Enhanced cocaine-induced locomotor sensitization and intrinsic excitability of NAc medium spiny neurons in adult but not in adolescent rats susceptible to diet-induced obesity

Psychopharmacology

Volumn 233, Issue 5, 2016, Pages 773-784

  Oginsky, Max F ^a   Maust, Joel D ^a   Corthell, John T ^a   Ferrario, Carrie R ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Cocaine; Excitability; Nucleus accumbens; Obesity; Sensitization; Striatum

Indexed keywords

COCAINE; CENTRAL STIMULANT AGENT; GLUTAMIC ACID DERIVATIVE;

ACTION POTENTIAL; ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; CONTROLLED STUDY; DIET INDUCED OBESITY; DISEASE PREDISPOSITION; FOOD COMPOSITION; LIMBIC SYSTEM; LOCOMOTION; MALE; MOTIVATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; REWARD; SYNAPTIC TRANSMISSION; WEIGHT GAIN; WHOLE CELL PATCH CLAMP; AGING; ANIMAL; CYTOLOGY; DIET; DOSE RESPONSE; DRUG EFFECTS; GENETICS; MOTOR ACTIVITY; NEOSTRIATUM; NERVE CELL; OBESITY; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AGING; ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; COCAINE; DIET; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTAMATES; MALE; MOTOR ACTIVITY; NEOSTRIATUM; NEURONS; NUCLEUS ACCUMBENS; OBESITY; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION;

EID: 84958108312     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-4157-x     Document Type: Article

References (72)

1. Baladi MG, Koek W, Aumann M, Velasco F, France CP (2012) Eating high fat chow enhances the locomotor-stimulating effects of cocaine in adolescent and adult female rats. Psychopharmacology 222:447-457
2. Baladi MG, Horton RE, Owens WA, Daws LC, France CP (2015) Eating high fat chow decreases dopamine clearance in adolescent and adult male rats but selectively enhances the locomotor stimulating effects of cocaine in adolescents. Int J Neuropsychopharmacol 18
3. Balleine BW (2005) Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits. Physiol Behav 86:717-730
4. Berthoud HR (2012) The neurobiology of food intake in an obesogenic environment. Proc Nutr Soc 71:478-487
5. Boudreau AC, Wolf ME (2005) Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25:9144-9151
6. Burger KS, Stice E (2014) Greater striatopallidal adaptive coding during cue-reward learning and food reward habituation predict future weight gain. NeuroImage 99:122-128
7. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321-352
8. Castro DC, Cole SL, Berridge KC (2015) Lateral hypothalamus, nucleus accumbens, and ventral pallidum roles in eating and hunger: interactions between homeostatic and reward circuitry. Front Syst Neurosci 9:90
9. Cosgrove KP, Veldhuizen MG, Sandiego CM, Morris ED, Small DM (2015) Opposing relationships of BMI with BOLD and dopamine D2/3 receptor binding potential in the dorsal striatum. Synapse 69:195-202
10. Crombag HS, Sutton JM, Takamiya K, Holland PC, Gallagher M, Huganir RL (2008a) A role for alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid GluR1 phosphorylation in the modulatory effects of appetitive reward cues on goal-directed behavior. Eur J Neurosci 27:3284-3291
11. Crombag HS, Sutton JM, Takamiya K, Lee HK, Holland PC, Gallagher M, Huganir RL (2008b) A necessary role for GluR1 serine 831 phosphorylation in appetitive incentive learning. Behav Brain Res 191:178-183
12. Dagher A (2009) The neurobiology of appetite: hunger as addiction. Int J Obes 33(Suppl 2):S30-S33
13. Daws LC, Avison MJ, Robertson SD, Niswender KD, Galli A, Saunders C (2011) Insulin signaling and addiction. Neuropharmacology 61:1123-1128
14. Demos KE, Heatherton TF, Kelley WM (2012) Individual differences in nucleus accumbens activity to food and sexual images predict weight gain and sexual behavior. J Neurosci 32:5549-5552
15. Everitt BJ, Wolf ME (2002) Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22:3312-3320
16. Ferrario CR, Gorny G, Crombag HS, Li Y, Kolb B, Robinson TE (2005) Neural and behavioral plasticity associated with the transition from controlled to escalated cocaine use. Biol Psychiatry 58:751-759
17. Ferrario CR, Li X, Wang X, Reimers JM, Uejima JL, Wolf ME (2010) The role of glutamate receptor redistribution in locomotor sensitization to cocaine. Neuropsychopharmacology 35:818-833
18. Ferrario CR, Loweth JA, Milovanovic M, Ford KA, Galinanes GL, Heng LJ, Tseng KY, Wolf ME (2011) Alterations in AMPA receptor subunits and TARPs in the rat nucleus accumbens related to the formation of Ca(2)(+)-permeable AMPA receptors during the incubation of cocaine craving. Neuropharmacology 61:1141-1151
19. Ferrario CR, Goussakov I, Stutzmann GE, Wolf ME (2012) Withdrawal from cocaine self-administration alters NMDA receptor-mediated Ca2+ entry in nucleus accumbens dendritic spines. PLoS One 7, e40898
20. Figlewicz DP, Szot P, Chavez M, Woods SC, Veith RC (1994) Intraventricular insulin increases dopamine transporter mRNA in rat VTA/substantia nigra. Brain Res 644:331-334
21. Flagel SB, Watson SJ, Akil H, Robinson TE (2008) Individual differences in the attribution of incentive salience to a reward-related cue: influence on cocaine sensitization. Behav Brain Res 186:48-56
22. Geiger BM, Behr GG, Frank LE, Caldera-Siu AD, Beinfeld MC, Kokkotou EG, Pothos EN (2008) Evidence for defective mesolimbic dopamine exocytosis in obesity-prone rats. FASEB J 22:2740-2746
23. Geiger BM, Haburcak M, Avena NM, Moyer MC, Hoebel BG, Pothos EN (2009) Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 159:1193-1199
24. Hryhorczuk C, Florea M, Rodaros D, Poirier I, Daneault C, Des Rosiers C, Arvanitogiannis A, Alquier T, Fulton S (2015) Dampened mesolimbic dopamine function and signaling by saturated but not monounsaturated dietary lipids. Neuropsychopharmacology
25. Hu XT (2007) Cocaine withdrawal and neuro-adaptations in ion channel function. Mol Neurobiol 35:95-112
26. Jansen A, Vanreyten A, van Balveren T, Roefs A, Nederkoorn C, Havermans R (2008) Negative affect and cue-induced overeating in non-eating disordered obesity. Appetite 51:556-562
27. Jensen CD, Kirwan CB (2015) Functional brain response to food images in successful adolescent weight losers compared with normal-weight and overweight controls. Obesity (Silver Spring) 23:630-636
28. Karasinska JM, George SR, Cheng R, O'Dowd BF (2005) Deletion of dopamine D1 and D3 receptors differentially affects spontaneous behaviour and cocaine-induced locomotor activity, reward and CREB phosphorylation. Eur J Neurosci 22:1741-1750
29. Kasanetz F, Manzoni OJ (2009) Maturation of excitatory synaptic transmission of the rat nucleus accumbens from juvenile to adult. J Neurophysiol 101:2516-2527
30. Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27:765-776
31. Kourrich S, Thomas MJ (2009) Similar neurons, opposite adaptations: psychostimulant experience differentially alters firing properties in accumbens core versus shell. J Neurosci 29:12275-12283
32. Kourrich S, Rothwell PE, Klug JR, Thomas MJ (2007) Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci 27:7921-7928
33. Kourrich S, Calu DJ, Bonci A (2015) Intrinsic plasticity: an emerging player in addiction. Nat Rev Neurosci 16:173-184
34. Levin BE, Dunn-Meynell AA, Balkan B, Keesey RE (1997) Selective breeding for diet-induced obesity and resistance in Sprague-Dawley rats. Am J Physiol 273:R725-R730
35. MacQueen JB (1967) Some methods for classification and analysis of multivariate observations proceedings of 5th Berkeley Symposium on Mathematical Statistics and Probability University of California Press pp 281-297
36. Marinelli M, Rudick CN, Hu XT, White FJ (2006) Excitability of dopamine neurons: modulation and physiological consequences. CNS Neurol Disord Drug Targets 5:79-97
37. McCutcheon JE, Marinelli M (2009) Age matters. Eur J Neurosci 29:997-1014
38. McGuire BA, Baladi MG, France CP (2011) Eating high-fat chow enhances sensitization to the effects of methamphetamine on locomotion in rats. Eur J Pharmacol 658:156-159
39. Murdaugh DL, Cox JE, Cook EW 3rd, Weller RE (2012) fMRI reactivity to high-calorie food pictures predicts short- and long-term outcome in a weight-loss program. NeuroImage 59:2709-2721
40. Nisenbaum ES, Wilson CJ (1995) Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 15:4449-4463
41. Perez MF, White FJ, Hu XT (2006) Dopamine D(2) receptor modulation of K(+) channel activity regulates excitability of nucleus accumbens neurons at different membrane potentials. J Neurophysiol 96:2217-2228
42. Perry ML, Leinninger GM, Chen R, Luderman KD, Yang H, Gnegy ME, Myers MG Jr, Kennedy RT (2010) Leptin promotes dopamine transporter and tyrosine hydroxylase activity in the nucleus accumbens of Sprague-Dawley rats. J Neurochem 114:666-674
43. Pulvirenti L, Swerdlow NR, Koob GF (1989) Microinjection of a glutamate antagonist into the nucleus accumbens reduces psychostimulant locomotion in rats. Neurosci Lett 103:213-218
44. Rada P, Bocarsly ME, Barson JR, Hoebel BG, Leibowitz SF (2010) Reduced accumbens dopamine in Sprague-Dawley rats prone to overeating a fat-rich diet. Physiol Behav 101:394-400
45. Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247-291
46. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33-46
47. Robinson MJ, Burghardt PR, Patterson CM, Nobile CW, Akil H, Watson SJ, Berridge KC, Ferrario CR (2015) Individual differences in cue-induced motivation and striatal systems in rats susceptible to diet-induced obesity. Neuropsychopharmacology
48. Scheyer AF, Wolf ME, Tseng KY (2014) A protein synthesis-dependent mechanism sustains calcium-permeable AMPA receptor transmission in nucleus accumbens synapses during withdrawal from cocaine self-administration. J Neurosci 34:3095-3100
49. Sekerli M, Del Negro CA, Lee RH, Butera RJ (2004) Estimating action potential thresholds from neuronal time-series: new metrics and evaluation of methodologies. IEEE Trans Biomed Eng 51:1665-1672
50. Setlow B, Holland PC, Gallagher M (2002) Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive Pavlovian second-order conditioned responses. Behav Neurosci 116:267-275
51. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463
52. Stice E, Dagher A (2010) Genetic variation in dopaminergic reward in humans. Forum Nutr 63:176-185
53. Stice E, Spoor S, Bohon C, Veldhuizen MG, Small DM (2008) Relation of reward from food intake and anticipated food intake to obesity: a functional magnetic resonance imaging study. J Abnorm Psychol 117:924-935
54. Stice E, Yokum S, Bohon C, Marti N, Smolen A (2010) Reward circuitry responsivity to food predicts future increases in body mass: moderating effects of DRD2 and DRD4. NeuroImage 50:1618-1625
55. Stice E, Yokum S, Zald D, Dagher A (2011) Dopamine-based reward circuitry responsivity, genetics, and overeating. Curr Top Behav Neurosci 6:81-93
56. Stice E, Figlewicz DP, Gosnell BA, Levine AS, Pratt WE (2012) The contribution of brain reward circuits to the obesity epidemic. Neurosci Biobehav Rev
57. Stoeckel LE, Weller RE, Cook EW 3rd, Twieg DB, Knowlton RC, Cox JE (2008) Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage 41:636-647
58. Tetley A, Brunstrom J, Griffiths P (2009) Individual differences in food-cue reactivity. The role of BMI and everyday portion-size selections. Appetite 52:614-620
59. Tomasi D, Volkow ND (2013) Striatocortical pathway dysfunction in addiction and obesity: differences and similarities. Crit Rev Biochem Mol Biol 48:1-19
60. Vainik U, Dagher A, Dube L, Fellows LK (2013) Neurobehavioural correlates of body mass index and eating behaviours in adults: a systematic review. Neurosci Biobehav Rev 37:279-299
61. Valenza M, Steardo L, Cottone P, Sabino V (2015) Diet-induced obesity and diet-resistant rats: differences in the rewarding and anorectic effects of D-amphetamine. Psychopharmacology
62. Vanderschuren LJ, Pierce RC (2010) Sensitization processes in drug addiction. Curr Top Behav Neurosci 3:179-195
63. Vezina P (2004) Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci Biobehav Rev 27:827-839
64. Vezina P, Leyton M (2009) Conditioned cues and the expression of stimulant sensitization in animals and humans. Neuropharmacology 56(Suppl 1):160-168
65. Vollbrecht PJ, Mabrouk OS, Nelson AD, Kennedy RT, Ferrario CR (2015a) Interactions between pre-existing differences and junk-food induced alterations in striatal dopamine systems of obesity-prone rats. Obesity (Silver Spring)
66. Vollbrecht PJ, Nobile CW, Chadderdon AM, Jutkiewicz EM, Ferrario CR (2015b) Pre-existing differences in motivation for food and sensitivity to cocaine-induced locomotion in obesity-prone rats. Physiol Behav 152:151-160
67. Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397-2410
68. Wolf ME (2010) The Bermuda triangle of cocaine-induced neuroadaptations. Trends Neurosci 33:391-398
69. Wolf ME, Ferrario CR (2010) AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci Biobehav Rev 35:185-211
70. Wyvell CL, Berridge KC (2000) Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci 20:8122-8130
71. Wyvell CL, Berridge KC (2001) Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. J Neurosci 21:7831-7840
72. Yokum S, Ng J, Stice E (2011) Attentional bias to food images associated with elevated weight and future weight gain: an fMRI study. Obesity (Silver Spring) 19:1775-1783