Habitual responding for alcohol depends upon both AMPA and D2 receptor signaling in the dorsolateral striatum

Frontiers in Behavioral Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Corbit, Laura H ^a   Nie, Hong ^b   Janak, Patricia H ^b,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Devaluation; Dopamine; Dorsal striatum; Glutamate; Habit learning; Rat

Indexed keywords

EID: 84906919420     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00301     Document Type: Article

References (47)

1. Adams, C. D. (1982). Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q. J. Exp. Psychol. 34B, 77-98.
2. Anzalone, A., Lizardi-Ortiz, J. E., Ramos, M., De Mei, C., Hopf, F. W., Iaccarino, C., et al. (2012). Dual control of dopamine synthesis and release by presynaptic and postsynaptic dopamine D2 receptors. J. Neurosci. 32, 9023-9034. doi: 10. 1523/jneurosci.0918-12.2012
3. Ashby, F. G., Turner, B. O., and Horvitz, J. C. (2010). Cortical and basal ganglia contributions to hait learning and automaticity. Trends Cogn. Sci. 14, 208-215. doi: 10.1016/j.tics.2010.02.001
4. Barnes, T. D., Kubota, Y., Hu, D., Jin, D. Z., and Graybiel, A. M. (2005). Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437, 1158-1161. doi: 10.1038/nature04053
5. Belin, D., and Everitt, B. J. (2008). Cocaine seeking habits depend upon dopaminedependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57, 432-441. doi: 10.1016/j.neuron.2007.12.019
6. Carelli, R. M., Wolske, M., and West, M. O. (1997). Loss of lever press-related firing of rat striatal forelimb neurons after repeated sessions in a lever pressing task. J. Neurosci. 17, 1804-1814.
7. Choi, W. Y., Balsam, P. D., and Horvitz, J. C. (2005). Extended habit training reduces dopamine mediation of appetitive response expression. J. Neurosci. 25, 6729-6733. doi: 10.1523/jneurosci.1498-05.2005
8. Corbit, L. H., Chieng, B. C., and Balleine, B. W. (2014). Effects of repeated cocaine exposure on habit learning and reversal by N-acetylcysteine. Neuropsycho pharmacology 39, 1893-1901. doi: 10.1038/npp.2014.37
9. Corbit, L. H., and Janak, P. H. (2007a). Ethanol-associated cues produce general pavlovian-instrumental transfer. Alcohol. Clin. Exp. Res. 31, 766-774. doi: 10. 1111/j.1530-0277.2007.00359.x
10. Corbit, L. H., and Janak, P. H. (2007b). Inactivation of the lateral but not medial dorsal striatum eliminates the excitatory impact of Pavlovian stimuli on instrumental responding. J. Neurosci. 27, 13977-13981. doi: 10.1523/JNEUROSCI. 4097-07.2007
11. Corbit, L. H., Nie, H., and Janak, P. H. (2012). Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol. Psychiatry 72, 389-395. doi: 10.1016/j.biopsych.2012.02.024
12. Czachowski, C. L., Chappell, A. M., and Samson, H. H. (2001). Effects of raclopride in the nucleus accumbens on ethanol seeking and consumption. Alcohol. Clin. Exp. Res. 25, 1431-1440. doi: 10.1111/j.1530-0277.2001.tb02144.x
13. Dias-Ferreira, E., Susa, J. C., Melo, I., Morgado, P., Mesquita, A. R., Cerqueira, J. J., et al. (2009). Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325, 621-625. doi: 10.1126/science.1171203
14. Dickinson, A., Smith, J., and Mirenowicz, J. (2000). Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav. Neurosci. 114, 468-483. doi: 10.1037/0735-7044.114.3.468
15. Faure, A., Haberland, U., Conde, F., and El Massioui, N. (2005). Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J. Neurosci. 25, 2771-2780. doi: 10.1523/jneurosci.3894-04.2005
16. Floyer-Lea, A., and Matthews, P. M. (2005). Distinguishable brain activation networks for short-and long-term motor skill learning. J. Neurophysiol. 94, 512-518. doi: 10.1152/jn.00717.2004
17. Furlong, T. M., Jayaweera, H. K., Balleine, B. W., and Corbit, L. H. (2014). Binge-like consumption of a palatable food accelerates habitual control of behavior and is dependent on activation of the dorsolateral striatum. J. Neurosci. 34, 5012-5022. doi: 10.1523/JNEUROSCI.3707-13.2014
18. Hogarth, L., Field, M., and Rose, A. K. (2013). Phasic transition from goaldirected to habitual control over drug-seeking produced by conflicting reinforcer expectancy. Addict. Biol. 18, 88-97. doi: 10.1111/adb.12009
19. Jahanshahi, M., and Frith, C. D. (1998). Willed action and its impairments. Cogn. Neuropsychol. 15, 483-533. doi: 10.1080/026432998381005
20. Jeanblanc, J., He, D. Y., McGough, N. N., Logrip, M. L., Phamluong, K., Janak, P. H., et al. (2006). The dopamine D3 receptor is part of a homeostatic pathway regulating ethanol consumption. J. Neurosci. 26, 1457-1464. doi: 10. 1523/jneurosci.3786-05.2006
21. Johnson, P. M., and Kenny, P. J. (2010). Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat. Neurosci. 13, 635-641. doi: 10.1038/nn.2519
22. Joyce, J. N., Loeschen, S. K., and Marshall, J. F. (1985). Dopamine D-2 receptors in rat caudate-putamen: the lateral to medial gradient does not correspond to dopaminergic innervation. Brain Res. 338, 209-218. doi: 10.1016/00068993(85)90149-0
23. Karni, A., Meyer, G., Jezzard, P., Adams, M. M., Turner, R., and Ungerleider, L. G. (1995). Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155-158. doi: 10.1038/377155a0
24. Lê, A. D., and Shaham, Y. (2002). Neurobiology of relapse to alcohol in rats. Pharmacol. Ther. 94, 137-156. doi: 10.1016/s0163-7258(02)00200-0
25. LeBlanc, K. H., Maidment, N. T., and Ostlund, S. B. (2013). Repeated cocaine exposure facilitates the expression of incentive motivation and induces habitual control in rats. PLoS One 8:e61355. doi: 10.1371/journal.pone.0061355
26. Loeber, S., Croissant, B., Heinz, A., Mann, K., and Flor, H. (2006). Cue exposure in the treatment of alcohol dependence: effects on drinking outcome, craving and self-efficacy. Br. J. Clin. Psychol. 45, 515-529. doi: 10.1348/014466505x 82586
27. Nelson, A., and Killcross, S. (2006). Amphetamine exposure enhances habit formation. J. Neurosci. 26, 3805-3812. doi: 10.1523/jneurosci.4305-05.2006
28. Nelson, A. J., and Killcross, S. (2013). Accelerated habit formation following amphetamine exposure is reversed by D1, but enhanced by D2, receptor antagonists. Front. Neurosci. 7:76. doi: 10.3389/fnins.2013.00076
29. Nordquist, R. E., Voorn, P., de Mooij-Van Malsen, J. G., Joosten, R. N., Pennartz, C. M., and Vanderschuren, L. J. (2007). Augmented reinforcer value and accelerated habit formation after repeated amphetamine treatment. Eur. Neuropsychopharmacol. 17, 532-540. doi: 10.1016/j.euroneuro.2006.12.005
30. Ostlund, S. B., Maidment, N. T., and Balleine, B. W. (2010). Alcohol-paired contextual cues produce an immediate and selective loss of goal-directed action in rats. Front. Integr. Neurosci. 4:19. doi: 10.3389/fnint.2010.00019
31. Park, K., Volkow, N. D., Pan, Y., and Du, C. (2013). Chronic cocaine dampens dopamine signaling during cocaine intoxication and unbalances D1 over D2 receptor signaling. J. Neurosci. 33, 15827-15836. doi: 10.1523/JNEUROSCI.1935-13.2013
32. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates. 4th Edn. San Diego: Academic.
33. Salamone, J. D., Cousins, M. S., and Snyder, B. J. (1997). Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci. Biobehav. Rev. 21, 341-359. doi: 10.1016/s01497634(96)00017-6
34. Schultz, W. (2007). Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259-288. doi: 10.1146/annurev.neuro.28.061604. 135722
35. Tang, C., Pawlak, A. P., Prokopenko, V., and West, M. O. (2007). Changes in activity of the striatum during formation of a motor habit. Eur. J. Neurosci. 25, 1212-1227. doi: 10.1111/j.1460-9568.2007.05353.x
36. Vanderschuren, L. J., Di Ciano, P., and Everitt, B. J. (2005). Involvement of the dorsal striatum in cue-controlled cocaine seeking. J. Neurosci. 25, 8665-8670. doi: 10.1523/jneurosci.0925-05.2005
37. Vanderschuren, L. J., and Everitt, B. J. (2005). Behavioral and neural mechanisms of compulsive drug seeking. Eur. J. Pharmacol. 526, 77-88. doi: 10.1016/j.ejphar. 2005.09.037
38. Volkow, N. D., Fowler, J. S., Wang, G. J., Hitzemann, R., Logan, J., Schlyer, D. J., et al. (1993). Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14, 169-177. doi: 10.1002/syn. 890140210
39. Volkow, N. D., Wang, G. J., Telang, F., Fowler, J. S., Logan, J., Childress, A. R., et al. (2006). Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J. Neurosci. 26, 6583-6588. doi: 10.1523/jneurosci.1544-06. 2006
40. Wang, J., Carnicella, S., Phamluong, K., Jeanblanc, J., Ronesi, J. A., Chaudhri, N., et al. (2007). Ethanol induces long-term facilitation of NR2B-NMDA receptor activity in the dorsal striatum: implications for alcohol drinking behavior. J. Neurosci. 27, 3593-3602. doi: 10.1523/jneurosci.4749-06.2007
41. Wickens, J. R., Horvitz, J. C., Costa, R. M., and Killcross, S. (2007). Dopaminergic mechanisms in actions and habits. J. Neurosci. 27, 8181-8183. doi: 10. 1523/jneurosci.1671-07.2007
42. Wickens, J. R., Reynolds, J. N., and Hyland, B. I. (2003). Neural mechanisms of reward-related motor learning. Curr. Opin. Neurobiol. 13, 685-690. doi: 10. 1016/j.conb.2003.10.013
43. Willuhn, I., Burgeno, L. M., Groblewski, P. A., and Phillips, P. E. (2014). Excessive cocaine use results from decreased phasic dopamine signaling in the striatum. Nat. Neurosci. 17, 704-709. doi: 10.1038/nn.3694
44. Wilson, C. J., Chang, H. T., and Kitai, S. T. (1983). Disfacilitation and long-lasting inhibition of neostriatal neurons in the rat. Exp. Brain Res. 51, 227-235. doi: 10. 1007/bf00237198
45. Yin, H. H., Knowlton, B. J., and Balleine, B. W. (2004). Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 19, 181-189. doi: 10.1111/j.1460-9568.2004. 03095.x
46. Yin, H. H., Mulcare, S. P., Hilário, M. R., Clouse, E., Holloway, T., Davis, M. I., et al. (2009). Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333-341. doi: 10.1038/ nn.2261
47. Zapata, A., Minney, V. L., and Shippenberg, T. S. (2010). Shift from goaldirected to habitual cocaine seeking after prolonged experience in rats. J. Neurosci. 30, 15457-15463. doi: 10.1523/JNEUROSCI.4072-10.2010