Optogenetic inhibition of D1R containing nucleus accumbens neurons alters cocaine-mediated regulation of Tiam1

Frontiers in Molecular Neuroscience

Volumn , Issue MAY, 2013, Pages

  Chandra, Ramesh ^a   Lenz, Jeffrey ^a   Gancarz, Amy M ^b,c   Chaudhury, Dipesh ^d   Schroeder, Gabrielle L ^b   Han, Ming Hu ^d   Cheer, Joseph F ^a   Dietz, David M ^b,c   Kay Lobo, Mary ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c RESEARCH INSTITUTE ON ADDICTIONS   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cocaine; Medium spiny neurons; Nucleus accumbens; Optogenetics; Tiam1

Indexed keywords

ADENOVIRUS VECTOR; CHANNELRHODOPSIN 2; COCAINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; PROTEIN TIAM1; RHODOPSIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

ADDICTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; LOCOMOTION; MEDIUM SPINY NEURON; MESENCEPHALON; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; PHOTOSTIMULATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; RAT; RNA ISOLATION; SENSITIZATION;

EID: 84877286369     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00013     Document Type: Article

References (44)

1. Bertran-Gonzalez, J., Bosch, C., Maroteaux, M., Matamales, M., Herve, D., Valjent, E., and Girault, J.A. (2008). Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J. Neurosci. 28, 5671-5685.
2. Cingolani, L.A., and Goda, Y. (2008). Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9, 344-356.
3. Dietz, D.M., Dietz, K.C., Nestler, E.J., and Russo, S.J. (2009). Molecular mechanisms of psychostimulant-induced structural plasticity. Pharmacopsychiatry 42, 69-78.
4. Dietz, D.M., Sun, H., Lobo, M.K., Cahill, M.E., Chadwick, B., Gao, V., Koo, J.W., Mazei-Robison, M.S., Dias, C., Maze, I., Damez-Werno, D., Dietz, K.C., Scobie, K.N., Ferguson, D., Christoffel, D., Ohnishi, Y., Hodes, G.E., Zheng, Y., Neve, R.L., Hahn, K.M., Russo, S.J., and Nestler, E.J. (2012). Rac1 is essential in cocaine-induced structural plasticity of nucleus accumbens neurons. Nat. Neurosci. 15, 891-896.
5. Ferguson, S.M., Eskenazi, D., Ishikawa, M., Wanat, M.J., Phillips, P.E., Dong, Y., Roth, B.L., and Neumaier, J.F. (2006). Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat. Neurosci. 14, 22-24.
6. Ferguson, S.M., Eskenazi, D., Ishikawa, M., Wanat, M.J., Phillips, P.E., Dong, Y., Roth, B.L., and Neumaier, J.F. (2011). Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat. Neurosci. 14, 22-24.
7. Gancarz, A.M., Kausch, M.A., Lloyd, D.R., and Richards, J.B. (2012). Between-session progressive ratio performance in rats responding for cocaine and water reinforcers. Psychopharmacology 222, 215-223.
8. Gradinaru, V., Zhang, F., Ramakrishnan, C., Mattis, J., Prakash, R., Diester, I., Goshen, I., Thompson, K.R., and Deisseroth, K. (2010). Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165.
9. 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. USA (In Press).
10. Guez-Barber, D., Fanous, S., Golden, S.A., Schrama, R., Koya, E., Stern, A.L., Bossert, J.M., Harvey, B.K., Picciotto, M.R., and Hope, B.T. (2011). FACS identifies unique cocaine-induced gene regulation in selectively activated adult striatal neurons. J. Neurosci. 31, 4251-4259
11. Halpain, S. (2000). Actin and the agile spine: how and why do dendritic spines dance? Trends Neurosci. 23, 141-146.
12. Heiman, M., Schaefer, A., Gong, S., Peterson, J.D., Day, M., Ramsey, K.E., Suarez-Farinas, M., Schwarz, C., Stephan, D.A., Surmeier, D.J., Greengard, P., Heintz, N. (2008). A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748
13. 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.
14. Ikemoto, S. (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27-78
15. Kalivas, P.W. (2009). The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci. 10, 561-572.
16. Kelz, M.B., Chen, J., Carlezon, W.A., Jr., Whisler, K., Gilden, L., Beckmann, A.M., Steffen, C, Zhang, Y.J., Marotti, L., Self, D.W., Tkatch, T., Baranauskas, G., Surmeier, D.J., Neve, R.L., Duman, R.S., Picciotto, M.R., and Nestler, E.J. (1999). Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401, 272-276.
17. Kim, J., Park, B.H., Lee, J.H., Park, S.K., and Kim, J.H. (2011). Cell type-specific alterations in the nucleus accumbens by repeated exposures to cocaine. Biol. Psychiatry 69, 1026-1034.
18. Koya, E., Golden, S.A., Harvey, B.K., Guez-Barber, D.H., Berkow, A., Simmons, D.E., Bossert, J.M., Nair, S.G., Uejima, J.L., Marin, M.T., Mitchell, T.B., Farquhar, D., Ghosh, S.C., Mattson, B.J., and Hope, B.T. (2009). Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nat. Neurosci. 12, 1069-1073
19. Kravitz, A.V., Freeze, B.S., Parker, P.R., Kay, K., Thwin, M.T., Deisseroth, K., and Kreitzer, A.C. (2010). Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622-626.
20. Kravitz, A.V., Owen, S.F., and Kreitzer, A.C. (2012). Optogenetic identification of striatal projection neuron subtypes during in-vivo recordings. Brain Res. (In Press)
21. Lee, K.W., Kim, Y., Kim, A.M., Helmin, K., Nairn, A.C, and Greengard, P. (2006). Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc. Natl. Acad. Sci. USA 103, 3399-3404.
22. Li, Y., Acerbo, M.J., and Robinson, T.E. (2004). The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur. J. Neurosci. 20, 1647-1654.
23. Lobo, M.K., Karsten, S.L., Gray, M., Geschwind, D.H., and Yang, X.W. (2006). FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat. Neurosci. 9, 443-452
24. Lobo, M.K., Covington, H.E., 3rd, Chaudhury, D., Friedman, A.K., Sun, H., Damez-Werno, D., Dietz, D.M., Zaman, S., Koo, J.W., Kennedy, P.J., Mouzon, E., Mogri, M., Neve, R.L., Deisseroth, K., Han, M.H., and Nestler, E.J. (2010). Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390.
25. 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, 1-11.
26. Maze, I., Covington, H.E., 3rd, Dietz, D.M., Laplant, Q., Renthal, W., Russo, S.J., Mechanic, M., Mouzon, E., Neve, R.L., Haggarty, S.J., Ren, Y., Sampath, S.C., Hurd, Y.L., Greengard, P., Tarakhovsky, A., Schaefer, A., and Nestler, E.J. (2010). Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327, 213-216.
27. Moratalla, R., Robertson, H.A., and Graybiel, A.M. (1992). Dynamic regulation of NGFI-A (zif268, egr1) gene expression in the striatum. J. Neurosci. 12, 2609-2622.
28. Nimchinsky, E.A., Sabatini, B.L., and Svoboda, K. (2002). Structure and function of dendritic spines. Annu. Rev. Physiol. 64, 313-353.
29. Pascoli V., Turiault M., and Lüscher C. (2011). Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 2011, 48 71-75.
30. Pulipparacharuvil, S., Renthal, W., Hale, C.F., Taniguchi, M., Xiao, G., Kumar, A., Russo, S.J., Sikder, D., Dewey, C.M., Davis, M.M., Greengard, P., Nairn, A.C., Nestler, E.J., and Cowan, C.W. (2008). Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59, 621-633.
31. Renthal, W., Kumar, A., Xiao, G., Wilkinson, M., Covington, H.E., 3rd, Maze, I., Sikder, D., Robison, A.J., LaPlant, Q., Dietz, D.M., Russo, S.J., Vialou, V., Chakravarty, S., Kodadek, T.J., Stack, A., Kabbaj, M., and Nestler, E.J. (2009). Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62, 335-348
32. Robinson, T.E., and Kolb, B. (2004). Structural plasticity associated with exposure to drugs of abuse. Neuropharmaco. 47 Suppl 1, 33-46.
33. Robison, A.J., and Nestler, E.J. (2011). Transcriptional and epigenetic mechanisms of addiction. Nat. Rev. Neurosci. 12, 623-637.
34. Russo, S.J., Dietz, D.M., Dumitriu, D., Morrison, J.H., Malenka, R.C., and Nestler, E.J. (2010). The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33, 267-276.
35. Schubert, V., and Dotti, C.G. (2007). Transmitting on actin: synaptic control of dendritic architecture. J. Cell Sci. 120, 205-212.
36. Sparta, D.R., Stamatakis, A.M., Phillips, J.L., Hovelso, N., Van Zessen, R., and Stuber, G.D. (2011). Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat. Protoc. 7, 12-23.
37. Stefanik, M.T., Moussawi, K., Kupchik, Y.M., Smith, K.C., Miller, R.L., Huff, M.L., Deisseroth, K., Kalivas, P.W., and LaLumiere, R.T. (2013). Optogenetic inhibition of cocaine seeking in rats. Addict. Biol. 18, 50-53
38. Stuber, G.D., Sparta, D.R., Stamatakis, A.M., van Leeuwen, W.A., Hardjoprajitno, J.E., Cho, S., Tye, K.M., Kempadoo, K.A., Zhang, F., Deisseroth, K., and Bonci, A. (2011). Excitatory transmission from the amygdala to nucleus Accumbens facilitates reward seeking. Nature. 475, 377-380.
39. Tai, L.H., Lee, A.M., Benavidez, N., Bonci, A., and Wilbrecht, L. (2012). Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value. Nat. Neurosci. 15, 1281-1289
40. Toda, S., Shen, H.W., Peters, J., Cagle, S., and Kalivas, P.W. (2006). Cocaine increases actin cycling: effects in the reinstatement model of drug seeking. J. Neurosci. 26, 1579-1587.
41. Tolias, K.F., Bikoff, J.B., Kane, C.G., Tolias, C.S., Hu, L., and Greenberg, M.E. (2007). The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc. Natl. Acad. Sci. USA 104, 7265-7270.
42. Tye, K.M., Prakash, R., Kim, S.Y., Fenno, L.E., Grosenick, L., Zarabi, H., Thompson, K.R., Gradinaru, V., Ramakrishnan, C., and Deisseroth, K. (2011). Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471, 358-362.
43. Witten, I.B., Lin, S.C., Brodsky, M., Prakash, R., Diester, I., Anikeeva, P., Gradinaru, V., Ramakrishnan, C., and Deisseroth, K. (2010). Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330, 1677-1681.
44. Witten, I., Steinberg, E., Lee, S., Davidson, T., Zalocusky, K., Brodsky, M., Yizhar, O., Cho, S., Gong, S., Ramakrishnan, C., Stuber, G., Tye, K., Janak, P., and Deisseroth, K. (2011). Recombinase-Driver Rat Lines: Tools, Techniques, and Optogenetic Application to Dopamine-Mediated Reinforcement. Neuron 72, 721-733