Neuroplasticity in the Mesolimbic System Induced by Natural Reward and Subsequent Reward Abstinence

Biological Psychiatry

Volumn 67, Issue 9, 2010, Pages 872-879

  Pitchers, Kyle K ^a   Balfour, Margaret E ^b   Lehman, Michael N ^a   Richtand, Neil M ^b,c,d   Yu, Lei ^b   Coolen, Lique M ^a  

^a WESTERN UNIVERSITY   (Canada)

^b UNIVERSITY OF CINCINNATI   (United States)

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

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Dendritic spine; dopamine; nucleus accumbens; psychostimulant; sexual behavior; substance abuse

Indexed keywords

DEXAMPHETAMINE;

ABSTINENCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; LIMBIC CORTEX; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; REWARD; SENSITIZATION; SEXUAL BEHAVIOR;

AMIDINES; AMPHETAMINE; ANALYSIS OF VARIANCE; ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; CONDITIONING, OPERANT; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; LIMBIC SYSTEM; MALE; MOTOR ACTIVITY; NEURONAL PLASTICITY; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SEXUAL BEHAVIOR, ANIMAL; SILVER STAINING; TIME FACTORS;

EID: 77950367941     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.09.036     Document Type: Article

References (94)

1. Pucilowski O., and Kostowski W. Aggressive behaviour and the central serotonergic systems. Behav Brain Res 9 (1983) 33-48
2. Hernandez L., and Hoebel B.G. Feeding and hypothalamic stimulation increase dopamine turnover in the accumbens. Physiol Behav 44 (1988) 599-606
3. Noel M.B., and Wise R.A. Ventral tegmental injections of a selective mu or delta opioid enhance feeding in food-deprived rats. Brain Res 673 (1995) 304-312
4. Martel P., and Fantino M. Influence of the amount of food ingested on mesolimbic dopaminergic system activity: A microdialysis study. Pharmacol Biochem Behav 55 (1996) 297-302
5. Martel P., and Fantino M. Mesolimbic dopaminergic system activity as a function of food reward: A microdialysis study. Pharmacol Biochem Behav 53 (1996) 221-226
6. Avena N.M., Rada P., and Hoebel B.G. Evidence for sugar addiction: Behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32 (2008) 20-39
7. Avena N.M., Rada P., and Hoebel B.G. Sugar and fat bingeing have notable differences in addictive-like behavior. J Nutr 139 (2009) 623-628
8. Yoshida M., Yokoo H., Mizoguchi K., Kawahara H., Tsuda A., Nishikawa T., et al. Eating and drinking cause increased dopamine release in the nucleus accumbens and ventral tegmental area in the rat: Measurement by in vivo microdialysis. Neurosci Lett 139 (1992) 73-76
9. Pfaus J.G., Damsma G., Nomikos G.G., Wenkstern D.G., Blaha C.D., Phillips A.G., et al. Sexual behavior enhances central dopamine transmission in the male rat. Brain Res 530 (1990) 345-348
10. Balfour M.E., Yu L., and Coolen L.M. Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats. Neuropsychopharmacology 29 (2004) 718-730
11. Kohlert J.G., and Meisel R.L. Sexual experience sensitizes mating-related nucleus accumbens dopamine responses of female Syrian hamsters. Behav Brain Res 99 (1999) 45-52
12. Young L.J., Lim M.M., Gingrich B., and Insel T.R. Cellular mechanisms of social attachment. Horm Behav 40 (2001) 133-138
13. Young L.J., and Wang Z. The neurobiology of pair bonding. Nat Neurosci 7 (2004) 1048-1054
14. Wise R.A., and Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol Rev 94 (1987) 469-492
15. Di Chiara G., and Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 85 (1988) 5274-5278
16. Robinson T.E., and Kolb B. 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
17. Robinson T.E., Gorny G., Mitton E., and Kolb B. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39 (2001) 257-266
18. Meredith G.E., Ypma P., and Zahm D.S. Effects of dopamine depletion on the morphology of medium spiny neurons in the shell and core of the rat nucleus accumbens. J Neurosci 15 (1995) 3808-3820
19. Post R.M., and Rose H. Increasing effects of repetitive cocaine administration in the rat. Nature 260 (1976) 731-732
20. Segal D.S., and Mandell A.J. Long-term administration of d-amphetamine: Progressive augmentation of motor activity and stereotypy. Pharmacol Biochem Behav 2 (1974) 249-255
21. Kalivas P.W., and Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Brain Res Rev 16 (1991) 223-244
22. Lett B.T. Repeated exposures intensify rather than diminish the rewarding effects of amphetamine, morphine, and cocaine. Psychopharmacology 98 (1989) 357-362
23. Shippenberg T.S., and Heidbreder C. Sensitization to the conditioned rewarding effects of cocaine: Pharmacological and temporal characteristics. J Pharmacol Exp Ther 273 (1995) 808-815
24. Shippenberg T.S., Heidbreder C., and Lefevour A. Sensitization to the conditioned rewarding effects of morphine: Pharmacology and temporal characteristics. Eur J Pharmacol 299 (1996) 33-39
25. Crombag H.S., Bossert J.M., Koya E., and Shaham Y. Review. Context-induced relapse to drug seeking: A review. Philos Trans R Soc Lond 363 (2008) 3233-3243
26. Robinson T.E., and Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47 suppl 1 (2004) 33-46
27. Li Y., Kolb B., and Robinson T.E. The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen. Neuropsychopharmacology 28 (2003) 1082-1085
28. Robinson T.E., Gorny G., Savage V.R., and Kolb B. Widespread but regionally specific effects of experimenter-versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 46 (2002) 271-279
29. Brown R.W., and Kolb B. Nicotine sensitization increases dendritic length and spine density in the nucleus accumbens and cingulate cortex. Brain Res 899 (2001) 94-100
30. Robinson T.E., and Kolb B. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17 (1997) 8491-8497
31. Sarti F., Borgland S.L., Kharazia V.N., and Bonci A. Acute cocaine exposure alters spine density and long-term potentiation in the ventral tegmental area. Eur J Neurosci 26 (2007) 749-756
32. Bowers M.S., McFarland K., Lake R.W., Peterson Y.K., Lapish C.C., Gregory M.L., et al. Activator of G protein signaling 3: A gatekeeper of cocaine sensitization and drug seeking. Neuron 42 (2004) 269-281
33. Lu L., Hope B.T., Dempsey J., Liu S.Y., Bossert J.M., and Shaham Y. Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat Neurosci 8 (2005) 212-219
34. McClung C.A., and Nestler E.J. Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6 (2003) 1208-1215
35. McClung C.A., and Nestler E.J. Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 33 (2008) 3-17
36. Saal D., Dong Y., Bonci A., and Malenka R.C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37 (2003) 577-582
37. Nugent F.S., and Kauer J.A. LTP of GABAergic synapses in the ventral tegmental area and beyond. J Physiol 586 (2008) 1487-1493
38. Nugent F.S., Penick E.C., and Kauer J.A. Opioids block long-term potentiation of inhibitory synapses. Nature 446 (2007) 1086-1090
39. Kauer J.A. Addictive drugs and stress trigger a common change at VTA synapses. Neuron 37 (2003) 549-550
40. Kauer J.A., and Malenka R.C. Synaptic plasticity and addiction. Nat Rev 8 (2007) 844-858
41. Liu Q.S., Pu L., and Poo M.M. Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437 (2005) 1027-1031
42. Thomas M.J., Beurrier C., Bonci A., and Malenka R.C. Long-term depression in the nucleus accumbens: A neural correlate of behavioral sensitization to cocaine. Nat Neurosci 4 (2001) 1217-1223
43. Thomas M.J., and Malenka R.C. Synaptic plasticity in the mesolimbic dopamine system. Philos Trans R Soc Lond 358 (2003) 815-819
44. Thomas M.J., Malenka R.C., and Bonci A. Modulation of long-term depression by dopamine in the mesolimbic system. J Neurosci 20 (2000) 5581-5586
45. Thierry A.M., Tassin J.P., Blanc G., and Glowinski J. Selective activation of mesocortical DA system by stress. Nature 263 (1976) 242-244
46. de Jong J.G., Wasilewski M., van der Vegt B.J., Buwalda B., and Koolhaas J.M. A single social defeat induces short-lasting behavioral sensitization to amphetamine. Physiol Behav 83 (2005) 805-811
47. Tidey J.W., and Miczek K.A. Social defeat stress selectively alters mesocorticolimbic dopamine release: An in vivo microdialysis study. Brain Res 721 (1996) 140-149
48. Mathews I.Z., Mills R.G., and McCormick C.M. Chronic social stress in adolescence influenced both amphetamine conditioned place preference and locomotor sensitization. Dev Psychobiol 50 (2008) 451-459
49. Yap J.J., Covington III H.E., Gale M.C., Datta R., and Miczek K.A. Behavioral sensitization due to social defeat stress in mice: Antagonism at mGluR5 and NMDA receptors. Psychopharmacology 179 (2005) 230-239
50. Miczek K.A., Covington III H.E., Nikulina Jr. E.M., and Hammer R.P. Aggression and defeat: Persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27 (2004) 787-802
51. Robinson T.E., and Berridge K.C. The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18 (1993) 247-291
52. Leri F., Flores J., Rodaros D., and Stewart J. Blockade of stress-induced but not cocaine-induced reinstatement by infusion of noradrenergic antagonists into the bed nucleus of the stria terminalis or the central nucleus of the amygdala. J Neurosci 22 (2002) 5713-5718
53. Marinelli M., and Piazza P.V. Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci 16 (2002) 387-394
54. Piazza P.V., and Le Moal M. The role of stress in drug self-administration. Trends Pharmacol Sci 19 (1998) 67-74
55. Meisel R.L., and Mullins A.J. Sexual experience in female rodents: Cellular mechanisms and functional consequences. Brain Res 1126 (2006) 56-65
56. Wallace D.L., Vialou V., Rios L., Carle-Florence T.L., Chakravarty S., Kumar A., et al. The influence of DeltaFosB in the nucleus accumbens on natural reward-related behavior. J Neurosci 28 (2008) 10272-10277
57. Wolf M.E., Sun X., Mangiavacchi S., and Chao S.Z. Psychomotor stimulants and neuronal plasticity. Neuropharmacology 47 suppl 1 (2004) 61-79
58. Thomas M.J., Kalivas P.W., and Shaham Y. Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br J Pharmacol 154 (2008) 327-342
59. Nestler E.J. Molecular basis of long-term plasticity underlying addiction. Nat Rev 2 (2001) 119-128
60. Segal D.S., and Kuczenski R. Individual differences in responsiveness to single and repeated amphetamine administration: Behavioral characteristics and neurochemical correlates. J Pharmacol Exp Ther 242 (1987) 917-926
61. Pritchard L.M., Logue A.D., Hayes S., Welge J.A., Xu M., Zhang J., et al. 7-OH-DPAT and PD 128907 selectively activate the D3 dopamine receptor in a novel environment. Neuropsychopharmacology 28 (2003) 100-107
62. Pugh B.C., and Rossi M.L. A paraffin wax technique of Golgi-Cox impregnated CNS that permits the joint application of other histological and immunocytochemical techniques. J Neural Transm Suppl 39 (1993) 97-105
63. Uylings H.B., and van Pelt J. Measures for quantifying dendritic arborizations. Network 13 (2002) 397-414
64. Hyman S.E., Malenka R.C., and Nestler E.J. Neural mechanisms of addiction: The role of reward-related learning and memory. Annu Rev Neurosci 29 (2006) 565-598
65. Della Maggiore V., and Ralph M.R. The effect of amphetamine on locomotion depends on the motor device utilized. The open field vs. the running wheel. Pharmacol Biochem Behav 65 (2000) 585-590
66. Aragona B.J., Detwiler J.M., and Wang Z. Amphetamine reward in the monogamous prairie vole. Neurosci Lett 418 (2007) 190-194
67. Avena N.M., and Hoebel B.G. Amphetamine-sensitized rats show sugar-induced hyperactivity (cross-sensitization) and sugar hyperphagia. Pharmacol Biochem Behav 74 (2003) 635-639
68. Fiorino D.F., and Phillips A.G. Facilitation of sexual behavior and enhanced dopamine efflux in the nucleus accumbens of male rats after D-amphetamine-induced behavioral sensitization. J Neurosci 19 (1999) 456-463
69. Barr A.M., Fiorino D.F., and Phillips A.G. Effects of withdrawal from an escalating dose schedule of d-amphetamine on sexual behavior in the male rat. Pharmacol Biochem Behav 64 (1999) 597-604
70. Mitchell J.B., and Stewart J. Facilitation of sexual behaviors in the male rat in the presence of stimuli previously paired with systemic injections of morphine. Pharmacol Biochem Behav 35 (1990) 367-372
71. Bradley K.C., and Meisel R.L. Sexual behavior induction of c-Fos in the nucleus accumbens and amphetamine-stimulated locomotor activity are sensitized by previous sexual experience in female Syrian hamsters. J Neurosci 21 (2001) 2123-2130
72. Castner S.A., Xiao L., and Becker J.B. Sex differences in striatal dopamine: In vivo microdialysis and behavioral studies. Brain Res 610 (1993) 127-134
73. Becker J.B., Molenda H., and Hummer D.L. Gender differences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Ann N Y Acad Sci 937 (2001) 172-187
74. Grimm J.W., Hope B.T., Wise R.A., and Shaham Y. Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412 (2001) 141-142
75. Agmo A. Copulation-contingent aversive conditioning and sexual incentive motivation in male rats: Evidence for a two-stage process of sexual behavior. Physiol Behav 77 (2002) 425-435
76. Chang F.L., and Greenough W.T. Lateralized effects of monocular training on dendritic branching in adult split-brain rats. Brain Res 232 (1982) 283-292
77. Van Reempts J., Dikova M., Werbrouck L., Clincke G., and Borgers M. Synaptic plasticity in rat hippocampus associated with learning. Behav Brain Res 51 (1992) 179-183
78. Nestler E.J., and Aghajanian G.K. Molecular and cellular basis of addiction. Science 278 (1997) 58-63
79. Norrholm S.D., Bibb J.A., Nestler E.J., Ouimet C.C., Taylor J.R., and Greengard P. Cocaine-induced proliferation of dendritic spines in nucleus accumbens is dependent on the activity of cyclin-dependent kinase-5. Neuroscience 116 (2003) 19-22
80. Rosenzweig M.R., and Bennett E.L. Psychobiology of plasticity: Effects of training and experience on brain and behavior. Behav Brain Res 78 (1996) 57-65
81. Adams V.L., Goodman R.L., Salm A.K., Coolen L.M., Karsch F.J., and Lehman M.N. Morphological plasticity in the neural circuitry responsible for seasonal breeding in the ewe. Endocrinology 147 (2006) 4843-4851
82. Jansen H.T., Cutter C., Hardy S., Lehman M.N., and Goodman R.L. Seasonal plasticity within the gonadotropin-releasing hormone (GnRH) system of the ewe: Changes in identified GnRH inputs and glial association. Endocrinology 144 (2003) 3663-3676
83. Lamprecht R., and LeDoux J. Structural plasticity and memory. Nat Rev 5 (2004) 45-54
84. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci 10 (1990) 1286-1291
85. Woolley C.S., Gould E., Frankfurt M., and McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10 (1990) 4035-4039
86. de Castilhos J., Forti C.D., Achaval M., and Rasia-Filho A.A. Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: A Golgi study. Brain Res 1240 (2008) 73-81
87. Schwarz J.M., Liang S.L., Thompson S.M., and McCarthy M.M. Estradiol induces hypothalamic dendritic spines by enhancing glutamate release: A mechanism for organizational sex differences. Neuron 58 (2008) 584-598
88. Dalla C., Whetstone A.S., Hodes G.E., and Shors T.J. Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci Lett 449 (2009) 52-56
89. Robinson T.E., and Kolb B. Morphine alters the structure of neurons in the nucleus accumbens and neocortex of rats. Synapse 33 (1999) 160-162
90. Vezina P., Giovino A.A., Wise R.A., and Stewart J. Environment-specific cross-sensitization between the locomotor activating effects of morphine and amphetamine. Pharmacol Biochem Behav 32 (1989) 581-584
91. Cunningham S.T., Finn M., and Kelley A.E. Sensitization of the locomotor response to psychostimulants after repeated opiate exposure: Role of the nucleus accumbens. Neuropsychopharmacology 16 (1997) 147-155
92. Spanagel R., and Shippenberg T.S. Modulation of morphine-induced sensitization by endogenous kappa opioid systems in the rat. Neurosci Lett 153 (1993) 232-236
93. Singer B.F., Tanabe L.M., Gorny G., Jake-Matthews C., Li Y., Kolb B., and Vezina P. Amphetamine-induced changes in dendritic morphology in rat forebrain correspond to associative drug conditioning rather than nonassociative drug sensitization. Biol Psychiatry 65 (2009) 835-840
94. Pulipparacharuvil S., Renthal W., Hale C.F., Taniguchi M., Xiao G., Kumar A., et al. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59 (2008) 621-633