Analgesia induced by localized injection of opiate peptides into the brain of infant rats

European Journal of Pain (United Kingdom)

Volumn 17, Issue 5, 2013, Pages 676-691

  Barr, G A ^a,b   Wang, S ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE];

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BRAIN REGION; CONTROLLED STUDY; FEMALE; MALE; MESENCEPHALON; MICROINJECTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PONS; PRIORITY JOURNAL; RAPHE MAGNUS NUCLEUS; RAT; ROSTRAL VENTRAL MEDULLA; SPINAL CORD DORSAL HORN; STIMULATION;

ANALGESIA; ANALGESICS, OPIOID; ANIMALS; ANIMALS, NEWBORN; BRAIN; FEMALE; INJECTIONS; MALE; OPIOID PEPTIDES; PAIN; PAIN MANAGEMENT; RATS; RATS, LONG-EVANS; RECEPTORS, OPIOID, MU;

EID: 84879583143     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2012.00245.x     Document Type: Article

References (74)

1. Bandler, R., Depaulis, A., Vergnes, M. (1985). Identification of midbrain neurones mediating defensive behaviour in the rat by microinjections of excitatory amino acids. Behav Brain Res 15, 107-119.
2. Bandler, R., Shipley, M.T. (1994). Columnar organization in the midbrain periaqueductal gray: Modules for emotional expression? Trends Neurosci 17, 379-389.
3. Barbaresi, P. (2010). Postnatal development of GABAimmunoreactive neurons and terminals in rat periaqueductal gray matter: A light and electron microscopic study. J Comp Neurol 518, 2240-2260.
4. Barr, G., Moriceau, S., Shionoya, K., Muzny, K., Gao, P., Wang, S., Sullivan, R. (2009). Transitions in infant learning are modulated by dopamine in the amygdala. Nat Neurosci 12, 1367-1369.
5. Barr, G.A. (1991). Neuropharmaco-ontogeny: Concepts and methods of study. In Developmental Psychobiology: New Methods and Changing Concepts, H.N. Shair, G.A. Barr, M.A. Hofer, eds. (New York: Oxford) pp. 321-341.
6. Barr, G.A., Miya, D.Y., Paredes, W. (1992). Analgesic effects of intraventricular and intrathecal injection of morphine and ketocyclazocine in the infant rat. Brain Res 584, 83-91.
7. Beitz, A.J. (1982). The nuclei of origin of brainstem serotonergic projections to the rodent spinal trigeminal nucleus. Neurosci Lett 2, 223-228.
8. Blass, E.M., Cramer, C.P., Fanselow, M.S. (1993). The development of morphine-induced antinociception in neonatal rats: A comparison of forepaw, hindpaw, and tail retraction from a thermal stimulus. Pharmacol Biochem Behav 44, 643-649.
9. Bodnar, R.J., Williams, C.L., Lee, S.J., Pasternak, G.W. (1988). Role of mu 1-opiate receptors in supraspinal opiate analgesia: A microinjection study. Brain Res 447, 25-34.
10. Cameron, A.A., Khan, I.A., Westlund, K.N., Cliffer, K.D., Willis, W.D. (1995a). The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris-leucoagglutinin study. I. Ascending projections. J Comp Neurol 351, 568-584.
11. Cameron, A.A., Khan, I.A., Westlund, K.N., Willis, W.D. (1995b). The efferent projections of the periaqueductal gray in the rat: A phaseolus vulgaris leucoagglutinin study 0.2. descending projections. J Comp Neurol 351, 585-601.
12. Cannon, J.T., Prieto, G.J., Liebeskind, J.C. (1982). Evidence for opioid and non-opioid forms of stimulation produced analgesia in the rat. Brain Res 243, 315-321.
13. Capuano, C.A., Leibowitz, S.F., Barr, G.A. (1992a). The pharmaco-ontogeny of the paraventricular alpha 2-noradrenergic receptor system mediating norepinephrine-induced feeding in the rat. Brain Res Dev Brain Res 68, 67-74.
14. Capuano, C.A., Leibowitz, S.F., Barr, G.A. (1992b). The pharmaco-ontogeny of the perifornical lateral hypothalamic beta 2-adrenergic and dopaminergic receptor systems mediating epinephrine- and dopamine-induced suppression of feeding in the rat. Brain Res Dev Brain Res 70, 1-7.
15. Capuano, C.A., Leibowitz, S.F., Barr, G.A. (1992c). Pharmacoontogeny of hypothalamic induced feeding. Dev Brain Res 68, 67-74.
16. Carden, S.E., Barr, G.A., Hofer, M.A. (1991). Differential effects of specific opioid receptor agonists on rat pup isolation calls. Brain Res Dev Brain Res 62, 17-22.
17. Carstens, E., Douglass, D.K. (1995). Midbrain suppression of limb withdrawal and tail flick reflexes in the rat: Correlates with descending inhibition of sacral spinal neurons. J Neurophysiol 73, 2179-2194.
18. Chan, T., Kyere, K., Davis, B., Shemyakin, A., Kabitzke, P., Shair, H., Barr, G.A., Wiedenmayer, C. (2011). The role of the medial prefrontal cortex in innate fear regulation in infants, juveniles, and adolescents. J Neurosci 31, 4991-4999.
19. Chen, S.W., Shemyakin, A., Wiedenmayer, C.P. (2006). The role of the amygdala and olfaction in unconditioned fear in developing rats. J Neurosci 26, 233-240.
20. Chieng, B., Christie, M.J. (1994a). Hyperpolarization by opioids acting on mu-receptors of a sub-population of rat periaqueductal gray neurones in vitro. Br J Pharmacol 113, 121-128.
21. Chieng, B., Christie, M.J. (1994b). Inhibition by opioids acting on mu receptors of GABA ergic and glutamatergic postsynaptic potentials in single rat periaqueductal gray neurones in vitro. Br J Pharmacol 113, 303-309.
22. D'Mello, R., Dickenson, A.H. (2008). Spinal cord mechanisms of pain. Br J Anaesth 101, 8-16.
23. Desprat, C., Zajac, J.M. (1994). Ontogeny of neuropeptide FF pharmacology and receptors in mouse brain. Dev Brain Res 82, 118-126.
24. Festing, M.F. (2006). Design and statistical methods in studies using animal models of development. ILAR J 47, 5-14.
25. Fields, H.L. (2000). Pain modulation: Expectation, opioid analgesia and virtual pain. Prog Brain Res 122, 245-253.
26. Fields, H.L., Vanegas, H., Hentall, I.D., Zorman, G. (1983). Evidence that disinhibition of brain stem neurones contributes to morphine analgesia. Nature 306, 684-686.
27. Fitzgerald, M. (1986). Monoamines and descending control of nociception. Trends Neurosci 9, 51-52.
28. Gallagher, D.W., Pert, A. (1978). Afferents to brain stem nuclei (brain stem raphae, nucleus reticularis pontis caudalis and nucleus gigantocellularis) in the rat as demonstrated by microiontophoretically applied horse radish peroxidase. Brain Res 144, 257-275.
29. Hathway, G.J., Koch, S., Low, L., Fitzgerald, M. (2009). The changing balance of brainstem-spinal cord modulation of pain processing over the first weeks of rat postnatal life. J Physiol 587, 2927-2935.
30. Heinricher, M.M., Martenson, M.E., Neubert, M.J. (2004). Prostaglandin E2 in the midbrain periaqueductal gray produces hyperalgesia and activates pain-modulating circuitry in the rostral ventromedial medulla. Pain 110, 419- 426.
31. Heller, A., Hutchens, J.O., Kirby, M.L., Karapas, F., Fernandez, C. (1979). Stereotaxic electrode placement in the neonatal rat. J Neurosci 1, 41-76.
32. Heyman, J.S., Mulvaney, S.A., Mosberg, H.I., Porreca, F. (1987). Opioid d-receptor involvement in supraspinal and spinal antinociception in mice. Brain Res 420, 100-108.
33. Heyman, J.S., Vaught, J.L., Raffa, R.B., Porreca, F. (1988). Can supraspinal delta opioid receptor mediate antinociception? Trends Pharmacol Sci 9, 134-138.
34. Hughes, H.E., Barr, G.A. (1988). Analgesic effects of intrathecally applied noradrenergic compounds in the developing rat: Differences due to thermal and mechanical nociception. Dev Brain Res 41, 109-120.
35. Jackson, H.C., Kitchen, I. (1989a). Behavioural effects of selective m, k, and d-opioid agonists in neonatal rats. Psychopharmacology 97, 404-409.
36. Jackson, H.C., Kitchen, I. (1989b). Behavioural effects of selective mu-, kappa-, and delta-opioid agonists in neonatal rats. Psychopharmacology (Berl) 97, 404-409.
37. Jensen, T.S., Yaksh, T.L. (1986). Comparison of the antinociceptive action of mu and delta opioid receptor ligands in the periaqueductal gray matter, medial and paramedial ventral medulla in the rat as studied by the microinjection technique. Brain Res 372, 301-312.
38. Jones, S.L., Gebhart, G.F. (1988). Inhibition of spinal nociceptive transmissin from the midbrain, pons and medulla in the rat: Activation of descending inhibition my morphine, glutamate and electrical stimulation. Brain Res 460, 281-296.
39. Kehoe, P., Blass, E.M. (1986). Central nervous system mediation of positive and negative reinforcement in neonatal albino rats. Brain Res 392, 69-75.
40. Koch, B., Sakly, M., Lutz-Bucher, B. (1980). Ontogeny of opiate receptor sites in brain: Apparent lack of low affinity sites during early neonatal life. Horm Metab Res 12, 342-343.
41. Kornblum, H.I., Hurlbut, D.E., Leslie, F.M. (1987). Postnatal development of multiple opioid receptors in rat brain. Brain Res 415, 21-41.
42. Leslie, F.M., Tso, S., Hurlbut, D.E. (1982). Differential appearance of opiate receptor subtypes in neonatal rat brain. Life Sci 31, 1393-1396.
43. Lunzer, M.M., Portoghese, P.S. (2007). Selectivity of delta- and kappa-opioid ligands depends on the route of central administration in mice. J Pharmacol Exp Ther 322, 166-171.
44. McDowell, J., Kitchen, I. (1986). Ontogenesis of d-opioid receptors in rat brain using [3H]-[D-Pen2, D-Pen5]enkephalin as a binding ligand. Eur J Pharmacol 128, 287-289.
45. McDowell, J., Kitchen, I. (1987). Development of opioid systems: Peptides, receptors and pharmacology. Brain Res Rev 12, 397-421.
46. McLaughlin, C.R., Dewey, W.L. (1994). A comparison of the antinociceptive effects of opioid agonists in neonatal and adult rats in phasic and tonic nociceptive tests. Pharmacol Biochem Behav 49, 1017-1023.
47. Moreau, J.L., Fields, H.L. (1986). Evidence for GABA involvement in midbrain control of medullary neurons that modulate nociceptive transmission. Brain Res 397, 37-46.
48. Morgan, M.M., Liebeskind, J.C. (1987). Site specificity in the development of tolerance to stimulation-produced analgesia from the periaqueductal grey matter of the rat. Brain Res 425, 356-359.
49. Morgan, M.M., Whittier, K.L., Hegarty, D.M., Aicher, S.A. (2008). Periaqueductal gray neurons project to spinally projecting GABAergic neurons in the rostral ventromedial medulla. Pain 140, 376-386.
50. Nichols, D.S., Thorn, B.E. (1990). Stimulation-produced analgesia and its cross-tolerance between dorsal and ventral PAG loci. Pain 41, 347-352.
51. Paxinos, G., Tork, I., Tecott, L., Valentino, K. (1991). Atlas of the Developing Rat Brain (San Diego, CA: Academic Press).
52. Porreca, F., Heyman, J.S., Mosberg, H.I., Omnas, J.R., Vaught, J.L. (1987). Role of mu and delta receptors in the supraspinal and spinal analgesic effects of [D-Pen2, D-Pen5]enkephalin in the mouse. J Pharmacol Exp Ther 241, 393-400.
53. Reichling, D.B., Basbaum, A.I. (1990). Contribution of brainstem GABA ergic circuitry to descending antinociceptive controls: II. Electron microscopic immunocytochemical evidence of GABA ergic control over the projection from the periaqueductal gray to the nucleus raphe magnus in the rat. J Comp Neurol 302, 378-393.
54. Rosenfeld, J.P. (1994). Interacting brain stem components of opiate-activated, descending, pain-inhibitory systems. Neurosci Biobehav Rev 18, 403-409.
55. Rossi, G.C., Pasternak, G.W., Bodnar, R.J. (1993). Synergistic brainstem interactions for morphine analgesia. Brain Res 624, 171-180.
56. Rossi, G.C., Pasternak, G.W., Bodnar, R.J. (1994). Mu and delta opioid synergy between the periaqueductal gray and the rostro-ventral medulla. Brain Res 665, 85-93.
57. Saeki, S., Yaksh, T.L. (1993). Suppression of nociceptive responses by spinal mu opioid agonists - effects of stimulus intensity and agonist efficacy. Anesth Analg 77, 265-274.
58. Sherwood, N., Timiras, P.S. (1971). Stereotaxic Atlas of the Developing Rat Brain (Berkeley, CA: University of California Press).
59. Smith, D.J., Perrotti, J.M., Crisp, T., Cabral, M.E., Long, J.T., Scalzitti, J.M. (1988). The mu opiate receptor is responsible for descending pain inhibition originating in the periaqueductal gray region of the rat brain. Eur J Pharmacol 156, 47-54.
60. Spain, J.W., Bennett, D.B., Roth, B.L., Coscia, C.J. (1983). Ontogeny of benzomorphan-selective (kappa) sites: A computerized analysis. Life Sci 33(Suppl 1), 235-238.
61. Spain, J.W., Roth, B.L., Coscia, C.J. (1985). Differential ontogeny of multiple opioid receptors (mu, delta, and kappa). J Neurosci 5, 584-588.
62. Stamford, J.A. (1995). Descending control of pain. Br J Anaesth 75, 217-227.
63. Takagi, H., Satoh, M., Akaike, A., Shibata, T., Kuraishi, Y. (1978). Analgesia by enkephalins injected into the nucleus reticularis gigantocellularis of rat medulla oblongata. Eur J Pain 49, 113- 116.
64. Tarasiuk, A., Gibbs, L., Kendig, J.J. (1996). Descending inhibition in neonatal rat spinal cord: Actions of pentobarbital and morphine. Brain Res Bull 41, 39-45.
65. Tempel, A., Zukin, R.S. (1987). Neuroanatomical patterns of the u, d, and k opioid receptors of rat brain as determinied by quantitative in vitro autoradiography. Proc Natl Acad Sci U S A 84, 4308-4312.
66. Tive, L.A., Barr, G.A. (1992). Analgesia from the periaqueductal gray in the developing rat: Focal injections of morphine or glutamate and effects of intrathecal injection of methysergide or phentolamine. Brain Res 584, 92-109.
67. Tseng, L.F., Collins, K.A., Wang, Q. (1995). Differential ontogenesis of thermal and mechanical antinociception induced by morphine and beta-endorphin. Eur J Pharmacol 277, 71-76.
68. van Praag, H., Frenk, H. (1991). The development of stimulation-produced analgesia (SPA) in the rat. Brain Res Dev Brain Res 64, 71-76.
69. Vanegas, H. (2004). To the descending pain-control system in rats, inflammation-induced primary and secondary hyperalgesia are two different things. Neurosci Lett 361, 225-228.
70. Vaught, J.L., Mathiasen, J.R., Raffa, R.B. (1988). Examination of the involvement of supraspinal and spinal mu and delta opioid receptors in analgesia using the mu receptor deficient CXBK mouse. J Pharmacol Exp Ther 245, 13-16.
71. Watkins, L.R., Wiertelak, E.P., Maier, S.F. (1992). Kappa opiate receptors mediate tail-shock induced antinociception at spinal levels. Brain Res 582, 1-9.
72. Wheeler-Aceto, H., Cowan, A. (1991). Standardization of the rat paw formalin test for the evaluation of analgesics. Psychopharmacology 104, 35-44.
73. Willis, W.D.J. (1988). Anatomy and physiology of descending control of nociceptive responses of dorsala horn neurons: Comprehensive review. In Progress in Brain Research, H.L. Fields, J.-M. Besson, eds. (Amsterdam: Elsevier Science Publishers) pp. 1-29.
74. Zhang, A.Z., Pasternak, G.W. (1981). Ontogeny of opioid pharmacology and receptors: High and low affinity site differences. Eur J Pharmacol 73, 29-40.