Sensitized activation of Fos and brain-derived neurotrophic factor in the medial prefrontal cortex and ventral tegmental area accompanies behavioral sensitization to amphetamine

Neuropharmacology

Volumn 61, Issue 4, 2011, Pages 558-564

  Fanous, Sanya ^a,b,d,e   Lacagnina, Michael J ^b,d   Nikulina, Ella M ^a,b   Hammer Jr , Ronald P ^a,b,c,d  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d ARIZONA STATE UNIVERSITY   (United States)

^e NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Amphetamine; BDNF; Fluorogold; Prefrontal cortex; Sensitization; Ventral tegmental area

Indexed keywords

AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; PROTEIN FOS; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN TISSUE; CONTROLLED STUDY; DRUG INFUSION; DRUG SENSITIZATION; LOCOMOTION; MALE; NERVE CELL STIMULATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REPEAT PROCEDURE; SPRAGUE DAWLEY RAT; VENTRAL TEGMENTUM;

AMPHETAMINE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; MALE; MOTOR ACTIVITY; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; VENTRAL TEGMENTAL AREA;

EID: 79959985868     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.04.026     Document Type: Article

References (57)

1. C.A. Altar, N. Cai, T. Bliven, M. Juhasz, J.M. Conner, A.L. Acheson, R.M. Lindsay, and S.J. Wiegand Anterograde transport of brain-derived neurotrophic factor and its role in the brain Lett. Nat. 389 1997 856 860 (Pubitemid 27462980)
2. H.W. Berendse, Y. Galis-de Graaf, and H.J. Groenewegen Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat J. Comp. Neurol. 316 1992 314 347
3. Y. Bjijou, P. De Deurwaerdere, U. Spampinato, L. Stinus, and M. Cador D-amphetamine-induced behavioral sensitization: effect of lesioning dopaminergic terminals in the medial prefrontal cortex, the amygdala and the entorhinal cortex Neuroscience 109 2002 499 516 (Pubitemid 34122001)
4. I. Boileau, A. Dagher, M. Leyton, R.N. Gunn, G.B. Baker, M. Diksic, and C. Benkelfat Modeling sensitization to stimulants in humans: an [11C]raclopride/positron emission tomography study in healthy men Arch. Gen. Psychiatry 63 2006 1386 1395 (Pubitemid 44878522)
5. C.A. Bolanos, and E.J. Nestler Neurotrophic mechanisms in drug addiction Neuromolecular Med. 5 2004 69 83 (Pubitemid 38391958)
6. M. Cador, Y. Bjijou, S. Cailhol, and L. Stinus D-amphetamine-induced behavioral sensitization: implication of a glutamatergic medial prefrontal cortex-ventral tegmental area innervation Neuroscience 94 1999 705 721 (Pubitemid 29474959)
7. M.V. Caldeira, C.V. Melo, D.B. Pereira, R.F. Carvalho, A.L. Carvalho, and C.B. Duarte BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons Mol. Cell Neurosci. 35 2007 208 219 (Pubitemid 46843562)
8. G. Carmignoto, T. Pizzorusso, S. Tia, and S. Vicini Brain-derived neurotrophic factor and nerve growth factor potentiate excitatory synaptic transmission in the rat visual cortex J. Physiol. 498 Pt 1 1997 153 164 (Pubitemid 27056886)
9. D.B. Carr, and S.R. Sesack Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons J. Neurosci. 20 2000 3864 3873 (Pubitemid 30266247)
10. J. Colussi-Mas, S. Geisler, L. Zimmer, D.S. Zahm, and A. Berod Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double-labelling study Eur. J. Neurosci. 26 2007 1011 1025 (Pubitemid 47274628)
11. J.M. Conner, J.C. Lauterborn, Q. Yan, C.M. Gall, and S. Varon Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport J. Neurosci. 17 1997 2295 2313 (Pubitemid 27137397)
12. H.E. Covington 3rd, and K.A. Miczek Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration "binges" Psychopharmacology (Berl) 158 2001 388 398 (Pubitemid 33141315)
13. S. Fanous, R.P. Hammer Jr., and E.M. Nikulina Short- and long-term effects of intermittent social defeat stress on brain-derived neurotrophic factor expression in mesocorticolimbic brain regions Neuroscience 167 2010 598 607
14. C. Flores, A.N. Samaha, and J. Stewart Requirement of endogenous basic fibroblast growth factor for sensitization to amphetamine J. Neurosci. 20 2000 RC55
15. C. Flores, and J. Stewart Basic fibroblast growth factor as a mediator of the effects of glutamate in the development of long-lasting sensitization to stimulant drugs: studies in the rat Psychopharmacology (Berl) 151 2000 152 165 (Pubitemid 30646418)
16. F. Fumagalli, L. Di Pasquale, L. Caffino, G. Racagni, and M.A. Riva Repeated exposure to cocaine differently modulates BDNF mRNA and protein levels in rat striatum and prefrontal cortex Eur. J. Neurosci. 26 2007 2756 2763 (Pubitemid 350115522)
17. F. Fumagalli, L. Pasquale, G. Racagni, and M.A. Riva Dynamic regulation of fibroblast growth factor 2 (FGF-2) gene expression in the rat brain following single and repeated cocaine administration J. Neurochem. 96 2006 996 1004
18. S. Geisler, C. Derst, R.W. Veh, and D.S. Zahm Glutamatergic afferents of the ventral tegmental area in the rat J. Neurosci. 27 2007 5730 5743 (Pubitemid 350021081)
19. S. Geisler, and D.S. Zahm Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions J. Comp. Neurol. 490 2005 270 294 (Pubitemid 41140993)
20. J.W. Grimm, L. Lu, T. Hayashi, B.T. Hope, T.P. Su, and Y. Shaham Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving J. Neurosci. 23 2003 742 747 (Pubitemid 36206164)
21. J.M. Gulley, and J.J. Stanis Adaptations in medial prefrontal cortex function associated with amphetamine-induced behavioral sensitization Neuroscience 166 2010 615 624
22. G. Hedou, A.L. Jongen-Relo, C.A. Murphy, C.A. Heidbreder, and J. Feldon Sensitized Fos expression in subterritories of the rat medial prefrontal cortex and nucleus accumbens following amphetamine sensitization as revealed by stereology Brain Res. 950 2002 165 179 (Pubitemid 35253927)
23. H. Horch, A. Kruttgen, S. Portbury, and L. Katz Destabilization of cortical dendrites and spines by BDNF Neuron 23 1999 353 364 (Pubitemid 29315729)
24. B.A. Horger, C.A. Iyasere, M.T. Berhow, C.J. Messer, E.J. Nestler, and J.R. Taylor Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor J. Neurosci. 19 1999 4110 4122 (Pubitemid 29222283)
25. G.W. Huntley, D.L. Benson, E.G. Jones, and P.J. Isackson Developmental expression of brain derived neurotrophic factor mRNA by neurons of fetal and adult monkey prefrontal cortex Brain Res. Dev. Brain Res. 70 1992 53 63
26. P.W. Kalivas, and J.E. Alesdatter Involvement of N-methyl-D-aspartate receptor stimulation in the ventral tegmental area and amygdala in behavioral sensitization to cocaine J. Pharmacol. Exp. Ther. 267 1993 486 495 (Pubitemid 23325044)
27. P.W. Kalivas, and B. Weber Amphetamine injection into the ventral mesencephalon sensitizes rats to peripheral amphetamine and cocaine J. Pharmacol. Exp. Ther. 245 1988 1095 1102
28. H.J. Kang, and E.M. Schuman Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus J. Physiol. 89 1995 11 22
29. J.H. Kim, and P. Vezina Metabotropic glutamate receptors are necessary for sensitization by amphetamine Neuroreport 9 1998 403 406 (Pubitemid 28109195)
30. B. Le Foll, J. Diaz, and P. Sokoloff A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning Neuroreport 16 2005 175 178 (Pubitemid 40250395)
31. V. Lessmann, K. Gottmann, and R. Heumann BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones NeuroReport 6 1994 21 25
32. Y. Li, X.T. Hu, T.G. Berney, A.J. Vartanian, C.D. Stine, M.E. Wolf, and F.J. White Both glutamate receptor antagonists and prefrontal cortex lesions prevent induction of cocaine sensitization and associated neuroadaptations Synapse 34 1999 169 180 (Pubitemid 29508592)
33. G.E. Meredith, S. Callen, and D.A. Scheuer Brain-derived neurotrophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration Brain Res. 949 2002 218 227 (Pubitemid 35246197)
34. M.M. Morshedi, and G.E. Meredith Differential laminar effects of amphetamine on prefrontal parvalbumin interneurons Neuroscience 149 2007 617 624 (Pubitemid 47633022)
35. M.M. Morshedi, and G.E. Meredith Repeated amphetamine administration induces Fos in prefrontal cortical neurons that project to the lateral hypothalamus but not the nucleus accumbens or basolateral amygdala Psychopharmacology (Berl) 197 2008 179 189
36. M.M. Morshedi, D.J. Rademacher, and G.E. Meredith Increased synapses in the medial prefrontal cortex are associated with repeated amphetamine administration Synapse 63 2009 126 135
37. E.M. Nikulina, H.E. Covington 3rd, L. Ganschow, R.P. Hammer Jr., and K.A. Miczek Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: fos in the ventral tegmental area and amygdala Neuroscience 123 2004 857 865 (Pubitemid 38130096)
38. P.E. Paulson, D.M. Camp, and T.E. Robinson Time course of transient behavioral depression and persistent behavioral sensitization in relation to regional brain monoamine concentrations during amphetamine withdrawal in rats Psychopharmacology (Berl) 103 1991 480 492
39. A. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 2007 Elsevier Amsterdam
40. O.T. Phillipson Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat J. Comp. Neurol. 187 1979 117 143
41. L. Pu, Q.S. Liu, and M.M. Poo BDNF-dependent synaptic sensitization in midbrain dopamine neurons after cocaine withdrawal Nat. Neurosci. 9 2006 605 607 (Pubitemid 44012256)
42. T.E. Robinson, and K.C. Berridge The neural basis of drug craving: an incentive-sensitization theory of addiction Brain Res. Brain Res. Rev. 18 1993 247 291 (Pubitemid 23219500)
43. T.E. Robinson, P.A. Jurson, J.A. Bennett, and K.M. Bentgen Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with (+)-amphetamine: a microdialysis study in freely moving rats Brain Res. 462 1988 211 222
44. T.E. Robinson, and B. Kolb Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine Eur. J. Neurosci. 11 1999 1598 1604 (Pubitemid 29192234)
45. S.J. Russo, C.A. Bolanos, D.E. Theobald, N.A. DeCarolis, W. Renthal, A. Kumar, C.A. Winstanley, N.E. Renthal, M.D. Wiley, D.W. Self, D.S. Russell, R.L. Neve, A.J. Eisch, and E.J. Nestler IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates Nat. Neurosci. 10 2007 93 99 (Pubitemid 46026532)
46. S. Schenk, and B. Partridge Sensitization and tolerance in psychostimulant self-administration Pharmacol. Biochem. Behav. 57 1997 543 550 (Pubitemid 27296766)
47. D.S. Segal Behavioral and neurochemical correlates of repeated d-amphetamine administration Adv. Biochem. Psychopharmacol. 13 1975 247 262
48. K.B. Seroogy, K.H. Lundgren, T.M. Tran, K.M. Guthrie, P.J. Isackson, and C.M. Gall Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs J. Comp. Neurol. 342 1994 321 334 (Pubitemid 24105091)
49. S. Sesack, A. Deutch, R. Roth, and B. Bunney Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J. Comp. Neurol. 290 1989 213 242 (Pubitemid 20006320)
50. S.R. Sesack, and V.M. Pickel Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area J. Comp. Neurol. 320 1992 145 160
51. L. Shuster, G. Yu, and A. Bates Sensitization to cocaine stimulation in mice Psychopharmacology (Berl) 52 1977 185 190 (Pubitemid 8090210)
52. L. Sklair-Tavron, W.X. Shi, S.B. Lane, H.W. Harris, B.S. Bunney, and E.J. Nestler Chronic morphine induces visible changes in the morphology of mesolimbic dopamine neurons Proc. Natl. Acad. Sci. U S A 93 1996 11202 11207 (Pubitemid 26333142)
53. Z.Y. Tong, P.G. Overton, and D. Clark Chronic administration of (+)-amphetamine alters the reactivity of midbrain dopaminergic neurons to prefrontal cortex stimulation in the rat Brain Res. 674 1995 63 74
54. T.M. Tzschentke, and W.J. Schmidt Functional heterogeneity of the rat medial prefrontal cortex: effects of discrete subarea-specific lesions on drug-induced conditioned place preference and behavioural sensitization Eur. J. Neurosci. 11 1999 4099 4109 (Pubitemid 29537589)
55. J. Uslaner, A. Badiani, H.E. Day, S.J. Watson, H. Akil, and T.E. Robinson Environmental context modulates the ability of cocaine and amphetamine to induce c-fos mRNA expression in the neocortex, caudate nucleus, and nucleus accumbens Brain Res. 920 2001 106 116 (Pubitemid 33086784)
56. P. Vezina D1 dopamine receptor activation is necessary for the induction of sensitization by amphetamine in the ventral tegmental area J. Neurosci. 16 1996 2411 2420 (Pubitemid 26154350)
57. M.E. Wolf, S.L. Dahlin, X.T. Hu, C.J. Xue, and K. White Effects of lesions of prefrontal cortex, amygdala, or fornix on behavioral sensitization to amphetamine: comparison with N-methyl-D-aspartate antagonists Neuroscience 69 1995 417 439