Optogenetics reveals a role for accumbal medium spiny neurons expressing dopamine D2 receptors in cocaine-induced behavioral sensitization

Frontiers in Behavioral Neuroscience

Volumn 8, Issue OCT, 2014, Pages 1-11

  Song, Shelly Sooyun ^a   Kang, Byeong Jun ^a   Lee, Hyo Jin ^a   Sim, Hye Ri ^a   Kim, Tae Hyong ^a   Yoon, Sehyoun ^a   Yoon, Bong June ^a   Baik, Ja Hyun ^a   Wen, Lei ^b,c,d   Augustine, George J ^b,c,d  

^a Korea University   (South Korea)

^b Korea Institute of Science and Technology   (South Korea)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Cocaine; Dopamine D2 receptors; Drug addiction; Medium spiny neurons; Optogenetics

Indexed keywords

COCAINE; DOPAMINE 2 RECEPTOR; RHODOPSIN; VIRUS VECTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; COCAINE DEPENDENCE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EVOKED INHIBITORY POSTSYNAPTIC CURRENT; HABITUATION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; IMMUNOFLUORESCENCE; IN VIVO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; LATENT PERIOD; MEDIUM SPINY NERVE CELL; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; PHENOTYPIC PLASTICITY; PHOTOSTIMULATION; PROTEIN EXPRESSION; RELAPSE; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; WITHDRAWAL SYNDROME;

EID: 84908011634     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00336     Document Type: Article

References (46)

1. Baik, J. H. (2013). Dopamine signaling in reward-related behaviors. Front. Neural Circuits 7:152. doi: 10.3389/fncir.2013.00152
2. Baik, J. H., Picetti, R., Saiardi, A., Thiriet, G., Dierich, A., Depaulis, A., et al. (1995). Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors. Nature 377, 424-428. doi: 10.1038/377424a0
3. Berridge, K. C. (2007). The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 191, 391-431. doi: 10.1007/s00213-006-0578-x
4. Bock, R., Shin, J. H., Kaplan, A. R., Dobi, A., Markey, E., Kramer, P. F., et al. (2013). Strenghtening the accumbal indirect pathway promotes resilience to compulsive cocaine use. Nat. Neurosci. 16, 632-638. doi: 10.1038/nn.3369
5. Bocklisch, C., Pascoli, V., Wong, J. C., House, D. R., Yvon, C., de Roo, M., et al. (2013). Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science 341, 1521-1525. doi: 10.1126/science.1237059
6. Boudreau, A. C., Reimers, J. M., Milovanovic, M., and Wolf, M. E. (2007). 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, 10621-10635. doi: 10.1523/jneurosci.2163-07.2007
7. Boudreau, A. C., and Wolf, M. E. (2005). Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J. Neurosci. 25, 9144-9151. doi: 10.1523/jneurosci.2252-05.2005
8. Chandra, R., Lenz, J. D., Gancarz, A. M., Chaudhury, D., Schroeder, G. L., Han, M. H., et al. (2013). Optogenetic inhibition of D1R containing nucleus accumbens neurons alters cocaine-mediated regulation of Tiam1. Front. Mol. Neurosci. 6:13. doi: 10.3389/fnmol.2013.00013
9. Chang, H. T., and Kitai, S. T. (1985). Projection neurons of the nucleus accumbens: an intracellular labeling study. Brain Res. 347, 112-116. doi: 10.1016/0006-8993(85)90894-7
10. Chausmer, A. L., Elmer, G. I., Rubinstein, M., Low, M. J., Grandy, D. K., and Katz, J. L. (2002). Cocaine-induced locomotor activity and cocaine discrimination in dopamine D2 receptor mutant mice. Psychopharmacology (Berl)163, 54-61. doi: 10.1007/s00213-002-1142-y
11. Chevalier, G., and Deniau, J. M. (1990). Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13, 277-280. doi: 10.1016/0166-2236(90)90109-n
12. Czubayko, U., and Plenz, D. (2002). Fast synaptic transmission between striatal spiny projection neurons. Proc. Natl. Acad. Sci. U S A 99, 15764-15769. doi: 10.1073/pnas.242428599
13. Ferguson, S. M., Eskenazi, D., Ishikawa, M., Wanat, M. J., Phillips, P. E., Dong, Y., et al. (2011). Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat. Neurosci. 14, 22-24. doi: 10.1038/nn.2703
14. Goto, Y., and Grace, A. A. (2005). Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat. Neurosci. 8, 805-812. doi: 10.1038/nn1471
15. Grofová, I. (1975). The identification of striatal and pallidal neurons projecting to substantia nigra. An experimental study by means of retrograde axonal transport of horseradish peroxidase. Brain Res. 91, 286-291. doi: 10.1016/0006-8993(75)90550-8
16. Grueter, B. A., Robison, A. J., Neve, R. L., Nestler, E. J., and Malenka, R. C. (2013). ΔFosB differentially modulates nucleus accumbens direct and indirect pathway function. Proc. Natl. Acad. Sci. U S A 110, 1923-1928. doi: 10.1073/pnas.1221742110
17. Gustafson, N., Gireesh-Dharmaraj, E., Czubayko, U., Blackwell, K. T., and Plenz, D. (2006). A comparative voltage and current-clamp analysis of feedback and feedforward synaptic transmission in the striatal microcircuit in vitro.J. Neurophysiol. 95, 737-752. doi: 10.1152/jn.00802.2005
18. Hikida, T., Kimura, K., Wada, N., Funabiki, K., and Nakanishi, S. (2010). Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66, 896-907. doi: 10.1016/j.neuron.2010.05.011
19. Kalivas, P. W., and Duffy, P. (1990). Effect of acute and daily cocaine treatment on extracellular dopamine in the nucleus accumbens. Synapse 5, 48-58. doi: 10.1002/syn.890050104
20. Kalivas, P. W., Pierce, R. C., Cornish, J., and Sorg, B. A. (1998). A role for sensitization in craving and relapse in cocaine addiction. J. Psychopharmacol. 12, 49-53. doi: 10.1177/026988119801200107
21. Koos, T., Tepper, J. M., and Wilson, C. J. (2004). Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J. Neurosci. 24, 7916-7922. doi: 10.1523/jneurosci.2163-04.2004
22. Kourrich, S., Rothwell, P. E., Klug, J. R., and Thomas, M. J. (2007). Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J. Neurosci. 27, 7921-7928. doi: 10.1523/jneurosci.1859-07.2007
23. Kravitz, A. V., Freeze, B. S., Parker, P. R., Kay, K., Thwin, M. T., Deisseroth, K., et al. (2010). Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622-626. doi: 10.1038/nature09159
24. Kravitz, A. V., Tye, L. D., and Kreitzer, A. C. (2012). Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat. Neurosci. 15, 816-818. doi: 10.1038/nn.3100
25. Kreitzer, A. C., and Malenka, R. C. (2008). Striatal plasticity and basal ganglia circuit function. Nature 60, 543-554. doi: 10.1016/j.neuron.2008.11.005
26. Le Moine, C., and Bloch, B. (1996). Expression of the D3 dopamine receptor in peptidergic neurons of the nucleus accumbens: comparison with the D1 and D2 dopamine receptors. Neuroscience 73, 131-143. doi: 10.1016/0306-4522(96)00029-2
27. Lobo, M. K., Covington, H. E. 3rd, Chaudhury, D., Friedman, A. K., Sun, H., Damez-Werno, D., et al. (2010). Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390. doi: 10.1126/science.1188472
28. Lobo, M. K., and Nestler, E. J. (2011). The striatal balancing act in drug addiction: distinct roles of direct and indirect pathway medium spiny neurons. Front. Neuroanat. 5:41. doi: 10.3389/fnana.2011.00041
29. Lüscher, C., and Malenka, R. C. (2011). Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69, 650-663. doi: 10.1016/j.neuron.2011.01.017
30. O'Donnell, P., and Grace, A. A. (1993). Physiological and morphological properties of accumbens core and shell neurons recorded in vitro. Synapse 13, 135-160. doi: 10.1002/syn.890130206
31. Pascoli, V., Turiault, M., and Lüscher, C. (2011). Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 481, 71-75. doi: 10.1038/nature10709
32. Preston, R. J., Bishop, G. A., and Kitai, S. T. (1980). Medium spiny neuron projection from the rat neostriatum: an intracellular horseradish peroxidase study. Brain Res. 183, 253-263. doi: 10.1016/0006-8993(80)90462-x
33. Robinson, T. E., and Berridge, K. C. (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 18, 247-291. doi: 10.1016/0165-0173(93)90013-p
34. Robinson, T. E., and Berridge, K. C. (2003). Addiction. Annu. Rev. Psychol. 54, 25-53. doi: 10.1146/annurev.psych.54.101601.145237
35. Schmidt, H. D., and Pierce, R. C. (2010). Cocaine-induced neuroadaptations in glutamate transmission: potential therapeutic targets for craving and addiction. Ann. N Y Acad. Sci. 1187, 35-75. doi: 10.1111/j.1749-6632.2009.05144.x
36. Sesack, S. R., and Grace, A. A. (2010). Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35, 27-47. doi: 10.1038/npp.2009.93
37. Sim, H. R., Choi, T. Y., Lee, H. J., Kang, E. Y., Yoon, S., Han, P. L., et al. (2013). Role of dopamine D2 receptors in plasticity of stress-induced addictive behaviours. Nat. Commun. 4:1579. doi: 10.1038/ncomms2598
38. Smith, R. J., Lobo, M. K., Spencer, S., and Kalivas, P. W. (2013). Cocaine-induced adaptations in D1 and D2 accumbens projection neurons (a dichotomy not necessarily synonymous with direct and indirect pathways). Curr. Opin. Neurobiol. 23, 546-552. doi: 10.1016/j.conb.2013.01.026
39. Steketee, J. D., and Kalivas, P. W. (2011). Drug wanting: behavioral sensitization and relapse to drug-seeking behavior. Pharmacol. Rev. 63, 348-365. doi: 10.1124/pr.109.001933
40. Taverna, S., Ilijic, E., and Surmeier, D. J. (2008). Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease. J. Neurosci. 28, 5504-5512. doi: 10.1523/JNEUROSCI.5493-07.2008
41. Taverna, S., van Dongen, Y. C., Groenewegen, H. J., and Pennartz, C. M. (2004). Direct physiological evidence for synaptic connectivity between medium-sized spiny neurons in rat nucleus accumbens in situ. J. Neurophysiol. 91, 1111-1121. doi: 10.1152/jn.00892.2003
42. Thomas, M. J., Kalivas, P. W., and Shaham, Y. (2008). Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br. J. Pharmacol. 154, 327-342. doi: 10.1038/bjp.2008.77
43. Tunstall, M. J., Oorschot, D. E., Kean, A., and Wickens, J. R. (2002). Inhibitory interactions between spiny projection neurons in the rat striatum. J. Neurophysiol. 88, 1263-1269. doi: 10.1152/jn.00886.2001
44. Vanderschuren, L. J., and Kalivas, P. W. (2000). Alterations to dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berl) 151, 99-120. doi: 10.1007/s002130000493
45. Wilson, C. J., and Groves, P. M. (1980). Fine structure and synaptic connection of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase. J. Comp. Neurol. 194, 599-615. doi: 10.1002/cne.901940308
46. Wise, R. A. (2004). Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494. doi: 10.1038/nrn1406