The rewarding and locomotor-sensitizing effects of repeated cocaine administration are distinct and separable in mice

Neuropharmacology

Volumn 62, Issue 4, 2012, Pages 1858-1866

  Riday, Thorfinn T ^a   Kosofsky, Barry E ^b   Malanga, C J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Brain stimulation reward; CREB; GluR1; GluR2; Intracranial self stimulation; Sensitization

Indexed keywords

AMPA RECEPTOR; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; RECEPTOR SUBUNIT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFECT; ELECTROSTIMULATION; LOCOMOTION; MALE; MOTOR ACTIVITY; MOTOR PERFORMANCE; MOUSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SELF STIMULATION; SENSITIZATION; VENTRAL TEGMENTUM;

ANIMALS; BEHAVIOR, ANIMAL; COCAINE; CORPUS STRIATUM; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOPAMINE UPTAKE INHIBITORS; MALE; MICE; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; RECEPTORS, AMPA; REWARD; VENTRAL TEGMENTAL AREA;

EID: 84856428422     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.12.011     Document Type: Article

References (82)

1. S.H. Ahmed, and M. Cador Dissociation of psychomotor sensitization from compulsive cocaine consumption Neuropsychopharmacology 31 2006 563 571 (Pubitemid 43276972)
2. S.H. Ahmed, P.J. Kenny, G.F. Koob, and A. Markou Neurobiological evidence for hedonic allostasis associated with escalating cocaine use Nat. Neurosci. 5 2002 625 626 (Pubitemid 34742974)
3. R.K. Bachtell, K.H. Choi, D.L. Simmons, E. Falcon, L.M. Monteggia, R.L. Neve, and D.W. Self Role of GluR1 expression in nucleus accumbens neurons in cocaine sensitization and cocaine-seeking behavior Eur. J. Neurosci. 27 2008 2229 2240 (Pubitemid 351590908)
4. P. Bauco, and R.A. Wise Synergistic effects of cocaine with lateral hypothalamic brain stimulation reward: lack of tolerance or sensitization J. Pharmacol. Exp. Ther. 283 1997 1160 1167 (Pubitemid 28016489)
5. P. Bauco, Y. Wang, and R.A. Wise Lack of sensitization or tolerance to the facilitating effect of ventral tegmental area morphine on lateral hypothalamic brain stimulation reward Brain Res. 617 1993 303 308 (Pubitemid 23209797)
6. O. Ben-Shahar, S.H. Ahmed, G.F. Koob, and A. Ettenberg The transition from controlled to compulsive drug use is associated with a loss of sensitization Brain Res. 995 2004 46 54 (Pubitemid 37486014)
7. O. Ben-Shahar, J.M. Moscarello, B. Jacob, M.P. Roarty, and A. Ettenberg Prolonged daily exposure to i.v. cocaine results in tolerance to its stimulant effects Pharmacol. Biochem. Behav. 82 2005 411 416 (Pubitemid 41727954)
8. A.C. Boudreau, and M.E. Wolf Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens J. Neurosci. 25 2005 9144 9151 (Pubitemid 41500822)
9. A.C. Boudreau, J.M. Reimers, M. Milovanovic, and M.E. Wolf Cell surface AMPA receptors in the rat nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases J. Neurosci. 27 2007 10621 10635 (Pubitemid 47502017)
10. W.A. Carlezon Jr., and E.H. Chartoff Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation Nat. Protoc. 2 2007 2987 2995
11. W.A. Carlezon Jr., and E.J. Nestler Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci. 25 2002 610 615 (Pubitemid 35356507)
12. W.A. Carlezon Jr., J. Thome, V.G. Olson, S.B. Lane-Ladd, E.S. Brodkin, N. Hiroi, R.S. Duman, R.L. Neve, and E.J. Nestler Regulation of cocaine reward by CREB Science 282 1998 2272 2275 (Pubitemid 29004079)
13. W.A. Carlezon Jr., M.S. Todtenkopf, D.L. McPhie, P. Pimentel, A.M. Pliakas, J.R. Stellar, and M. Trzcinska Repeated exposure to rewarding brain stimulation downregulates GluR1 expression in the ventral tegmental area Neuropsychopharmacology 25 2001 234 241 (Pubitemid 32566345)
14. B.T. Chen, M.S. Bowers, M. Martin, F.W. Hopf, A.M. Guillory, R.M. Carelli, J.K. Chou, and A. Bonci Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA Neuron 59 2008 288 297 (Pubitemid 352033682)
15. E. Childs, M. Shoaib, and I.P. Stolerman Cocaine self-administration in rats with histories of cocaine exposure and discrimination Psychopharmacology (Berl.) 186 2006 168 176 (Pubitemid 43727333)
16. L. Churchill, C.J. Swanson, M. Urbina, and P.W. Kalivas Repeated cocaine alters glutamate receptor subunit levels in the nucleus accumbens and ventral tegmental area of rats that develop behavioral sensitization J. Neurochem. 72 1999 2397 2403 (Pubitemid 29242190)
17. J.A. Dinieri, C.L. Nemeth, A. Parsegian, T. Carle, V.V. Gurevich, E. Gurevich, R.L. Neve, E.J. Nestler, and W.A. Carlezon Jr. Altered sensitivity to rewarding and aversive drugs in mice with inducible disruption of cAMP response element-binding protein function within the nucleus accumbens J. Neurosci. 29 2009 1855 1859
18. Y. Dong, T. Green, D. Saal, H. Marie, R. Neve, E.J. Nestler, and R.C. Malenka CREB modulates excitability of nucleus accumbens neurons Nat. Neurosci. 9 2006 475 477
19. R. Esposito, and C. Kornetsky Morphine lowering of self-stimulation thresholds: lack of tolerance with long-term administration Science 195 1977 189 191 (Pubitemid 8012001)
20. L.W. Fitzgerald, J. Ortiz, A.G. Hamedani, and E.J. Nestler Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents J. Neurosci. 16 1996 274 282
21. R.A. Frank, S. Martz, and T. Pommering The effect of chronic cocaine on self-stimulation train-duration thresholds Pharmacol. Biochem. Behav. 29 1988 755 758 (Pubitemid 19260920)
22. C.R. Gallistel Self-stimulation in the rat: quantitative characteristics of the reward pathway J. Comp. Physiol. Psychol. 92 1978 977 998 (Pubitemid 9078992)
23. B. Gilliss, C.J. Malanga, J.O. Pieper, and W.A. Carlezon Jr. Cocaine and SKF-82958 potentiate brain stimulation reward in Swiss-Webster mice Psychopharmacology (Berl.) 163 2002 238 248 (Pubitemid 35013616)
24. J. Henning, D. Koczan, A. Glass, T. Karopka, J. Pahnke, A. Rolfs, R. Benecke, and U. Gimsa Deep brain stimulation in a rat model modulates TH, CaMKIIa and Homer1 gene expression Eur. J. Neurosci. 25 2007 239 250 (Pubitemid 46096238)
25. B.A. Horger, K. Shelton, and S. Schenk Preexposure sensitizes rats to the rewarding effects of cocaine Pharmacol. Biochem. Behav. 37 1990 707 711
26. C.B. Hubner, and J.E. Moreton Effects of selective D1 and D2 dopamine antagonists on cocaine self-administration in the rat Psychopharmacology (Berl.) 105 1991 151 156
27. S.E. Hyman, and E.J. Nestler Initiation and adaptation: a paradigm for understanding psychotropic drug action Am. J. Psychiatry 153 1996 151 162 (Pubitemid 26038955)
28. P.W. Kalivas, and N.D. Volkow The neural basis of addiction: a pathology of motivation and choice Am. J. Psychiatry 162 2005 1403 1413 (Pubitemid 41105554)
29. P.J. Kenny, G.F. Koob, and A. Markou Conditioned facilitation of brain reward function after repeated cocaine administration Behav. Neurosci. 117 2003 1103 1107 (Pubitemid 37243792)
30. P.J. Kenny, S.A. Chen, O. Kitamura, A. Markou, and G.F. Koob Conditioned withdrawal drives heroin consumption and decreases reward sensitivity J. Neurosci. 26 2006 5894 5900 (Pubitemid 44318354)
31. P.J. Kenny Brain reward systems and compulsive drug use Trends Pharmacol. Sci. 28 2007 135 141 (Pubitemid 46283593)
32. L.A. Knackstedt, and P.W. Kalivas Extended access to cocaine self-administration enhances drug-primed reinstatement but not behavioral sensitization J. Pharmacol. Exp. Ther. 322 2007 1103 1109 (Pubitemid 47295776)
33. T.E. Koeltzow, and P. Vezina Locomotor activity and cocaine-seeking behavior during acquisition and reinstatement of operant self-administration behavior in rats Behav. Brain Res. 160 2005 250 259 (Pubitemid 40603521)
34. L. Kokkinidis, and R.M. Zacharko Enhanced self-stimulation responding from the substantia nigra after chronic amphetamine treatment: a role for conditioning factors Pharmacol. Biochem. Behav. 12 1980 543 547 (Pubitemid 10070121)
35. G.F. Koob, and M. Le Moal Review. Neurobiological mechanisms for opponent motivational processes in addiction Philos. Trans. R Soc. Lond B. Biol. Sci. 363 2008 3113 3123
36. C. Kornetsky, and G. Bain Brain-stimulation reward: a model for the study of the rewarding effects of abused drugs NIDA Res. Monogr. 124 1992 73 93 (Pubitemid 23081975)
37. C. Kornetsky, and C. Duvauchelle Dopamine, a common substrate for the rewarding effects of brain stimulation reward, cocaine, and morphine NIDA Res. Monogr. 145 1994 19 39
38. S. Kourrich, P.E. Rothwell, J.R. Klug, and M.J. Thomas Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens J. Neurosci. 27 2007 7921 7928 (Pubitemid 47173313)
39. C.M. Lack, S.R. Jones, and D.C. Roberts Increased breakpoints on a progressive ratio schedule reinforced by IV cocaine are associated with reduced locomotor activation and reduced dopamine efflux in nucleus accumbens shell in rats Psychopharmacology (Berl.) 195 2008 517 525 (Pubitemid 350161771)
40. D. Lecca, F. Cacciapaglia, V. Valentini, E. Acquas, and G. Di Chiara Differential neurochemical and behavioral adaptation to cocaine after response contingent and noncontingent exposure in the rat Psychopharmacology (Berl.) 191 2007 653 667 (Pubitemid 46355877)
41. B.T. Lett Repeated exposures intensify rather than diminish the rewarding effects of amphetamine, morphine, and cocaine Psychopharmacology (Berl.) 98 1989 357 362 (Pubitemid 19162424)
42. D. Levy, M. Shabat-Simon, U. Shalev, N. Barnea-Ygael, A. Cooper, and A. Zangen Repeated electrical stimulation of reward-related brain regions affects cocaine but not "natural" reinforcement J. Neurosci. 27 2007 14179 14189 (Pubitemid 351377870)
43. D.S. Lorrain, G.M. Arnold, and P. Vezina Previous exposure to amphetamine increases incentive to obtain the drug: long-lasting effects revealed by the progressive ratio schedule Behav. Brain Res. 107 2000 9 19
44. W. Lu, L.M. Monteggia, and M.E. Wolf Repeated administration of amphetamine or cocaine does not alter AMPA receptor subunit expression in the rat midbrain Neuropsychopharmacology 26 2002 1 13 (Pubitemid 34075271)
45. L. Lu, J.W. Grimm, Y. Shaham, and B.T. Hope Molecular neuroadaptations in the accumbens and ventral tegmental area during the first 90 days of forced abstinence from cocaine self-administration in rats J. Neurochem. 85 2003 1604 1613 (Pubitemid 36702572)
46. A. Mendrek, C.D. Blaha, and A.G. Phillips Pre-exposure of rats to amphetamine sensitizes self-administration of this drug under a progressive ratio schedule Psychopharmacology (Berl.) 135 1998 416 422 (Pubitemid 28254849)
47. E. Miliaressis, P.P. Rompre, P. Laviolette, L. Philippe, and D. Coulombe The curve-shift paradigm in self-stimulation Physiol. Behav. 37 1986 85 91 (Pubitemid 16121802)
48. C. Nocjar, and J. Panksepp Chronic intermittent amphetamine pretreatment enhances future appetitive behavior for drug- and natural-reward: interaction with environmental variables Behav. Brain Res. 128 2002 189 203 (Pubitemid 34051574)
49. J. Olds, and P. Milner Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain J. Comp. Physiol. Psychol. 47 1954 419 427
50. V.G. Olson, C.P. Zabetian, C.A. Bolanos, S. Edwards, M. Barrot, A.J. Eisch, T. Hughes, D.W. Self, R.L. Neve, and E.J. Nestler Regulation of drug reward by cAMP response element-binding protein: evidence for two functionally distinct subregions of the ventral tegmental area J. Neurosci. 25 2005 5553 5562 (Pubitemid 40800647)
51. G.T. Paxinos, and K.B. Franklin The Mouse Brain in Stereotaxic Coordinates 1996 Academic Press San Diego
52. A.G. Phillips, and P. Di Ciano Behavioral sensitization is induced by intravenous self-administration of cocaine by rats Psychopharmacology (Berl.) 124 1996 279 281 (Pubitemid 26130539)
53. P.V. Piazza, J.M. Deminiere, M. le Moal, and H. Simon Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration Brain Res. 514 1990 22 26 (Pubitemid 20147583)
54. R.C. Pierce, K. Bell, P. Duffy, and P.W. Kalivas Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization J. Neurosci. 16 1996 1550 1560 (Pubitemid 26145933)
55. P.J. Pierre, and P. Vezina Predisposition to self-administer amphetamine: the contribution of response to novelty and prior exposure to the drug Psychopharmacology (Berl.) 129 1997 277 284 (Pubitemid 27085399)
56. N.R. Richardson, and D.C. Roberts Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy J. Neurosci. Methods 66 1996 1 11 (Pubitemid 26180064)
57. 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)
58. T.E. Robinson, and K.C. Berridge Review. The incentive sensitization theory of addiction: some current issues Philos. Trans. R Soc. Lond B. Biol. Sci. 363 2008 3137 3146
59. D. Saal, Y. Dong, A. Bonci, and R.C. Malenka Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons Neuron 37 2003 577 582 (Pubitemid 36262980)
60. N. Sakai, J. Thome, S.S. Newton, J. Chen, M.B. Kelz, C. Steffen, E.J. Nestler, and R.S. Duman Inducible and brain region-specific CREB transgenic mice Mol. Pharmacol. 61 2002 1453 1464 (Pubitemid 34575756)
61. S. Schenk, and B. Partridge Sensitization to cocaine's reinforcing effects produced by various cocaine pretreatment regimens in rats Pharmacol. Biochem. Behav. 66 2000 765 770 (Pubitemid 30639471)
62. T. Schulte, S. Brecht, T. Herdegen, M. Illert, H.M. Mehdorn, and W. Hamel Induction of immediate early gene expression by high-frequency stimulation of the subthalamic nucleus in rats Neuroscience 138 2006 1377 1385 (Pubitemid 43363553)
63. G. Schulteis, and J. Liu Brain reward deficits accompany withdrawal (hangover) from acute ethanol in rats Alcohol 39 2006 21 28 (Pubitemid 44287278)
64. G. Schulteis, A. Markou, M. Cole, and G.F. Koob Decreased brain reward produced by ethanol withdrawal Proc. Natl. Acad. Sci. U S A 92 1995 5880 5884
65. T.S. Shippenberg, and C. Heidbreder Sensitization to the conditioned rewarding effects of cocaine: pharmacological and temporal characteristics J. Pharmacol. Exp. Ther. 273 1995 808 815
66. A.K. Stoker, and A. Markou Withdrawal from chronic cocaine administration induces deficits in brain reward function in C57BL/6J mice Behav. Brain Res. 223 2011 176 181
67. M.A. Sutton, E.F. Schmidt, K.H. Choi, C.A. Schad, K. Whisler, D. Simmons, D.A. Karanian, L.M. Monteggia, R.L. Neve, and D.W. Self Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour Nature 421 2003 70 75 (Pubitemid 36077086)
68. M.J. Thomas, R.C. Malenka, and A. Bonci Modulation of long-term depression by dopamine in the mesolimbic system J. Neurosci. 20 2000 5581 5586 (Pubitemid 30636883)
69. M.J. Thomas, C. Beurrier, A. Bonci, and R.C. Malenka Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine Nat. Neurosci. 4 2001 1217 1223 (Pubitemid 33135627)
70. M.S. Todtenkopf, A. Parsegian, A. Naydenov, R.L. Neve, C. Konradi, and W.A. Carlezon Jr. Brain reward regulated by AMPA receptor subunits in nucleus accumbens shell J. Neurosci. 26 2006 11665 11669 (Pubitemid 44772138)
71. M.A. Ungless, J.L. Whistler, R.C. Malenka, and A. Bonci Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons Nature 411 2001 583 587 (Pubitemid 32531404)
72. C.L. Walters, and J.A. Blendy Different requirements for cAMP response element binding protein in positive and negative reinforcing properties of drugs of abuse J. Neurosci. 21 2001 9438 9444 (Pubitemid 33096887)
73. C.L. Walters, Y.C. Kuo, and J.A. Blendy Differential distribution of CREB in the mesolimbic dopamine reward pathway J. Neurochem. 87 2003 1237 1244 (Pubitemid 37485079)
74. F.J. White, X.T. Hu, X.F. Zhang, and M.E. Wolf Repeated administration of cocaine or amphetamine alters neuronal responses to glutamate in the mesoaccumbens dopamine system J. Pharmacol. Exp. Ther. 273 1995 445 454
75. R.A. Wise, and E. Munn Effects of repeated amphetamine injections on lateral hypothalamic brain stimulation reward and subsequent locomotion Behav. Brain Res. 55 1993 195 201 (Pubitemid 23217491)
76. R.A. Wise, P. Newton, K. Leeb, B. Burnette, D. Pocock, and J.B. Justice Jr. Fluctuations in nucleus accumbens dopamine concentration during intravenous cocaine self-administration in rats Psychopharmacology (Berl.) 120 1995 10 20
77. R.A. Wise Addictive drugs and brain stimulation reward Annu. Rev. Neurosci. 19 1996 319 340 (Pubitemid 26080832)
78. R.A. Wise Drug-activation of brain reward pathways Drug Alcohol Depend. 51 1998 13 22 (Pubitemid 28353753)
79. R.A. Wise Forebrain substrates of reward and motivation J. Comp. Neurol. 493 2005 115 121 (Pubitemid 41636193)
80. R.A. Yokel, and R.A. Wise Increased lever pressing for amphetamine after pimozide in rats: implications for a dopamine theory of reward Science 187 1975 547 549
81. A. Zapata, V.I. Chefer, R. Ator, T.S. Shippenberg, and B.A. Rocha Behavioural sensitization and enhanced dopamine response in the nucleus accumbens after intravenous cocaine self-administration in mice Eur. J. Neurosci. 17 2003 590 596 (Pubitemid 36255895)
82. X.F. Zhang, X.T. Hu, F.J. White, and M.E. Wolf Increased responsiveness of ventral tegmental area dopamine neurons to glutamate after repeated administration of cocaine or amphetamine is transient and selectively involves AMPA receptors J. Pharmacol. Exp. Ther. 281 1997 699 706 (Pubitemid 27203801)