neurons to noxious orofacial stimulation. Pain 1996, 65:101-109.
11. Broggi G., Messina G., Franzini A. Cluster headache and TACs: rationale for central and peripheral neuromodulation. Neurol Sci 2009, 30(Suppl 1):75-79.
12. Broggi G., Messina G., Marras C., Dones I., Franzini A. Neuromodulation for refractory headaches. Neurol Sci 2010, 31(Suppl. 1):S87-S92.
13. Cecchini A.P., Mea E., Tullo V., Curone M., Franzini A., Broggi G., Savino M., Bussone G., Leone M. Vagus nerve stimulation in drug-resistant daily chronic migraine with depression: preliminary data. Neurol Sci 2009, 30(Suppl. 1):S101-S104.
14. Chandler M.J., Qin C., Yuan Y., Foreman R.D. Convergence of trigeminal input with visceral and phrenic inputs on primate C1-C2 spinothalamic tract neurons. Brain Res 1999, 829:204-208.
15. Di Stani F., Calabresi M., Pappagallo M., Scattoni L., Bruti G., Cerbo R. Atypical primary headache responding to finger pressure: possible involvement of the vagus nerve?. J Headache Pain 2007, 8:60-62.
16. Dorr A.E., Debonnel G. Effect of vagus nerve stimulation and noradrenergic transmission. J Pharmacol Exp Ther 2006, 318:890-898.
17. Edvinsson L., Uddman R. Neurobiology in primary headaches. Brain Res 2005, 48:438-456.
18. Evans A.R., Jones S.L., Blair R.W. Effects of vagal afferent nerve stimulation on noxious heat-evoked Fos-like immunoreactivity in the rat lumbar spinal cord. J Comp Neurol 1994, 22:490-498.
19. Fu Q.G., Chandler M.J., McNeill D.L., Foreman R.D. Vagal afferent fibers excite upper cervical neurons and inhibit activity of lumbar spinal cord neurons in the rat. Pain 1992, 51:91-100.
20. Goadsby P.J. Migraine, allodinia, sensitisation and all of that. Eur Neurol 2005, 53(Suppl. 1):10-16.
21. Goadsby P.J., Chabrit A.R., Andreou A.P., Akerman S. Neurobiology of migraine. Neuroscience 2009, 161:327-341.
22. Goadsby P.J., Knight Y. Inhibition of trigeminal neurones after intravenous administration of naratriptan through an action at 5-hydroxy- tryptamine (5-HT1B/1D) receptors. Br J Pharmacol 1997, 122:918-922.
23. Groves D.A., Bowman E.M., Brown V.J. Recordings from the rat locus coeruleus during acute vagal nerve stimulation in the anaesthetised rat. Neurosci Lett 2005, 379:174-179.
24. Hobbs S.F., Oh U.T., Chandler M.J., Foreman R.D. Cardiac and abdominal vagal afferent inhibition of primate T9-S1 spinothalamic cells. Am J Physiol 1989, 257:R889-R895.
25. Hord E.D., Evans M.S., Mueed S., Adamolekun B., Naritoku D.K. The effect of vagus nerve stimulation on migraines. J Pain 2003, 4:530-534.
26. Hoskin K.L., Bulmer D.C., Goadsby P.J. Fos expression in the trigeminocervical complex of the cat after stimulation of the superior sagittal sinus is reduced by l-NAME. Neurosci Lett 1999, 266:173-176.
27. Imbe H., Dubner R., Ren K. Masseteric inflammation-induced Fos protein expression in the trigeminal interpolaris/caudalis transition zone: contribution of somatosensory-vagal-adrenal integration. Brain Res 1999, 845:165-175.
28. Jakubowski M., Levy D., Goor-Aryeh I., Collins B., Bajwa Z., Burstein R. Terminating migraine with allodynia and ongoing central sensitization using parenteral administration of COX1/COX2 inhibitors. Headache 2005, 45:850-861.
29. Jakubowski M., Levy D., Kainz V., Zhang X.C., Kosaras B., Burstein R. Sensitization of central trigeminovascular neurons: blockade by intravenous naproxen infusion. Neuroscience 2007, 148:573-583.
30. Kirchner A., Birklein F., Stefan H., Handwerker H.O. Left vagus nerve stimulation suppresses experimentally induced pain. Neurology 2000, 55:1167-1171.
31. Kirchner A., Stefan H., Bastian K., Birklein F. Vagus nerve stimulation suppresses pain but has limited effects on neurogenic inflammation in humans. Eur J Pain 2006, 10:449-455.
32. Kosel M., Schlaepfer T.E. Mechanisms and state of the art of vagus nerve stimulation. J ECT 2002, 18:189-192.
33. Lenaerts M.E., Oommen K.J., Couch J.R., Skaggs V. Can vagus nerve stimulation help migraine?. Cephalalgia 2008, 28:392-395.
34. Liu Y., Broman J., Zhang M., Edvinsson L. Brainstem and thalamic projections from a craniovascular sensory nervous centre in the rostral cervical spinal dorsal horn of rats. Cephalalgia 2009, 29:935-948.
35. Lyubashina O., Panteleev S. Effects of cervical vagus nerve stimulation on amygdala-evoked responses of the medial prefrontal cortex neurons in rat. Neurosci Res 2009, 65:122-125.
36. Maixner W., Bossut D.F., Whitsel E.A. Evaluation of vagal afferent modulation of the digastric reflex in cats. Brain Res 1991, 560:55-62.
37. Manta S., Dong J., Debonnel G., Blier P. Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation. J Psychiatry Neurosci 2009, 34:272-280.
38. Mauskop A. Vagus nerve stimulation relieves chronic refractory migraine and cluster headaches. Cephalalgia 2005, 25:82-86.
39. Messlinger K. Migraine: where and how does the pain originate?. Exp Brain Res 2009, 196:179-193.
40. Millan M.J. Descending control of pain. Prog Neurobiol 2002, 66:355-474.
41. Mørch C.D., Hu J.W., Arendt-Nielsen L., Sessle B.J. Convergence of cutaneous, musculoskeletal, dural and visceral afferents onto nociceptive neurons in the first cervical dorsal horn. Eur J Neurosci 2007, 26:142-154.
42. Ness T.J., Fillingim R.B., Randich A., Backensto E.M., Faught E. Low intensity vagal nerve stimulation lowers human thermal pain thresholds. Pain 2000, 86:81-85.
43. Nishikawa Y., Koyama N., Yoshida Y., Yokota T. Activation of ascending antinociceptive system by vagal afferent input as revealed in the nucleus ventralis posteromedialis. Brain Res 1999, 833:108-111.
44. Noseda R., Monconduit L., Constandil L., Chalus M., Villanueva L. Central nervous system networks involved in the processing of meningeal and cutaneous inputs from the ophthalmic branch of the trigeminal nerve in the rat. Cephalalgia 2008, 28:813-824.
45. Panneton W.M., McCulloch P.F., Sun W. Trigemino-autonomic connections in the muskrat: the neural substrate for the diving response. Brain Res 2000, 874:48-65.
46. Ray B.S., Wolff H.G. Experimental studies on headache. Pain sensitive structures of the head and their significance in headache. Arch Surg 1940, 41:813-856.
47. Ren K., Randich A., Gebhart G.F. Vagal afferent modulation of spinal nociceptive transmission in the rat. J Neurophysiol 1989, 62:401-415.
48. Ren K., Randich A., Gebhart G.F. Effects of electrical stimulation of vagal afferents on spinothalamic tract cells in the rat. Pain 1991, 44:311-319.
49. Roch M., Messlinger K., Kulchitsky V., Tichonovich O., Azev O., Koulchitsky S. Ongoing activity in trigeminal wide-dynamic range neurons is driven from the periphery. Neuroscience 2007, 150:681-691.
50. Ruffoli R., Giorgi F.S., Pizzanelli C., Murri L., Paparelli A., Fornai F. The chemical neuroanatomy of vagus nerve stimulation. J Chem Neuroanat 2011, 42:288-296.
51. Ruggiero D.A., Underwood M.D., Mann J.J., Anwar M., Arango V. The human nucleus of the solitary tract: visceral pathways revealed with an "in vitro" postmortem tracing method. J Auton Nerv Syst 2000, 79:181-190.
52. Sadler R.M., Purdy R.A., Rahey S. Vagal nerve stimulation aborts migraine in patient with intractable epilepsy. Cephalalgia 2002, 22:482-484.
53. Sessle B.J. Acute and chronic craniofacial pain: bransteim mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000, 11:57-91.
54. Sokolov A.Y., Lyubashina O.A., Panteleev S.S., Chizh B.A. Neurophysiological markers of central sensitisation in the trigeminal pathway and their modulation by the cyclo-oxygenase inhibitor ketorolac. Cephalalgia 2010, 30:1241-1249.
55. Sokolov A.Y., Lyubashina O.A., Panteleev S.S. Spinal trigeminal neurons demonstrate an increase in responses to dural electrical stimulation in the orofacial formalin test. J Headache Pain 2012, 13:75-82.
56. Storer R.J., Akerman S., Goadsby P.J. GABA receptors modulate trigeminovascular nociceptive neurotransmission in the trigeminocervical complex. Br J Pharmacol 2001, 134:896-904.
57. Storer R.J., Akerman S., Goadsby P.J. Calcitonin gene-related peptide (CGRP) modulates nociceptive trigeminovascular transmission in the cat. Br J Pharmacol 2004, 142:1171-1181.
58. Storer R.J., Akerman S., Shields K.G., Goadsby P.J. GABAA receptor modulation of trigeminovascular nociceptive neurotransmission by midazolam is antagonized by flumazenil. Brain Res 2004, 1013:188-193.
59. Storer R.J., Goadsby P.J. Trigeminovascular nociceptive transmission involves N-methyl-d-aspartate and non-N-methyl-d-aspartate glutamate receptors. Neuroscience 1999, 90:1371-1376.
60. Takeda M., Tanimoto T., Ojima K., Matsumoto S. Suppressive effect of vagal afferents on the activity of the trigeminal spinal neurons related to the jaw-opening reflex in rats: involvement of the endogenous opioid system. Brain Res Bull 1998, 47:49-56.
61. Tanimoto T., Takeda M., Matsumoto S. Suppressive effect of vagal afferents on cervical dorsal horn neurons responding to tooth pulp electrical stimulation in the rat. Exp Brain Res 2002, 145:468-479.
62. Thies R., Foreman R.D. Inhibition and excitation of thoracic spinoreticular neurons by electrical stimulation of vagal afferent nerves. Exp Neurol 1983, 82:1-16.
63. Thurston C.L., Randich A. Quantitative characterization and spinal substrates of antinociception produced by electrical stimulation of the subdiaphragmatic vagus in rats. Pain 1991, 44:201-209.
64. Thurston C.L., Randich A. Effects of vagal afferent stimulation on ON and OFF cells in the rostroventral medulla: relationships to nociception and arterial blood pressure. J Neurophysiol 1992, 67:180-196.
65. Thurston C.L., Randich A. Responses of on and off cells in the rostral ventral medulla to stimulation of vagal afferents and changes in mean arterial blood pressure in intact and cardiopulmonary deafferented rats. Pain 1995, 62:19-38.
66. Zerari-Mailly F., Buisseret P., Buisseret-Delmas C., Nosjean A. Trigemino-solitarii-facial pathway in rats. J Comp Neurol 2005, 487:176-189.
67. Zhang L.L., Ashwell K.W. The development of cranial nerve and visceral afferents to the nucleus of the solitary tract in the rat. Anat Embryol (Berl) 2001, 204:135-151.