Involvement of nucleus accumbens AMPA receptor trafficking in augmentation of D- amphetamine reward in food-restricted rats

Psychopharmacology

Volumn 231, Issue 15, 2014, Pages 3055-3063

  Peng, Xing Xiang ^a   Cabeza De Vaca, Soledad ^a   Ziff, Edward B ^a   Carr, Kenneth D ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Alexandria Center for Life Sciences   (United States)

Author keywords

1 NASPM; AMPA receptors; d amphetamine; Food restriction; GluA1; Nucleus accumbens; Postsynaptic density; Reward; Self stimulation

Indexed keywords

AMPA RECEPTOR; DEXAMPHETAMINE; PROTEIN GLUA1; PROTEIN GLUA2; PROTEIN GLUA3; SERINE; UNCLASSIFIED DRUG; 1-NAPHTHYLACETYLSPERMINE; AMINO ACID RECEPTOR BLOCKING AGENT; CENTRAL STIMULANT AGENT; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 3; SPERMINE;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CELL FRACTIONATION; CONTROLLED STUDY; DIET RESTRICTION; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; REWARD; SELF STIMULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; FOOD DEPRIVATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; DEXTROAMPHETAMINE; EXCITATORY AMINO ACID ANTAGONISTS; FOOD DEPRIVATION; MALE; NUCLEUS ACCUMBENS; PROTEIN TRANSPORT; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; REWARD; SELF STIMULATION; SPERMINE;

EID: 84904423083     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-014-3476-7     Document Type: Article

References (90)

1. Austin SB, Gortmaker SL (2001) Dieting and smoking initiation in early adolescent girls and boys: a prospective study. Am J Public Health 91:446-450 (Pubitemid 32179461)
2. Avena NM, Rada P, Hoebel BG (2008) Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32:20-39 (Pubitemid 350160955)
3. Barry MR, Ziff EB (2002) Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12:279-286
4. Bell SM, Stewart RB, Thompson SC, Meisch RA (1997) Food-deprivation increases cocaine-induced conditioned place preference and locomotor activity in rats. Psychopharmacology 131:1-8 (Pubitemid 27242848)
5. Bernard V, Somogyi P, Bolam JP (1997) Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat. J Neurosci 17:819-833 (Pubitemid 27024593)
6. Boehm J, Kang M-G, Johnson RC, Esteban J, Rl H, Malinow R (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51:213-225 (Pubitemid 44041865)
7. Boudreau AC, Wolf ME (2005) Behavioral sensitization to cocaine associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25:9144-9151 (Pubitemid 41500822)
8. Cabeza de Vaca S, Carr KD (1998) Food restriction enhances the central rewarding effect of abused drugs. J Neurosci 18:7502-7510
9. Cabeza de Vaca S, Krahne L, Carr KD (2004) A progressive ratio schedule of self- stimulation testing reveals profound augmentation of d-amphetamine reward by food restriction but no effect of a "sensitizing" regimen of d-amphetamine. Psychopharmacology 175:106-113 (Pubitemid 39215537)
10. Cardinal RN, Everitt BJ (2004) Neural and psychological mechanisms underlying appetitive learning: links to drug addiction. Curr Opin Neurobiol 14:156-162 (Pubitemid 38479931)
11. Carr KD (2011) Food scarcity, neuroadaptations, and the pathogenic potential of dieting in an unnatural ecology: compulsive eating and drug abuse. Physiol Behav 104:162-167
12. Carr KD, Tsimberg Y, Berman Y, Yamamoto N (2003) Evidence of increased dopamine receptor signaling in food-restricted rats. Neuroscience 119:1157-1167 (Pubitemid 36776461)
13. Carr KD, Cabeza de Vaca S, Sun Y, Chau LS (2009) Reward-potentiating effects of D-1 dopamine receptor agonist and AMPA GluR1 antagonist in nucleus accumbens shell are increased by food restriction; possible relevance to enhancement of adaptive and maladaptive reward-directed behavior. Psychopharmacology 202:731-743
14. Carr KD, Chau LS, de Vaca C, Gustafson K, Stouffer M, Tukey DS, Restituito S, Ziff EB (2010) AMPA receptor subunit GluR1 downstream of D-1 dopamine receptor stimulation in nucleus accumbens shell mediates increased drug reward magnitude in food-restricted rats. Neuroscience 165:1074-1086
15. Carroll ME, Meisch RA (1984) Increased drug-reinforced behavior due to food deprivation. Adv Behav Pharmacol 4:47-88
16. Chao SZ, Ariano MA, Peterson DA, Wolf ME (2002) D1 dopamine receptor stimulation increases GluR1 surface expression in nucleus accumbens neurons. J Neurochem 83:704-712 (Pubitemid 35231824)
17. Cheskin LJ, Hess JM, Henningfield J, Gorelick DA (2005) Calorie restriction increases cigarette use in adult smokers. Psychopharmacology 179:430-436 (Pubitemid 40569046)
18. Choquet D (2010) Fast AMPAR trafficking for a high-frequency synaptic transmission. Eur J Neurosci 32:250-260
19. Conason A, Teixeira J, Hsu CH, Puma L, Knafo D, Geliebter A (2013) Substance use following bariatric weight loss surgery. JAMA Surg 148:145-150
20. Conrad KL, Tseng KY, Uejima JL, Reimers JM, Heng L-J, Shaham Y, Marinelli M, Wolf ME (2008) Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 454:118-121 (Pubitemid 351931970)
21. Consoli D, Contarino A, Tabarin A, Drago F (2009) Binge-like eating in mice. Int J Eat Disord 42:402-408
22. Cornish JL, Kalivas PW (2000) Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction. J Neurosci 20:RC89
23. Dalley JW, Laane K, Theobald DEH, Armstrong HC, Corlett PR, Chudasama Y, Robbins TW (2005) Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc Natl Acad Sci U S A 102:6189-6194 (Pubitemid 40594276)
24. D'Cunha TM, Sedki F, Macri J, Casola C, Shalev U (2013) The effects of chronic food restriction on cue-induced heroin seeking in abstinent male rats. Psychopharmacology 225:241-250
25. Deroche V, Marinelli M, Maccari S, Le Moal M, Simon H, Piazza PV (1995) Stress-induced sensitization and glucocorticoids: I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion. J Neurosci 15:7181-7188 (Pubitemid 3010056)
26. Di Chiara G (2005) Dopamine in disturbances of food and drug-motivated behavior: a case of homology? Physiol Behav 86:9-10
27. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D (2007) Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54:447-460 (Pubitemid 46659808)
28. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143 (Pubitemid 36182782)
29. Famous KR, Kumaresan V, Sadri-Vakili G, Schmidt HD, Mierke DF, Cha JH, Pierce RC (2008) Phosphorylation-dependent trafficking of GluR2-containing AMPA receptors in the nucleus accumbens plays a critical role in the reinstatement of cocaine seeking. J Neurosci 28:11061-11070
30. Ferrario CR, Li X, Wolf ME (2011) Effects of acute cocaine or dopamine receptor agonists on AMPA receptor distribution in the rat nucleus accumbens. Synapse 65:54-63
31. French SA, Perry CL, Leon GR, Fulkerson JA (1994) Weight concerns, dieting behavior, and smoking initiation among adolescents: a prospective study. Am J Public Health 84:1818-1820 (Pubitemid 24355650)
32. Glass MJ, Lane DA, Colago EEO, Chan J, Schlussman SD, Zhou Y, Kreek MJ, Pickel VM (2008) Chronic administration of morphine is associated with a decrease in surface AMPA GluR1 receptor subunit in dopamine D1 receptor expressing neurons in the shell and non-D1 receptor expressing neurons in the core of the rat nucleus accumbens. Exp Neurol 210:750-761
33. Goel A, Jiang B, Xu LW, Song L, Kirkwood A, Lee HK (2006) Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nat Neurosci 9:1001-1003 (Pubitemid 44264910)
34. Groenewegen HJ, Wright CI, Beijer AV, Voorn P (1999) Convergence and segregation of ventral striatal inputs and outputs. Ann N Y Acad Sci 877:49-63 (Pubitemid 29351850)
35. Haberny SL, Carr KD (2005a) Comparison of basal and D-1 dopamine receptor agonist-stimulated neuropeptide gene expression in caudate-putamen and nucleus accumbens of ad libitum fed and food-restricted rats. Mol Brain Res 141:121-127 (Pubitemid 41608692)
36. Haberny SL, Carr KD (2005b) Food restriction increases NMDA receptor-mediated CaMK II and NMDA receptor/ERK 1/2-mediated CREB phosphorylation in nucleus accumbens upon D-1 dopamine receptor stimulation in rats. Neuroscience 132:1035-1043
37. Haberny S, Berman Y, Meller E, Carr KD (2004) Chronic food restriction increases D-1 dopamine receptor agonist-induced ERK1/2 MAP kinase and CREB phosphorylation in caudate-putamen and nucleus accumbens. Neuroscience 125:289-298 (Pubitemid 38402181)
38. Hagan MM, Moss DE (1997) Persistence of binge-eating patterns after a history of restriction with intermittent bouts of refeeding on palatable food in rats: implications for bulimia nervosa. Int J Eat Disord 22:411-420 (Pubitemid 27459521)
39. Hajnal A, Smith GP, Norgren R (2004) Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol - Reg Integr Comp Physiol 286:R31-R37
40. He K, Song L, Cummings LW, Goldman J, Huganir RL, Lee HK (2009) Stabilization of Ca2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation. Proc Natl Acad Sci 106:20033-20038
41. He K, Goel A, Ciarkowski CE, Song L, Lee HK (2011) Brain area specific regulation of synaptic AMPA receptors by phosphorylation. Commun Integr Biol 4:569-572
42. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Ann Rev Neurosci 29:565-598 (Pubitemid 44476856)
43. Ivezaj V, Saules KK, Wiedemann AA (2012) "I didn't see this coming.": why are postbariatric patients in substance abuse treatment? Patients' perceptions of etiology and future recommendations. Obes Surg 22:1308-1314
44. Jitsuki S, Takemoto K, Kawasaki T, Tada H, Takahashi A, Becamel C, Sano A, Yuzaki M, Zukin RS, Ziff EB, Kessels HW, Takahashi T (2011) Serotonin mediates cross-modal reorganization of cortical circuits. Neuron 69:780-792
45. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, Neubert TA (2004) Identification and verification of novel rodent postsynaptic density proteins. Mol Cell Proteomics 3:857-871 (Pubitemid 39369199)
46. Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27:765-776
47. Kelley AE, Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306-3303
48. Kenny PJ (2011) Reward mechanisms in obesity: new insights and future directions. Neuron 69:664-679
49. Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340-350
50. Koike M, Iino M, Ozawa S (1997) Blocking effect of 1-naphthyl acetyl spermine on Ca2+-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 29:27-36 (Pubitemid 27365675)
51. Krahn D, Kurth C, Demitrack M, Drewnowski A (1992) The relationship of dieting severity and bulimic behaviors to alcohol and other drug use in young women. J Subst Abuse 4:341-353
52. Lee HK (2012) Ca-permeable AMPA receptors in homeostatic synaptic plasticity. Front Mol Neurosci 5(17):1-11
53. Li D, Herrera S, Bubula N, Nikitina E, Palmer AA, Hanck DA, Loweth JA, Vezina P (2011) Casein kinase 1 enables nucleus accumbens amphetamine-induced locomotion by regulating AMPA receptor phosphorylation. J Neurochem 118:237-247
54. Liu S, Zheng D, Peng XX, Cabeza de Vaca S, Carr KD (2011) Enhanced cocaine-conditioned place preference and associated brain regional levels of BDNF, p-ERK1/2 and p-Ser845-GluA1 in food-restricted rats. Brain Res 1400:31-41
55. Lobo MK, Covington HE 3rd, Chaudhury D, Friedman AK, Sun H, Damez-Werno D, Dietz DM, Zaman S, Koo JW, Kennedy PJ, Mouzon E, Mogri M, Neve RL, Deisseroth K, Han MH, Nestler EJ (2010) Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330:385-390
56. Man HY (2011) GluA2-lacking, calcium-permeable AMPA receptors-inducers of plasticity? Curr Opin Neurobiol 21:291-298
57. Man HY, Sekine-Aizawa Y, Huganir RL (2007) Regulation of {alpha}-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc Natl Acad Sci 104:3579-3584 (Pubitemid 46364201)
58. Mangiavacchi S, Wolf ME (2004) D1 dopamine receptor stimulation increases the rate of AMPA receptor insertion onto the surface of cultured nucleus accumbens neurons through a pathway dependent on protein kinase A. J Neurochem 88:1261-1271 (Pubitemid 38280694)
59. Moyer JT, Wolf JA, Finkel LH (2007) Effects of dopaminergic modulation on the integrative properties of the ventral striatal medium spiny neuron. J Neurophysiol 98:3731-3748
60. Nedelescu H, Kelso CM, Lázaro-Muñoz G, Purpura M, Cain CK, Ledoux JE, Aoki C (2010) Endogenous GluR1-containing AMPA receptors translocate to asymmetric synapses in the lateral amygdala during the early phase of fear memory formation: an electron microscopic immunocytochemical study. J Comp Neurol 518:4723-4739
61. Nelson CL, Milovanovic M, Wetter JB, Ford KA, Wolf ME (2009) Behavioral sensitization to amphetamine is not accompanied by changes in glutamate receptor surface expression in the rat nucleus accumbens. J Neurochem 109:35-51
62. Oh MC, Derkach VA, Guire ES, Soderling TR (2006) Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J Biol Chem 281:752-758
63. Ozawa S, Kamiya H, Tsuzuki K (1998) Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54:581-618 (Pubitemid 28123327)
64. Palmiter RD (2007) Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci 30:375-381
65. Pan Y, Haberny LY, Berman Y, Meller E, Carr KD (2006) Synthesis, protein levels and phosphorylation state of tyrosine hydroxylase in mesoaccumbens and nigrostriatal dopamine pathways of chronically food-restricted rats. Brain Res 1122:135-142 (Pubitemid 44708112)
66. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic, San Diego
67. Peng XX, Ziff EB, Carr KD (2011) Effects of food restriction and sucrose intake on synaptic delivery of AMPA receptors in nucleus accumbens. Synapse 65:1024-1031
68. Pisetsky EM, Chao YM, Dierker LC, May AM, Striegel-Moore RH (2008) Disordered eating and substance use in high-school students: results from the Youth Risk Behavior Surveillance System. Int J Eat Disord 41:464-470 (Pubitemid 351874988)
69. Pontieri FE, 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 92:12304-12308
70. Pothos EN, Creese I, Hoebel BG (1995) Restricted eating with weight loss selectively decreases extracellular dopamine in the nucleus accumbens and alters dopamine response to amphetamine, morphine, and food intake. J Neurosci 15:6640-6650
71. Reimers JM, Milovanovic M, Wolf ME (2011) Quantitative analysis of AMPA receptor subunit composition in addiction-related brain regions. Brain Res 1367:223-233
72. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, Huganir RL (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16:1179-1188 (Pubitemid 26227239)
73. Root TL, Pinheiro AP, Thornton L, Strober M, Fernandez-Aranda F, Brandt H, Crawford S, Fichter MM, Halmi KA, Johnson C, Kaplan AS, Klump KL, La Via M, Mitchell J, Woodside DB, Rotondo A, Berrettini WH, Kaye WH, Bulik CM (2010) Substance use disorders in women with anorexia nervosa. Int J Eat Disord 43:14-21
74. Rosse R, Deutsch S, Chilton M (2005) Cocaine addicts prone to cocaine-induced psychosis have lower bodymass index than cocaine addicts resistant to cocaine-induced psychosis - implications for the cocaine model of psychosis proneness. Isr J Psychiatry Relat Sci 42:45-50 (Pubitemid 41159763)
75. Shepherd JD (2012) Memory, plasticity and sleep - a role for calcium permeable AMPA receptors? Front Mol Neurosci 5(49):1-5
76. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343 (Pubitemid 32455340)
77. Simon GE, Von Korff M, Saunders K, Miglioretti DL, Crane PK, van Belle G, Kessler RC (2006) Association between obesity and psychiatric disorders in the US adult population. Arch Gen Psychiatry 63:824-830
78. Stamp JA, Mashoodh R, van Kampen JM, Robertson HA (2008) Food restriction enhances peak corticosterone levels, cocaine-induced locomotor activity, and DeltaFosB expression in the nucleus accumbens of the rat. Brain Res 1204:94-101
79. Stouffer M, Carr KD, Rice ME (2012) Insulin-induced increase in striatal dopamine release are enhanced by chronic food restriction and blunted by an obesogenic diet. Soc Neurosci Abstr 283:06
80. Stuber GD, Evans SB, Higgins MS, Pu Y, Figlewicz DP (2002) Food restriction modulates amphetamine-conditioned place preference and nucleus accumbens dopamine release in the rat. Synapse 46:83-90
81. Surmeier J, Ding J, Day M, Wang Z, Shen W (2007) D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 30:228-235 (Pubitemid 46654239)
82. Tsubokawa H, Oguro K, Masuzawa T, Nakaima T, Kawai N (1995) Effects of a spider toxin and its analogue on glutamate-activated currents in the hippocampal CA1 neuron after ischemia. J Neurophysiol 74:218-225
83. Volkow ND, Wang G-J, Fowler JS, Telang F (2008) Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Brit 363:3191-3200
84. Warren M, Frost-Pineda K, Gold M (2005) Body mass index and marijuana use. J Addict Dis 24:95-100 (Pubitemid 41542397)
85. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097 (Pubitemid 44300229)
86. Wiederman MW, Pryor T (1996) Substance abuse and impulsive behaviors among adolescents with eating disorders. Addict Behav 21:269-272 (Pubitemid 26106576)
87. Wise RA, Bozarth MA (1985) Brain mechanisms of drug reward and euphoria. Psychiatr Med 3:445-460
88. Wolf JA, Moyer JT, Maciej T, Lazarewicz DC, Benoit-Marand M, O'Donnell P, Finkel LH (2005) NMDA/AMPA ratio impacts state transitions and entrainment to oscillations in a computational model of the nucleus accumbens medium spiny projection neuron. J Neurosci 25:9080-9095 (Pubitemid 41509041)
89. Zheng D, Cabeza de Vaca S, Carr KD (2012) Food restriction increases acquisition, persistence and drug prime-induced expression of a cocaine-conditioned place preference in rats. Pharmacol Biochem Behav 100:538-544
90. Zheng D, Liu S, Cabeza de Vaca S, Carr KD (2013) Effects of time of feeding on psychostimulant reward, conditioned place preference, metabolic hormone levels, and nucleus accumbens biochemical measures in food-restricted rats. Psychopharmacology 227:307-320