Acute noxious stimulation modifies morphine effect in serotonergic but not dopaminergic midbrain areas

Neuroscience

Volumn 166, Issue 2, 2010, Pages 720-729

  Bajic, D ^a,b   Commons, K G ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Dorsal raphe; Formalin; Fos; Rat; Tryptophan hydroxylase; Ventral tegmental area

Indexed keywords

FORMALDEHYDE; MORPHINE SULFATE; PROTEIN FOS; DOPAMINE; MORPHINE; PROTEIN C FOS; SEROTONIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DORSAL RAPHE NUCLEUS; ELECTROENCEPHALOGRAM; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REWARD; SEROTONINERGIC NERVE CELL; VENTRAL TEGMENTUM; ANALYSIS OF VARIANCE; ANIMAL; CELL COUNT; DRUG EFFECT; FLUORESCENCE MICROSCOPY; METABOLISM; NERVE CELL; PAIN ASSESSMENT; SPRAGUE DAWLEY RAT; STIMULATION;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; DOPAMINE; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MICROSCOPY, FLUORESCENCE; MORPHINE; NEURONS; PAIN; PAIN MEASUREMENT; PHYSICAL STIMULATION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN;

EID: 77951901207     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.12.031     Document Type: Article

References (54)

1. Abbott FV, Franklin KBJ, Westbrook RF (1995) The formalin test: scoring properties of the first and second phases of the pain response in rats. Pain 60:91-102.
2. Abrams JK, Johnson PL, Hay-Schmidt A, Mikkelsen JD, Shekhar A, Lowry CA (2005) Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 133:983-997.
3. Alcaro A, Huber R, Panksepp J (2007) Behavioral functions of the mesolimbic dopaminergic system: an affective neuroethological perspective. Brain Res Rev 56:283-321.
4. Ballantyne JC (2007) Opioid analgesia: perspectives on right use and utility. Pain Physician 10:479-491.
5. Bardo MT, Rowlett JK, Harris MJ (1995) Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci Biobehav Rev 19:39-51.
6. Beart PM, McDonald D (1982) 5-Hydroxytryptamine and 5-hydroxytryptaminergic-dopaminergic interactions in the ventral tegmental area of rat brain. J Pharm Pharmacol 34:591-593.
7. Benloucif S, Galloway MP (1991) Facilitation of dopamine release in vivo by serotonin agonists: studies with microdialysis. Eur J Pharmacol 200:1-8.
8. Bullitt E (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol 296:517-530.
9. Chang SL, Squinto SP, Harlan RE (1988) Morphine activation of c-fos expression in rat brain. Biochem Biophys Res Commun 157: 698-704.
10. Chen T, Dong YX, Li YQ (2003) Fos expression in serotonergic neurons in the rat brainstem following noxious stimuli: an immunohistochemical double-labelling study. J Anat 203:579-588.
11. Cicero J, Ennis T, Ogden J, Meyer ER (2000) Gender differences in the reinforcing properties of morphine. Pharmacol Biochem Behav 65:91-96.
12. Commons KG, Connolley KR, Valentino RJ (2003) A neurochemically distinct dorsal raphe-limbic circuit with a potential role in affective disorders. Neuropsychopharmacology 28:206-215.
13. Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261-265.
14. Dubuisson D, Dennis SG (1977) The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brainstem stimulation in rats and cats. Pain 4:161-164.
15. Garcia MM, Brown HE, Harlan RE (1995) Alterations in immediateearly gene proteins in the rat forebrain induced by acute morphine injection. Brain Res 692:23-40.
16. Guan XM, McBride WJ (1989) Serotonin microinfusion into the ventral tegmental area increases accumbens dopamine release. Brain Res Bull 23:541-547.
17. Hagan RM, Jones BJ, Jordan CC, Tyers MB (1990) Effect of 5-HT3 receptor antagonists on responses to selective activation of mesolimbic dopaminergic pathways in the rat. Br J Pharmacol 99:227-232.
18. Herdegen T, Leah JD (1998) Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 28:370-490.
19. Hunt SP, Pini A, Evan G (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632-634.
20. Imai H, Park MR, Steindler DA, Kitai ST (1986a) The morphology and divergent axonal organization of midbrain raphe projection neurons in the rat. Brain Dev 8:343-354.
21. Imai H, Steindler DA, Kitai ST (1986b) The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 243:363-380.
22. Jacobs BL, Foote SL, Bloom FE (1978) Differential projections of neurons within the dorsal raphe nucleus of the rat: a horseradish peroxidase (HRP) study. Brain Res 147:149-153.
23. Keay KA, Clement CI, Owler B, Depaulis A, Bandler R (1994) Convergence of deep somatic and vesceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region. Neuroscience 61:727-732.
24. Lang B, Li YQ (1998) Serotoninergic neurons in the brainstem expressing FOS protein after orofacial noxious stimulation: an immunocytochemical double-labeling study. J Hirnforsch 39:263-268.
25. Leah JD, Herdegen T, Zimmermann M (1989) Physiological and pharmacological induction of c-fos protein immunoreactivity in superficial dorsal horn neurons. In: Processing of sensory information in the superficial dorsal horn of the spinal Cord, Vol. 176 (Cervero F, et al, eds), pp 307-310. New York: Plenum Press.
26. Leshner AI, Koob GF (1999) Drugs of abuse and the brain. Proc Assoc Am Physicians 111:99-108.
27. Liu J, Nickolenko J, Sharp FR (1994) Morphine induces c-fos and junB in striatum and nucleus accumbens via D1 and N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A 91:8537-8541.
28. Loyd DR, Morgan MM, Murphy AZ (2007) Morphine preferentially activates the periaqueductal gray-rostral ventromedial medullary pathway in the male rat: a potential mechanism for sex differences in antinociception. Neuroscience 147:456-468.
29. Luccarini P, Childeric A, Gaydier AM, Voisin D, Dallel R (2006) The orofacial formalin test in the mouse: a behavioral model for studying physiology and modulation of trigeminal nociception. J Pain 7:908-914.
30. Ma QP, Zhou Y, Han JS (1993) Noxious stimulation accelerated the expression of c-fos protooncogene in cholecystokininergic and dopaminergic neurons in the ventral tegmental area. Peptides 14:561-566.
31. McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1-28.
32. Minabe Y, Emori K, Ashby CR Jr (1996) The depletion of brain serotonin levels by para-chlorophenylalanine administration significantly alters the activity of midbrain dopamine cells in rats: an extracellular single cell recording study. Synapse 22:46-53.
33. Morgan JI, Cohen DR, Hempstead JL, Curran T (1987) Mapping pattern of c-fos expression in the central nervous system after seizure. Science 237:192-197.
34. Morgan MM, Fossum EN, Stalding BM, King MM (2006) Morphine antinociceptive potency on chemical, mechanical, and thermal nociceptive tests in the rat. J Pain 7:358-366.
35. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Orlando, FL: Academic Press.
36. Petrov T, Krukoff TL, Jhamandas JH (1994) Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 277:289-295.
37. Pierce RC, Kumaresan V (2006) The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev 30:215-238
38. Porter J, Jick H (1980) Addiction rare in patients treated with narcotics. N Engl J Med 302:123.
39. Rothman RB, Blough BE, Baumann MH (2008) Dual dopamine/serotonin releasers: potential treatment agents for stimulant addiction. Exp Clin Psychopharmacol 16:458-474.
40. Sagar SM, Sharp FR, Curran T (1988) Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240: 1328-1331.
41. Sharp FR, Sagar SM, Swanson RA (1993) Metabolic mapping with cellular resolution: c-fos vs. 2-deoxyglucose. Crit Rev Neurobiol 7:205-228.
42. Singh ME, Verty AN, Price I, McGregor IS, Mallet PE (2004) Modulation of morphine-induced Fos-immunoreactivity by the cannabinoid receptor antagonist SR 141716. Neuropharmacology 47:1157- 1169.
43. Schmidt HD, Anderson SM, Famous KR, Kumaresan V, Pierce RC (2005) Anatomy and pharmacology of cocaine priminginduced reinstatement of drug seeking. Eur J Pharmacol 526: 65-76.
44. Spanagel R, Weiss F (1999) The dopamine hypothesis of reward: past and current status. Trends Neurosci 22:521-527.
45. Suzuki T, Kishimoto Y, Ozaki S, Narita M (2001) Mechanism of opioid dependence and interaction between opioid receptors. Eur J Pain 5(Suppl A):63-65.
46. Trulson ME, Cannon MS, Raese JD (1985) Identification of dopaminecontaining cell bodies in the dorsal and median raphe nuclei of the rat brain using tyrosine hydroxylase immunochemistry. Brain Res Bull 15:229-234.
47. Ungless MA, Magill PJ, Bolam JP (2004) Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303:2040-2042.
48. Van Bockstaele EJ, Biswas A, Pickel VM (1993) Topography of serotonin neurons in the dorsal raphe nucleus that send axon collaterals to the rat prefrontal cortex and nucleus accumbens. Brain Res 624:188-198.
49. Van den Heuvel DM, Pasterkamp RJ (2008) Getting connected in the dopamine system. Prog Neurobiol 85:75-93.
50. Weiss F, Koob GF (2001) Drug addiction: functional neurotoxicity of the brain reward systems. Neurotox Res 3:145-156.
51. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.
52. Yan QS, Yan SE (2001) Activation of 5-HT(1B/1D) receptors in the mesolimbic dopamine system increases dopamine release from the nucleus accumbens: a microdialysis study. Eur J Pharmacol 418:55-64.
53. Yoshimoto K, McBride WJ (1992) Regulation of nucleus accumbens dopamine release by the dorsal raphe nucleus in the rat. Neurochem Res 17:401-407.
54. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110.