Neuroplasticity in brain reward circuitry following a history of ethanol dependence

European Journal of Neuroscience

Volumn 27, Issue 8, 2008, Pages 1912-1922

  Hansson, Anita C ^a   Rimondini, Roberto ^b   Neznanova, Olga ^a   Sommer, Wolfgang H ^a   Heilig, Markus ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Animal model; Extended amygdala; Immediate early genes; In situ hybridization; Mitogen activated protein kinase; Rat

Indexed keywords

ALCOHOL; CORTICOSTERONE; EARLY GROWTH RESPONSE FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; UO 126;

ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOL INTOXICATION; ALCOHOLISM; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MARKER GENE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; ONCOGENE C FOS; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; REWARD; SIGNAL TRANSDUCTION; THALAMUS MIDLINE NUCLEUS;

ALCOHOLISM; ANIMALS; BRAIN; BUTADIENES; CENTRAL NERVOUS SYSTEM DEPRESSANTS; EARLY GROWTH RESPONSE PROTEIN 1; ENZYME INHIBITORS; ETHANOL; GENE EXPRESSION; GENES, FOS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MAP KINASE KINASE KINASES; NEURONAL PLASTICITY; NITRILES; RATS; RATS, WISTAR; REWARD;

EID: 42049116946     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06159.x     Document Type: Article

References (70)

1. Alheid, G.F. (2003) Extended amygdala and basal forebrain. Amygdala Brain Func.: Basic Clin. App., 985, 185 205.
2. Arlinde, C., Sommer, W., Bjork, K., Reimers, M., Hyytia, P., Kiianmaa, K. Heilig, M. (2004) A cluster of differentially expressed signal transduction genes identified by microarray analysis in a rat genetic model of alcoholism. Pharmacogenom. J., 4, 208 218.
3. Bachtell, R.K., Tsivkovskaia, N.O. Ryabinin, A.E. (2002) Alcohol-induced c-Fos expression in the Edinger-Westphal nucleus: pharmacological and signal transduction mechanisms. J. Pharmacol. Exp. Ther., 302, 516 524.
4. Blanchard, D.C., Canteras, N.S., Markham, C.M., Pentkowski, N.S. Blanchard, R.J. (2005) Lesions of structures showing FOS expression to cat presentation: Effects on responsivity to a cat, cat odor, and nonpredator threat. Neurosci. Biobehav. Rev., 29, 1243 1253.
5. Breese, G.R., Overstreet, D.H. Knapp, D.J. (2005) Conceptual framework for the etiology of alcoholism: a 'kindling'/stress hypothesis. Psychopharmacology (Berl.), 178, 367 380.
6. Cai, G., Zhen, X., Uryu, K. Friedman, E. (2000) Activation of extracellular signal-regulated protein kinases is associated with a sensitized locomotor response to D(2) dopamine receptor stimulation in unilateral 6-hydroxydopamine-lesioned rats. J. Neurosci., 20, 1849 1857.
7. Chandler, L.J. Sutton, G. (2005) Acute ethanol inhibits extracellular signal-regulated kinase, protein kinase B, and adenosine 3':5'-cyclic monophosphate response element binding protein activity in an age- and brain region-specific manner. Alcohol. Clin. Exp. Res., 29, 672 682.
8. Chang, S.L., Patel, N.A. Romero, A.A. (1995) Activation and desensitization of Fos immunoreactivity in the rat brain following ethanol administration. Brain Res., 679, 89 98.
9. Chaudhuri, A., Matsubara, J.A. Cynader, M.S. (1995) Neuronal-activity in primate visual-cortex assessed by immunostaining for the transcription factor Zif268. Vis. Neurosci., 12, 35 50.
10. Chen, S.W.C., Shemyakin, A. Wiedenmayer, C.P. (2006) The role of the amygdala and olfaction in unconditioned fear in developing rats. J. Neurosci., 26, 233 240.
11. Coogan, A.N. Piggins, H.D. (2003) Circadian and photic regulation of phosphorylation of ERK1/2 and Elk-1 in the suprachiasmatic nuclei of the Syrian hamster. J. Neurosci., 23, 3085 3093.
12. Crankshaw, D.L., Briggs, J.E., Olszewski, P.K., Shi, Q., Grace, M.K., Billington, C.J. Levine, A.S. (2003) Effects of intracerebroventricular ethanol on ingestive behavior and induction of c-Fos immunoreactivity in selected brain regions. Physiol. Behav., 79, 113 120.
13. Davis, M. (1992) The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci., 15, 353 375.
14. Davis, R.J. (1995) Transcriptional regulation by MAP kinases. Mol. Reprod. Dev., 42, 459 467.
15. Davis, M.I., Szarowski, D., Turner, J.N., Morrisett, R.A. Shain, W. (1999) In vivo activation and in situ BDNF-stimulated nuclear translocation of mitogen-activated/extracellular signal-regulated protein kinase is inhibited by ethanol in the developing rat hippocampus. Neurosci. Lett., 272, 95 98.
16. Dayas, C.V., Buller, K.M. Day, T.A. (1999) Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur. J. Neurosci., 11, 2312 2322.
17. Derkinderen, P., Valjent, E., Toutant, M., Corvol, J.C., Enslen, H., Ledent, C., Trzaskos, J., Caboche, J. Girault, J.A. (2003) Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J. Neurosci., 23, 2371 2382.
18. Dielenberg, R.A., Hunt, G.E. McGregor, I.S. (2001) 'When a rat smells a cat': The distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience, 104, 1085 1097.
19. van Dongen, Y.C., Deniau, J.M., Pennartz, C.M., Galis-de, G.Y., Voorn, P., Thierry, A.M. Groenewegen, H.J. (2005) Anatomical evidence for direct connections between the shell and core subregions of the rat nucleus accumbens. Neuroscience, 136, 1049 1071.
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. Garcia, M.M., Brown, H.E. Harlan, R.E. (1995) Alterations in immediate-early gene proteins in the rat forebrain induced by acute morphine injection. Brain Res., 692, 23 40.
22. Girault, J.A., Valjent, E., Caboche, J. Herve, D. (2007) ERK2: a logical and gate critical for drug-induced plasticity? Curr. Opin. Pharmacol., 7, 77 85.
23. Gutstein, H.B., Thome, J.L., Fine, J.L., Watson, S.J. Akil, H. (1998) Pattern of c-fos mRNA induction in rat brain by acute morphine. Can. J. Physiol. Pharmacol., 76, 294 303.
24. Hansson, A.C., Sommer, W., Rimondini, R., Andbjer, B., Stromberg, I. Fuxe, K. (2003) c-fos reduces corticosterone-mediated effects on neurotrophic factor expression in the rat hippocampal CA1 region. J. Neurosci., 23, 6013 6022.
25. Hansson, A.C., Cippitelli, A., Sommer, W.H., Fedeli, A., Bjork, K., Soverchia, L., Terasmaa, A., Massi, M., Heilig, M. Ciccocioppo, R. (2006) Variation at the rat Crhr1 locus and sensitivity to relapse into alcohol seeking induced by environmental stress. Proc. Natl Acad. Sci. U.S.A., 103, 15 236 15 241.
26. Heilig, M. Koob, G.F. (2007) A key role for corticotropin-releasing factor in alcohol dependence. Trends Neurosci., 30, 399 406.
27. Heimer, L. (2003) A new anatomical framework for neuropsychiatric disorders and drug abuse. Am. J. Psychiat., 160, 1726 1739.
28. Herring, B.E., Mayfield, R.D., Camp, M.C. Alcantara, A.A. (2004) Ethanol-induced fos immunoreactivity in the extended amygdala and hypothalamus of the rat brain: Focus on cholinergic interneurons of the nucleus accumbens. Alcohol. Clin. Exp. Res., 28, 588 597.
29. Hitzemann, B. Hitzemann, R. (1997) Genetics, ethanol and the Fos response. A comparison of the C57BL/6J and DBA/2J inbred mouse strains. Alcohol. Clin. Exp. Res., 21, 1497 1507.
30. Holm, S. (1979) A simple sequentially rejective multiple test procedure. Scand. J. Stat., 6, 65 70.
31. Homayoun, H. Moghaddam, B. (2006) Progression of cellular adaptations in medial prefrontal and orbitofrontal cortex in response to repeated amphetamine. J. Neurosci., 26, 8025 8039.
32. Hoover, W.B. Vertes, R.P. (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct., 212, 149 179.
33. Kalivas, P.W., Volkow, N. Seamans, J. (2005) Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron, 45, 647 650.
34. Kalluri, H.S. Ticku, M.K. (2002) Ethanol-mediated inhibition of mitogen-activated protein kinase phosphorylation in mouse brain. Eur. J. Pharmacol., 439, 53 58.
35. Kaufmann, K., Bach, K. Thiel, G. (2001) The extracellular signal-regulated protein kinases Erk1/Erk2 stimulate expression and biological activity of the transcriptional regulator Egr-1. Biol. Chem., 382, 1077 1081.
36. Knapp, D.J., Braun, C.J., Duncan, G.E., Qian, Y., Fernandes, A., Crews, F.T. Breese, G.R. (2001) Regional specificity of ethanol and NMDA action in brain revealed with FOS-like immunohistochemistry and differential routes of drug administration. Alcohol. Clin. Exp. Res., 25, 1662 1672.
37. Lu, L., Koya, E., Zhai, H., Hope, B.T. Shaham, Y. (2006) Role of ERK in cocaine addiction. Trends Neurosci., 29, 695 703.
38. Mazzucchelli, C., Vantaggiato, C., Ciamei, A., Fasano, S., Pakhotin, P., Krezel, W., Welzl, H., Wolfer, D.P., Pages, G., Valverde, O., Marowsky, A., Porrazzo, A., Orban, P.C., Maldonado, R., Ehrengruber, M.U., Cestari, V., Lipp, H.P., Chapman, P.F., Pouyssegur, J. Brambilla, R. (2002) Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron, 34, 807 820.
39. McBride, W.J. (2002) Central nucleus of the amygdala and the effects of alcohol and alcohol-drinking behavior in rodents. Pharmacol. Biochem. Behav., 71, 509 515.
40. McDonald, A.J., Mascagni, F. Guo, L. (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience, 71, 55 75.
41. Möller, C., Wiklund, L., Sommer, W., Thorsell, A. Heilig, M. (1997) Decreased experimental anxiety and voluntary ethanol consumption in rats following central but not basolateral amygdala lesions. Brain Res., 760, 94 101.
42. Neznanova, O., Sommer, W.H., Rimondini, R., Hansson, A.C., Hyyatia, P. Heilig, M. (2007) Signal transduction in alcohol-preferring AA and alcohol-avoiding ANA rat lines. Alcohol. Clin. Exp. Res., 31 (6 193A.
43. O'Dell, L.E., Roberts, A.J., Smith, R.T. Koob, G.F. (2004) Enhanced alcohol self-administration after intermittent versus continuous alcohol vapor exposure. Alcohol. Clin. Exp. Res., 28, 1676 1682.
44. Paxinos, G. Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
45. Ponomarev, I., Maiya, R., Harnett, M.T., Schafer, G.L., Ryabinin, A.E., Blednov, Y.A., Morikawa, H., Boehm, S.L., Homanics, G.E., Berman, A., Lodowski, K.H., Bergeson, S.E. Harris, R.A. (2006) Transcriptional signatures of cellular plasticity in mice lacking the alpha 1 subunit of GABA(A) receptors. J. Neurosci., 26, 5673 5683.
46. Reynolds, S.M. Zahm, D.S. (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J. Neurosci., 25, 11 757 11 767.
47. Rimondini, R., Arlinde, C., Sommer, W. Heilig, M. (2002) Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J., 16, 27 35.
48. Rimondini, R., Sommer, W. Heilig, M. (2003) A temporal threshold for induction of persistent alcohol preference: behavioral evidence in a rat model of intermittent intoxication. J. Stud. Alcohol, 64, 445 449.
49. Rivier, C., Imaki, T. Vale, W. (1990) Prolonged exposure to alcohol - effect on Crf messenger-Rna levels, and Crf-induced and stress-induced Acth-secretion in the rat. Brain Res., 520, 1 5.
50. Roberto, M., Nelson, T.E., Ur, C.L., Brunelli, M., Sanna, P.P. Gruol, D.L. (2003) The transient depression of hippocampal CA1 LTP induced by chronic intermittent ethanol exposure is associated with an inhibition of the MAP kinase pathway. Eur. J. Neurosci., 17, 1646 1654.
51. Roberts, A.J., Heyser, C.J., Cole, M., Griffin, P. Koob, G.F. (2000) Excessive ethanol drinking following a history of dependence: animal model of allostasis. Neuropsychopharmacology, 22, 581 594.
52. Ryabinin, A.E. Wang, Y.M. (1998) Repeated alcohol administration differentially affects c-Fos and FosB protein immunoreactivity in DBA/2J mice. Alcohol. Clin. Exp. Res., 22, 1646 1654.
53. Ryabinin, A.E., Criado, J.R., Henriksen, S.J., Bloom, F.E. Wilson, M.C. (1997) Differential sensitivity of c-Fos expression in hippocampus and other brain regions to moderate and low doses of alcohol. Mol. Psychiat., 2, 32 43.
54. Sanna, P.P., Simpson, C., Lutjens, R. Koob, G. (2002) ERK regulation in chronic ethanol exposure and withdrawal. Brain Res., 948, 186 191.
55. Schoenbaum, G. Setlow, B. (2003) Lesions of nucleus accumbens disrupt learning about aversive outcomes. J. Neurosci., 23, 9833 9841.
56. Schoenbaum, G. Shaham, Y. (2008) The role of orbitofrontal cortex in drug addiction: a review of preclinical studies. Biol. Psychiat., 63, 256 262.
57. Schuck, S., Soloaga, A., Schratt, G., Arthur, J.S.C. Nordheim, A. (2003) The kinase MSK1 is required for induction of c-fos by lysophosphatidic acid in mouse embryonic stem cells. Bmc Mol. Biol., 4, v4:6.
58. Seger, R. Krebs, E.G. (1995) The MAPK signaling cascade. FASEB J., 9, 726 735.
59. Silverman, A.J., Hoffman, D.L. Zimmerman, E.A. (1981) The descending afferent connections of the paraventricular nucleus of the hypothalamus (PVN). Brain Res. Bull., 6, 47 61.
60. Sommer, W.H., Rimondini, R., Hansson, A.C. Heilig, M. (2008) Up-regulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala Crhr1 expression following a history of dependence. Biol. Psychiat., 63, 139 145.
61. Sumner, B.E., Cruise, L.A., Slattery, D.A., Hill, D.R., Shahid, M. Henry, B. (2004) Testing the validity of c-fos expression profiling to aid the therapeutic classification of psychoactive drugs. Psychopharmacology (Berl.), 171, 306 321.
62. Tsai, J.C., Liu, L.X., Cooley, B.C., Dichiara, M.R., Topper, J.N. Aird, W.C. (2000) The Egr-1 promoter contains information for constitutive and inducible expression in transgenic mice. FASEB J., 14, 1870 1872.
63. Valdez, G.R. Koob, G.F. (2004) Allostasis and dysregulation of corticotropin-releasing factor and neuropeptide Y systems: implications for the development of alcoholism. Pharmacol. Biochem. Behav., 79, 671 689.
64. Valjent, E., Corvol, J.C., Pages, C., Besson, M.J., Maldonado, R. Caboche, J. (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J. Neurosci., 20, 8701 8709.
65. Valjent, E., Pages, C., Rogard, M., Besson, M.J., Maldonado, R. Caboche, J. (2001) Delta 9-tetrahydrocannabinol-induced MAPK/ERK and Elk-1 activation in vivo depends on dopaminergic transmission. Eur. J. Neurosci., 14, 342 352.
66. Vertes, R.P. (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 51, 32 58.
67. Vertes, R.P. (2006) Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience, 142, 1 20.
68. Zhai, H., Li, Y., Wang, X. Lu, L. (2008) Drug-induced alterations in the extracellular signal-regulated kinase (ERK) signalling pathway: implications for reinforcement and reinstatement. Cell Mol. Neurobiol., 28, 157 172.
69. Zoeller, R.T. Fletcher, D.L. (1994) A single administration of ethanol simultaneously increases c-fos mRNA and reduces c-jun mRNA in the hypothalamus and hippocampus. Brain Res. Mol. Brain Res., 24, 185 191.
70. Zorrilla, E.P., Valdez, G.R. Weiss, F. (2001) Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology (Berl.), 158, 374 381.