Biological implications of coeruleospinal inhibition of nociceptive processing in the spinal cord

Frontiers in Integrative Neuroscience

Volumn , Issue SEPTEMBER, 2012, Pages

  Tsuruoka, Masayoshi ^a   Tamaki, Junichiro ^a   Maeda, Masako ^a   Hayashi, Bunsho ^a   Inoue, Tomio ^a  

^a SHOWA UNIVERSITY SCHOOL OF DENTISTRY   (Japan)

Author keywords

Air puff stimulation; Coeruleospinal pathway; Locus coeruleus subcoeruleus; Pain control; Peripheral inflammation; Spinal dorsal horn; Startle response

Indexed keywords

ACCURACY; ANTINOCICEPTION; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; COERULEOSPINAL INHIBITORY PATHWAY; ELECTROENCEPHALOGRAM; EVOKED BRAIN STEM RESPONSE; LOCUS CERULEUS; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; PAW EDEMA; REVIEW; SENSORY FEEDBACK; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SOMATOSENSORY SYSTEM; SPINAL CORD DORSAL HORN; SPINAL CORD LESION; STARTLE REFLEX; STIMULUS RESPONSE; TEMPERATURE SENSITIVITY;

EID: 84898557010     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2012.00087     Document Type: Review

References (73)

1. Adams, L. M., and Geyer, M. A. (1981). Effects of 6-hydroxydopamine lesions of locus coeruleus on startle in rats. Psychopharmacology 73, 394-398.
2. Al-Chaer, E. D., Feng, Y., and Willis, W. D. (1999). Comparative study of viscerosomatic input onto postsy-naptic dorsal column and spinothalamic tract neurons in the primate. J. Neurophysiol. 82, 1876-1882.
3. Al-Chaer, E. D., Lawand, N. B., Westlund, K. N., and Willis, W. D. (1996). Pelvic visceral input into the nucleus gracilis is largely mediated by the postsynaptic dorsal column pathway. J. Neurophysiol. 76, 2675-2690.
4. Anand, K. J., Coskun, V., Thrivikraman, K. V., Nemeroff, C. B., and Plotsky, P. M. (1999). Long-term behavioral effects of repetitive pain in neonatal rat pups. Physiol. Behav. 66, 627-637.
5. Aston-Jones, G., Chiang, C., and Aleexinsky, T. (1991). Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog. BrainRes. 88, 501-520.
6. Attal, N., Kayser, V., and Guilbaud, G. (1990). The bidirectional dose-dependent effect of systemic naloxone is also related to the intensity and duration of pain-related disorders: a study in rat model of peripheral mononeuropathy. Brain Res. 525, 170-174.
7. Baba, H., Kohno, T., Okamoto, M., Goldstein, P. A., Shomoji, K., and Yoshimura, M. (1998). Muscarinic facilitation of GABA release in substantia gelatinosa of the rat spinal dorsal horn. J. Physiol. 508, 83-93.
8. Barros, H. M., and Miczek, K. A. (1996). Withdrawal from oral cocaine in rats: ultrasonic and tactile startle. Psychopharmacology (Berl.) 125, 379-384.
9. Berridge, C. W., and Waterhouse, B. D. (2003). The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 42, 33-84.
10. Bushnell, M. C., Villemure, C., and Duncan, G. H. (2004). "Psychophysical and neurophysio-logical studies of pain modulation by attention, " in Psychological Methods of Pain Control: Basic Science and Clinical Perspectives. eds D. D. Price and M. C. Bushnell (Seattle, WA: IASP Press), 99-116.
11. Cassela, J. V., and Davis, M. (1986). Neural structures mediating acoustic and tactile startle reflexes and the acoustically elicited pinna response in rats: electrolytic and ibotenic acid studies. Soc. Neurosci. Abstr. 12, 1273.
12. Casto, R., Nguyen, T., and Printz, M. P. (1989). Characterization of cardiovascular and behavioral responses to altering stimuli in rats. Am. J. Physiol. 256, R1121-R1126.
13. Clark, F. M., and Proudfit, H. K. (1991). The projection of locus coeruleus neurons to the spinal cord in the rat determined by anterograde tracing combined with immuno-cytochemistry. Brain Res. 538, 231-245.
14. Clark, F. M., and Proudfit, H. K. (1992). Anatomical evidence for genetic differences in the innervation of the rat spinal cord by noradrenergic locus coeruleus neurons. Brain Res. 591, 44-53.
15. Cooke, D. F., and Graziano, M. S. (2003). Defensive movements evoked by air puff in monkeys. J. Neurophysiol. 90, 3317-3329.
16. Cooke, D. F., and Graziano, M. S. (2004). Super-flinchers and nerves of steel: defensive movements altered by chemical manipulation of a cortical motor area. Neuron 43, 585-593.
17. D'Amour, F. E., and Smith, D.L. (1941). A method for determining loss of pain sensation. J. Pharmacol. Exp. Ther. 72, 74-79.
18. Davis, M. (1984). "The mammalian startle response, " in Neural Mechanism of Startle Behavior. ed R. C. Eaton (New York, NY: Plenum Press), 287-351.
19. de Menezes, R. C., Zaretsky, D. V., Sarkar, S., Fontes, M. A., and Dimicco, J. A. (2008). Microinjection of muscimol into the periaqueductal gray suppresses cardiovascular and neuroendocrine response to air jet stress in conscious rats. Am. J. Physiol. Regul. Integr. Comp. Physol. 295, R881-R890.
20. Fanselow, M. S., and Helmstetter, F. J. (1988). Conditional analgesia, defensive freezing, and benzodiazepines. Behav. Neurosci. 102, 233-243.
21. Foote, S. L., Bloom, F. E., and Aston-Jones, G. (1983). Nucleus locus coeruleus: new evidence of anatomical and physiological specificity. Physiol. Rev. 63, 844-913.
22. Fritschy, J.-M., and Grzanna, R. (1990). Demonstration of two separate descending noradrenergic pathways to the rat spinal cord: evidence for an intragriseal trajectory of locus coeruleus axons in the superficial layers of the dorsal horn. J. Comp. Neurol. 291, 553-582.
23. Geyer, M. A., Flicker, C. E., and Lee, E. H. (1982). Effects of tactile startle on serotonin content ofmidbrain raphe neurons in rats. Behav. Brain Res. 4, 369-376.
24. Grzanna, R., and Fritschy, J.-M. (1991). Efferent projections of different subpopulations of central norader-enaline neurons. Prog. Brain Res. 88, 89-101.
25. Guyenet, P. G. (1980). The coeruleospinal noradrenergic neurons: anatomical and electrophysiological studies in the rat. BrainRes. 189, 121-133.
26. Hodge, C. J. Jr., Apkarian, A. V., Stevens, R., Vogelsang, G., and Wisnicki, H. J. (1981). Locus coeruleus modulation of dorsal horn unit responses to cutaneous stimulation. Brain Res. 204, 415-420.
27. Horie, H., Pamplin, P. J., and Yokota, T. (1991). Inhibition of nociceptive neurons in the shell region of nucleus ventralis posterolater-alis following conditioning stimulation of the periaqueductal gray of the cat. Evidence for an ascending inhibitory pathway. Brain Res. 561, 35-42.
28. Jones, S. L. (1991). Descending noradrenergic influences on pain. Prog. Brain Res. 88, 381-394.
29. Jones, S. L., and Gebhart, G. E. (1986a). Characterization of coeruleospinal inhibition of the nociceptive tail-flick reflex in the rat: mediation by spinal a 2-adrenoceptors. Brain Res. 364, 315-330.
30. Jones, S. L., and Gebhart, G. F. (1986b). Quantitative characterization of coeruleospinal inhibition of nociceptive transmission in the rat. J. Neurophysiol. 56, 1397-1410.
31. Jones, S. L., and Gebhart, G. F. (1987). Spinal pathways mediating tonic, coeruleospinal, and raphe-spinal descending inhibition in the rat. J. Neurophysiol. 58, 138-159.
32. Jones, S. L., and Gebhart, G. F. (1988). Inhibition of spinal nociceptive transmission from the midbrain, pons and medulla in the rat: activation of descending inhibition by morphine, glutamate and electrical stimulation. Brain Res. 460, 281-296.
33. Kayser, V., and Guilbaud, G. (1991). Physiological relevance and time course of a tonic endogenous opioid modulation of nociceptive messages, based on the effects of naloxone in a rat model of localized hyperalgesic inflammation, Brain Res. 567, 197-203.
34. Knapp, D. J., and Pohorecky, L. A. (1995). An air-puff stimulus method for elicitation of ultrasonic vocalizations in rats. J. Neurosci. Meth. 62, 1-5.
35. Koyama, N., Nishikawa, Y., Chua, T., Iwamoto, M., and Yokota, T. (1995). Differential inhibitory mechanisms in VPL versus intralaminar nociceptive neurons of the cat: I. Effects of periaqueductal gray stimulation. Jpn. J. Physiol. 45, 1005-1027.
36. Liu, L., Tsuruoka, M., Maeda, M., Hayashi, B., and Inoue, T. (2007). Coerulespinal inhibition of visceral nociceptive processing in the rat spinal cord. Neurosci. Lett. 426, 139-144.
37. Liu, L., Tsuruoka, M., Maeda, M., Hayashi, B., Wang, X., and Inoue, T. (2008). Descending modulation of visceral nociceptive transmission from the locus coeruleus/subcoeruleus in the rat. Brain Res. Bull. 76, 616-625.
38. Li, Y., Yue, H., Xing, Y., Sun, H., Pan, Z., and Xie, G. (2010). Oxymatrine inhibits development of morphine-induced tolerance associated with decreased expression of P-glycoprotein in rats. Integr. Cancer Ther. 9, 213-218.
39. Lockey, A. J., Kavaliers, M., and Ossenkopp, K. P. (2009). Lipopolysaccharide reduces tactile s tartle response magnitude but not prepulse inhibition in rats: a dose-response examination. Pharmacol. Biochem. Behav. 93, 47-53.
40. Margalit, D., and Segal, M. (1979). A pharmacologic study of analgesia produced by stimulation of the nucleus locus coeruleus. Psychopharmacology62, 169-183.
41. Millan, M. J., Czlonkowski, A., Morris, B., Stein, C., Arendt, R., Huber, A., et al. (1988). Inflammation of the hind limb as a model of unilateral, localized pain: influence on multiple opioid systems in the spinal cord of the rat. Pain 35, 299-312.
42. Mokha, S. S., McMillan, J. A., and Iggo, A. (1985). Descending control of spinal nociceptive transmission: actions produced on spinal multi-receptive neurons from the nuclei locus coeruleus (LC) and raphe magnus (NRM). Exp. Brain Res. 58, 213-225.
43. Ness, T. J. (2000). Evidence for ascending visceral nociceptive information in the dorsal midline and lateral spinal cord. Pain 87, 83-88.
44. Palecek, J., Paleckova, V., and Willis, W. D. (2002). The role of pathways in the spinal cord lateral and dorsal funiculi in signaling nociceptive somatic and visceral stimuli in rats. Pain 96, 297-307.
45. Palecek, J., Paleckova, V., and Willis, W. D. (2003). Fos expression in spinothalamic and postsynaptic dorsal column neurons following noxious visceral and cutaneous stimuli. Pain 104, 249-257.
46. Palecek, J., and Willis, W. D. (2003). The dorsal column pathway facilitates visceromotor responses to colorectal distention after colon inflammation in rats. Pain 104, 501-507.
47. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coodinates. New York, NY: Academic Press.
48. Proudfit, H. K., and Clark, F. M. (1991). The projections of locus coeruleus neurons to the spinal cord. Prog. Brain Res. 85, 123-141.
49. Ren, K., and Dubner, R. (1996). Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J. Neurophysiol. 76, 3025-3037.
50. Retting, R., Geyer, M. A., and Printz, M. P. (1986). Cardiovascular concomitants of tactile and acoustic startle responses in spontaneously hypertensive and normotensive rats. Physiol. Behav. 36, 1123-1128.
51. Rinaldi, P. C., and Thompson, R. F. (1985). Age, sex and strain comparison of habituation of the startle response in the rat. Physiol. Behav. 35, 9-13.
52. Schröder, W., Vry, J. D., Tzschentke, T. M., Jahnel, U., and Christoph, T. (2010). Differential contribution ofopioidand noradrenergic mechanisms of tapentadol in rat models of nociceptive and neuropathic pain. Eur. J. Pain 14, 814-821.
53. Segal, M., and Sandberg, D. (1977). Analgesia produced by electrical stimulation of catecholamine nuclei in the rat brain. Brain Res. 123, 369-372.
54. Silva, J. R., Silva, M. L., and Prado, W. A. (2010). Analgesia induced by 2-or 100 Hz electroacupuncture in the rat tail-flick test depends on the activation of different descending pain inhibitory mechanisms. J. Pain 12, 51-60.
55. Sluka, K. A., and Westlund, K. N. (1992). Spinal projections of the locus coeruleus and the nucleus subcoeruleus in the Halan and the Sasco Sprague-Dawley rat. Brain Res. 579, 67-73.
56. Sttensland, P., Hallberg, M., Kindlundh, A., Fahlke, C., and Nyberg, F. (2005). Amphetamine-induced aggression is enhanced in rats pre-treated with the anabolic androgenic steroid nandrolone decanoate. Steroid 70, 199-204.
57. Taylor, B. K., Casto, R., and Printz, M. P. (1991). Dissociation of tactile and acoustic components in air puff startle. Physiol. Behav. 49, 527-532.
58. Tsuruoka, M., Liu, L., Maeda, M., Hayashi, B., and Inoue, T. (2008). Coeruleospinal Influence on Visceral Nociceptive Processing in the Rat Spinal Cord. Abstracts of the 12th World Congress on Pain (CD): Presentation Number PT 348.
59. Tsuruoka, M., Maeda, M., Nagasawa, I., and Inoue, T. (2004). Spinal pathways mediating coeruleospinal antinociception in the rat. Neurosci. Lett. 362, 236-239.
60. Tsuruoka, M., Matsutani, K., and Inoue, T. (2003). Coeruleospinal inhibition of nociceptive processing in the dorsal horn during unilateral hindpaw inflammation in the rat. Pain 104, 353-361.
61. Tsuruoka, M., Tamaki, J., Maeda, M., Hayashi, B., and Inoue, T. (2010a). The nucleus locus coeruleus/subcoeruleus affects the defensive-like, immobile posture following an air-puff startle reaction in the rat. Neuroscience 168, 149-155.
62. Tsuruoka, M., Wang, D., Tamaki, J., and Inoue, T. (2010b). Descending influence from the nucleus locus coeruleus/subcoeruleus on visceral nociceptive transmission in the rat spinal cord. Neuroscience 165, 1019-1024.
63. Tsuruoka, M., Tamaki, J., Maeda, M., Hayashi, B., and Inoue, T. (2011). The nucleus locus coeruleus/subcoeruleus contributes to antinociception during freezing behavior following the air-puff startle in rats. Brain Res. 1393, 52-61.
64. Tsuruoka, M., and Willis, W. D. (1996a). Bilateral lesions in the area of the nucleus locus coeruleus affect the development of hyperalgesia during carrageenan-induced inflammation. Brain Res. 726, 233-236.
65. Tsuruoka, M., and Willis, W. D. (1996b). Descending modulation from the region of the locus coeruleus on nociceptive sensitivity in a rat model of inflammatory hyperalgesia. Brain Res. 743, 86-92.
66. Wei, F., Dubner, R., and Ren, K. (1999). Nucleus reticularis giganto-cellularis and nucleus raphe magnus in the brain stem exert opposite effects on behavioral hyperalgesia and spinal Fos protein expression after peripheral inflammation. Pain 80, 127-141.
67. Westlund, K. N., Bowker, R. M., Ziegler, M. G., and Coulter, J. D. (1983). Noradrenergic projections to the spinal cord in the rat. Brain Res. 263, 15-31.
68. Westlund, K. N., Bowker, R. M., Ziegler, M. G., and Coulter, J. D. (1984). Origins and terminations of descending noradrenergic projections to the spinal cord of monkey. Brain Res. 292, 1-16.
69. West, W. L., Yeomans, D. C., and Proudfit, H. K. (1993). The function of noradrenergic neurons in mediating antinociception induced by electrical stimulation of the locus coeruleus in two different sources of Sprague-Dawley rats. Brain Res. 626, 127-135.
70. Willis, W. D., and Coggeshall, R. E. (2004). Sensory Mechanisms of the Spinal Cord, Vol. 2. New York, NY: Kluwer Academic/Plenum, 857-876.
71. Woodworth, C. H., and Johnson, A. K. (1988). Isolation, tactile startle and resting blood pressure in Long-Evans rats. Physiol. Behav. 43, 609-616.
72. Woolfe, G., and MacDonald, A. D. (1944). The evaluation of the analgesic action of pethidine hydrochloride (Demerol). J. Pharmacol. Exp. Ther. 80, 300-307.
73. Zaretsky, D. V., Zaretskaia, M.V., Samuels, B. C., Cluxton, L.K., and DiMicco, J. A. (2003). Microinjection of muscimol into raphe pallidus suppresses tachycardia associated with air stress in conscious rats. J. Physiol. 546, 243-250.