Acute and sensitized response to 3,4-methylenedioxymethamphetamine in rats: Different behavioral profiles reflected in different patterns of Fos expression

European Journal of Neuroscience

Volumn 28, Issue 9, 2008, Pages 1895-1910

  Colussi Mas, Joyce ^a   Schenk, Susan ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Behavioral sensitization; Immunohistochemistry; Locomotor activity

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; PROTEIN FOS; SODIUM CHLORIDE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN NERVE CELL; CELL ACTIVATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DOSE RESPONSE; DRUG EXPOSURE; DRUG RESPONSE; GLOBUS PALLIDUS; HABENULA; HYPERACTIVITY; HYPOTHALAMUS; IMMUNODETECTION; INJECTION; LOCOMOTION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THALAMUS NUCLEUS; TIME;

AMYGDALA; ANIMALS; BASAL GANGLIA; BEHAVIOR, ANIMAL; BRAIN; BRAIN MAPPING; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE; HABENULA; HALLUCINOGENS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NUCLEUS ACCUMBENS; PROTO-ONCOGENE PROTEINS C-FOS; PSYCHOMOTOR AGITATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 54849412271     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06467.x     Document Type: Article

References (76)

1. Aberg, M., Wade, D., Wall, E. Izenwasser, S. (2007) Effect of MDMA (ecstasy) on activity and cocaine conditioned place preference in adult and adolescent rats. Neurotoxicol. Teratol., 29, 37 46.
2. Abrams, J.K., Johnson, P.L., Hollis, J.H. Lowry, C.A. (2004) Anatomic and functional topography of the dorsal raphe nucleus. Ann. NY Acad. Sci., 1018, 46 57.
3. Acquas, E., Pisanu, A., Spiga, S., Plumitallo, A., Zernig, G. Di Chiara, G. (2007) Differential effects of intravenous R,S-(+/-)-3,4- methylenedioxymethamphetamine (MDMA, Ecstasy) and its S(+)- and R(-)-enantiomers on dopamine transmission and extracellular signal regulated kinase phosphorylation (pERK) in the rat nucleus accumbens shell and core. J. Neurochem., 102, 121 132.
4. Alden, M., Besson, J.M. Bernard, J.F. (1994) Organization of the efferent projections from the pontine parabrachial area to the bed nucleus of the stria terminalis and neighboring regions: a PHA-L study in the rat. J. Comp. Neurol., 341, 289 314.
5. Bossert, J.M., Poles, G.C., Wihbey, K.A., Koya, E. Shaham, Y. (2007) Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. J. Neurosci., 27, 12655 12663.
6. Brennan, K.A. Schenk, S. (2006) Initial deficit and recovery of function after MDMA preexposure in rats. Psychopharmacology (Berl), 184, 239 246.
7. Brown, E.E., Robertson, G.S. Fibiger, H.C. (1992) Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures. J. Neurosci., 12, 4112 4121.
8. Cadoni, C., Solinas, M., Pisanu, A., Zernig, G., Acquas, E. Di Chiara, G. (2005) Effect of 3,4-methylendioxymethamphetamine (MDMA, 'ecstasy') on dopamine transmission in the nucleus accumbens shell and core. Brain Res., 1055, 143 148.
9. Callaway, C.W. Geyer, M.A. (1992) Stimulant effects of 3,4-methylenedioxymethamphetamine in the nucleus accumbens of rat. Eur. J. Pharmacol., 214, 45 51.
10. Callaway, C.W., Wing, L.L. Geyer, M.A. (1990) Serotonin release contributes to the locomotor stimulant effects of 3,4- methylenedioxymethamphetamine in rats. J. Pharmacol. Exp. Ther., 254, 456 464.
11. Clark, M.S., McDevitt, R.A. Neumaier, J.F. (2006) Quantitative mapping of tryptophan hydroxylase-2, 5-HT1A, 5-HT1B, and serotonin transporter expression across the anteroposterior axis of the rat dorsal and median raphe nuclei. J. Comp. Neurol., 498, 611 623.
12. Cole, B.J., Cador, M., Stinus, L., Rivier, J., Vale, W., Koob, G.F. Le Moal, M. (1990) Central administration of a CRF antagonist blocks the development of stress-induced behavioral sensitization. Brain Res., 512, 343 346.
13. Dafters, R.I. (1995) Hyperthermia following MDMA administration in rats: effects of ambient temperature, water consumption, and chronic dosing. Physiol. Behav., 58, 877 882.
14. De La Garza, R. 2nd. Cunningham, K.A. (2000) The effects of the 5-hydroxytryptamine(1A) agonist 8-hydroxy-2-(di-n-propylamino)tetralin on spontaneous activity, cocaine-induced hyperactivity and behavioral sensitization: a microanalysis of locomotor activity. J. Pharmacol. Exp. Ther., 292, 610 617.
15. De Leonibus, E., Mele, A., Oliverio, A. Pert, A. (2001) Locomotor activity induced by the non-competitive N-methyl-D-aspartate antagonist, MK-801: role of nucleus accumbens efferent pathways. Neuroscience, 104, 105 116.
16. Deutch, A.Y., Bubser, M. Young, C.D. (1998) Psychostimulant-induced Fos protein expression in the thalamic paraventricular nucleus. J. Neurosci., 18, 10680 10687.
17. Dragunow, M., Logan, B. Laverty, R. (1991) 3,4- Methylenedioxymethamphetamine induces Fos-like proteins in rat basal ganglia: reversal with MK 801. Eur. J. Pharmacol., 206, 255 258.
18. Druhan, J.P. Wilent, W.B. (1999) Effects of the competitive N-methyl-D-aspartate receptor antagonist, CPP, on the development and expression of conditioned hyperactivity and sensitization induced by cocaine. Behav. Brain Res., 102, 195 210.
19. Engber, T.M., Koury, E.J., Dennis, S.A., Miller, M.S., Contreras, P.C. Bhat, R.V. (1998) Differential patterns of regional c-Fos induction in the rat brain by amphetamine and the novel wakefulness-promoting agent modafinil. Neurosci. Lett., 241, 95 98.
20. Erdtmann-Vourliotis, M., Mayer, P., Riechert, U. Hollt, V. (1999) Acute injection of drugs with low addictive potential (delta(9)-tetrahydrocannabinol, 3,4-methylenedioxymethamphetamine, lysergic acid diamide) causes a much higher c-fos expression in limbic brain areas than highly addicting drugs (cocaine and morphine). Brain Res. Mol. Brain Res., 71, 313 324.
21. Ferrario, C.R. Robinson, T.E. (2007) Amphetamine pretreatment accelerates the subsequent escalation of cocaine self-administration behavior. Eur. Neuropsychopharmacol., 17, 352 357.
22. Forray, M.I. Gysling, K. (2004) Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary-adrenal axis. Brain Res., 47, 145 160.
23. Gabbott, P.L., Warner, T.A., Jays, P.R., Salway, P. Busby, S.J. (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol., 492, 145 177.
24. Gold, L.H., Koob, G.F. Geyer, M.A. (1988) Stimulant and hallucinogenic behavioral profiles of 3,4-methylenedioxymethamphetamine and N-ethyl-3,4-methylenedioxyamphetamine in rats. J. Pharmacol. Exp. Ther., 247, 547 555.
25. Gold, L.H., Hubner, C.B. Koob, G.F. (1989) A role for the mesolimbic dopamine system in the psychostimulant actions of MDMA. Psychopharmacology (Berl), 99, 40 47.
26. Hargreaves, G.A., Hunt, G.E., Cornish, J.L. McGregor, I.S. (2007) High ambient temperature increases 3,4-methylenedioxymethamphetamine (MDMA, 'ecstasy')-induced Fos expression in a region-specific manner. Neuroscience, 145, 764 774.
27. Harlan, R.E. Garcia, M.M. (1998) Drugs of abuse and immediate-early genes in the forebrain. Mol. Neurobiol., 16, 221 267.
28. Hashimoto, K., Tomitaka, S., Narita, N., Minabe, Y. Iyo, M. (1997) Induction of Fos protein by 3,4-methylenedioxymethamphetamine (Ecstasy) in rat brain: regional differences in pharmacological manipulation. Addict. Biol., 2, 317 326.
29. Heimer, L., Zahm, D.S., Churchill, L., Kalivas, P.W. Wohltmann, C. (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience, 41, 89 125.
30. Herman, J.P., Figueiredo, H., Mueller, N.K., Ulrich-Lai, Y., Ostrander, M.M., Choi, D.C. Cullinan, W.E. (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front. Neuroendocrinol., 24, 151 180.
31. Ikemoto, S. (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev., 56, 27 78.
32. Ikemoto, S., Qin, M. Liu, Z.H. (2005) The functional divide for primary reinforcement of D-amphetamine lies between the medial and lateral ventral striatum: is the division of the accumbens core, shell, and olfactory tubercle valid J. Neurosci., 25, 5061 5065.
33. Jones, D.L. Mogenson, G.J. (1980a) Nucleus accumbens to globus pallidus GABA projection subserving ambulatory activity. Am. J. Physiol., 238, R65 R69.
34. Jones, D.L. Mogenson, G.J. (1980b) Nucleus accumbens to globus pallidus GABA projection: electrophysiological and iontophoretic investigations. Brain Res., 188, 93 105.
35. Ju, G. Swanson, L.W. (1989) Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: I. Cytoarchitecture. J. Comp. Neurol., 280, 587 602.
36. Kalivas, P.W., Duffy, P. White, S.R. (1998) MDMA elicits behavioral and neurochemical sensitization in rats. Neuropsychopharmacology, 18, 469 479.
37. Kelly, P.H., Seviour, P.W. Iversen, S.D. (1975) Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res., 94, 507 522.
38. Kindlundh-Hogberg, A.M., Schioth, H.B. Svenningsson, P. (2007) Repeated intermittent MDMA binges reduce DAT density in mice and SERT density in rats in reward regions of the adolescent brain. Neurotoxicology, 28, 1158 1169.
39. Klitenick, M.A., Deutch, A.Y., Churchill, L. Kalivas, P.W. (1992) Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum. Neuroscience, 50, 371 386.
40. Kovacs, K.J. (1998) c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem. Int., 33, 287 297.
41. Mattson, B.J., Crombag, H.S., Mitchell, T., Simmons, D.E., Kreuter, J.D., Morales, M. Hope, B.T. (2007) Repeated amphetamine administration outside the home cage enhances drug-induced Fos expression in rat nucleus accumbens. Behav. Brain Res., 185, 88 98.
42. McCreary, A.C., Bankson, M.G. Cunningham, K.A. (1999) Pharmacological studies of the acute and chronic effects of (+)-3,4- methylenedioxymethamphetamine on locomotor activity: role of 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(1B/1D) receptors. J. Pharmacol. Exp. Ther., 290, 965 973.
43. Mele, A., Thomas, D.N. Pert, A. (1998) Different neural mechanisms underlie dizocilpine maleate- and dopamine agonist-induced locomotor activity. Neuroscience, 82, 43 58.
44. Meredith, G.E. (1999) The synaptic framework for chemical signaling in nucleus accumbens. Ann. NY Acad. Sci., 877, 140 156.
45. Moga, M.M., Saper, C.B. Gray, T.S. (1989) Bed nucleus of the stria terminalis: cytoarchitecture, immunohistochemistry, and projection to the parabrachial nucleus in the rat. J. Comp. Neurol., 283, 315 332.
46. Morgan, J.I. Curran, T. (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci., 14, 421 451.
47. Morley, K.C. McGregor, I.S. (2000) (+/-)-3,4- Methylenedioxymethamphetamine (MDMA, 'Ecstasy') increases social interaction in rats. Eur. J. Pharmacol., 408, 41 49.
48. Morley, K.C., Arnold, J.C. McGregor, I.S. (2005) Serotonin (1A) receptor involvement in acute 3,4-methylenedioxymethamphetamine (MDMA) facilitation of social interaction in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry, 29, 648 657.
49. Nagashima, K., Nakai, S., Tanaka, M. Kanosue, K. (2000) Neuronal circuitries involved in thermoregulation. Auton. Neurosci., 85, 18 25.
50. O'Loinsigh, E.D., Boland, G., Kelly, J.P. O'Boyle, K.M. (2001) Behavioural, hyperthermic and neurotoxic effects of 3,4- methylenedioxymethamphetamine analogues in the Wistar rat. Prog. Neuropsychopharmacol. Biol. Psychiatry, 25, 621 638.
51. O'Shea, E., Granados, R., Esteban, B., Colado, M.I. Green, A.R. (1998) The relationship between the degree of neurodegeneration of rat brain 5-HT nerve terminals and the dose and frequency of administration of MDMA ('ecstasy'). Neuropharmacology, 37, 919 926.
52. O'Shea, E., Escobedo, I., Orio, L., Sanchez, V., Navarro, M., Green, A.R. Colado, M.I. (2005) Elevation of ambient room temperature has differential effects on MDMA-induced 5-HT and dopamine release in striatum and nucleus accumbens of rats. Neuropsychopharmacology, 30, 1312 1323.
53. Okabe, C. Murphy, N.P. (2004) Short-term effects of the nociceptin receptor antagonist Compound B on the development of methamphetamine sensitization in mice: a behavioral and c-fos expression mapping study. Brain Res., 1017, 1 12.
54. Ostrander, M.M., Badiani, A., Day, H.E., Norton, C.S., Watson, S.J., Akil, H. Robinson, T.E. (2003) Environmental context and drug history modulate amphetamine-induced c-fos mRNA expression in the basal ganglia, central extended amygdala, and associated limbic forebrain. Neuroscience, 120, 551 571.
55. Palenicek, T., Votava, M., Bubenikova, V. Horacek, J. (2005) Increased sensitivity to the acute effects of MDMA ('ecstasy') in female rats. Physiol. Behav., 86, 546 553.
56. Paulus, M.P., Geyer, M.A., Gold, L.H. Mandell, A.J. (1990) Application of entropy measures derived from the ergodic theory of dynamical systems to rat locomotor behavior. Proc. Natl Acad. Sci. USA, 87, 723 727.
57. Paxinos, G. Watson, C. (2005) The Rat Brain in Stereotaxic Coordinates, 5th edn. Elsevier Academic Press, San Diego, CA.
58. Pontieri, F.E., Tanda, G. Di Chiara, G. (1995) Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the 'shell' as compared with the 'core' of the rat nucleus accumbens. Proc. Natl Acad. Sci. USA, 92, 12304 12308.
59. Pontieri, F.E., Tanda, G., Orzi, F. Di Chiara, G. (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature, 382, 255 257.
60. Ramos, M., Goni-Allo, B. Aguirre, N. (2004) Studies on the role of dopamine D1 receptors in the development and expression of MDMA-induced behavioral sensitization in rats. Psychopharmacology (Berl), 177, 100 110.
61. Robinson, T.E. Berridge, K.C. (2003) Addiction. Annu. Rev. Psychol., 54, 25 53.
62. Ross, J.D., Herin, D.V., Frankel, P.S., Thomas, M.L. Cunningham, K.A. (2006) Chronic treatment with a serotonin(2) receptor (5-HT(2)R) agonist modulates the behavioral and cellular response to (+)-3,4- methylenedioxymethamphetamine [(+)-MDMA]. Drug Alcohol Depend., 81, 117 127.
63. Rotllant, D., Nadal, R. Armario, A. (2007) Differential effects of stress and amphetamine administration on Fos-like protein expression in corticotropin releasing factor-neurons of the rat brain. Dev. Neurobiol., 67, 702 714.
64. Sarnyai, Z., Shaham, Y. Heinrichs, S.C. (2001) The role of corticotropin-releasing factor in drug addiction. Pharmacol. Rev., 53, 209 243.
65. Singewald, N., Salchner, P. Sharp, T. (2003) Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol. Psychiatry, 53, 275 283.
66. Spanos, L.J. Yamamoto, B.K. (1989) Acute and subchronic effects of methylenedioxymethamphetamine [(+/-)MDMA] on locomotion and serotonin syndrome behavior in the rat. Pharmacol. Biochem. Behav., 32, 835 840.
67. Stephenson, C.P., Hunt, G.E., Topple, A.N. McGregor, I.S. (1999) The distribution of 3,4-methylenedioxymethamphetamine 'Ecstasy'-induced c-fos expression in rat brain. Neuroscience, 92, 1011 1023.
68. Swerdlow, N.R. Koob, G.F. (1985) Separate neural substrates of the locomotor-activating properties of amphetamine, heroin, caffeine and corticotropin releasing factor (CRF) in the rat. Pharmacol. Biochem. Behav., 23, 303 307.
69. Swerdlow, N.R., Koob, G.F., Cador, M., Lorang, M. Hauger, R.L. (1993) Pituitary-adrenal axis responses to acute amphetamine in the rat. Pharmacol. Biochem. Behav., 45, 629 637.
70. Thompson, B.L. Rosen, J.B. (2006) Immediate-early gene expression in the central nucleus of the amygdala is not specific for anxiolytic or anxiogenic drugs. Neuropharmacology, 50, 57 68.
71. Todtenkopf, M.S., Mihalakopoulos, A. Stellar, J.R. (2002) Withdrawal duration differentially affects c-fos expression in the medial prefrontal cortex and discrete subregions of the nucleus accumbens in cocaine-sensitized rats. Neuroscience, 114, 1061 1069.
72. Treit, D. Fundytus, M. (1988) Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol. Biochem. Behav., 31, 959 962.
73. Usuda, I., Tanaka, K. Chiba, T. (1998) Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res., 797, 73 93.
74. Vezina, P. (2004) Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci. Biobehav. Rev., 27, 827 839.
75. Wang, J.Q., Smith, A.J. McGinty, J.F. (1995) A single injection of amphetamine or methamphetamine induces dynamic alterations in c-fos, zif/268 and preprodynorphin messenger RNA expression in rat forebrain. Neuroscience, 68, 83 95.
76. Won, M., Minabe, Y., Tani, K., Suzuki, K., Kawai, M., Sekine, Y., Ashby, C.R. Jr., Takei, N. Mori, N. (2003) The effects of dentate granule cell destruction on behavioral activity and Fos protein expression induced by systemic MDMA in rats. Neurosci. Res., 46, 153 160.