Increased conditioned place preference for cocaine in high anxiety related behavior (HAB) mice is associated with an increased activation in the accumbens corridor

Frontiers in Behavioral Neuroscience

Volumn 8, Issue DEC, 2014, Pages

  Prast, Janine M ^a   Schardl, Aurelia ^a   Sartori, Simone B ^a   Singewald, Nicolas ^a   Saria, Alois ^a   Zernig, Gerald ^a,b  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Accumbens corridor; Anxiety; c Fos; Cocaine CPP; D1 MSNs; D2 MSNs; Egr1

Indexed keywords

COCAINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; EARLY GROWTH RESPONSE FACTOR 1; PROTEIN C FOS; SODIUM CHLORIDE;

ACCUMBENS CORRIDOR; ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BEHAVIOR ASSESSMENT; CD-1 MOUSE; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; GENE EXPRESSION; GENETIC ASSOCIATION; GLIA CELL; HIGH ANXIETY RELATED BEHAVIOR; IMMEDIATE EARLY GENE; MEDIUM SPINY NEURON; MOUSE; NERVE CELL; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY NERVOUS SYSTEM; PLACE PREFERENCE; QUANTITATIVE ANALYSIS; SEPTUM PELLUCIDUM; TRANQUILIZING ACTIVITY;

EID: 84919881063     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00441     Document Type: Article

References (63)

1. Ahmadi, H., Nasehi, M., Rostami, P., and Zarrindast, M. R. (2013). Involvement of the nucleus accumbens shell dopaminergic system in prelimbic NMDA-induced anxiolytic-like behaviors. Neuropharmacology 71, 112–123. doi: 10.1016/j.neuropharm.2013.03.017
2. Bardo, M. T., Rowlett, J. K., and Harris, M. J. (1995). Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci. Biobehav. Rev. 19, 39–51. doi: 10.1016/0149-7634(94)00021-R
3. Beckmann, A. M., and Wilce, P. A. (1997). Egr transcription factors in the nervous system. Neurochem. Int. 31, 477–510. doi: 10.1016/S0197-0186(96)00136-2
4. Bewernick, B. H., Hurlemann, R., Matusch, A., Kayser, S., Grubert, C., Hadrysiewicz, B., et al. (2010). Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol. Psychiatry 67, 110–116. doi: 10.1016/j.biopsych.2009.09.013
5. Breiter, H. C., Gollub, R. L., Weisskoff, R. M., Kennedy, D. N., Berke, J. D., Goodman, J. M., et al. (1997). Acute effects of cocaine on human brain activity and emotion. Neuron 19, 591–611. doi: 10.1016/S0896-6273(00)80374-8
6. Breiter, H. C., and Rosen, B. R. (1999). Functional magnetic resonance imaging of brain reward circuitry in the human. Ann. N.Y. Acad. Sci. 877, 523–547. doi: 10.1111/j.1749-6632.1999.tb09287.x
7. Chambers, J. A., Power, K. G., and Durham, R. C. (2004). The relationship between trait vulnerability and anxiety and depressive diagnoses at long-term follow-up of generalized anxiety disorder. Anxiety Disord. 18, 587–607. doi: 10.1016/j.janxdis.2003.09.001
8. Chaudhuri, A. (1997). Neural activity mapping with inducible transcription factors. Neuronreport 8, 3–8. doi: 10.1097/00001756-199709080-00002
9. Chaudhuri, A., Zangenehpour, S., Rahbar-Dehgan, F., and Ye, F. (2000). Molecular maps of neural activity and quiescence. Acta Neurobiol. 60, 403–410.
10. Cole, A. J., Saffen, D., Baraban, J. M., and Worley, P. F. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474–476. doi: 10.1038/340474a0
11. Costall, B., Kelly, M., Naylor, R., and Onaivi, E. (1989). The actions of nicotine and cocaine in a mouse model of anxiety. Pharmacol. Biochem. Behav. 33, 197–203. doi: 10.1016/0091-3057(89)90450-4
12. Degroot, A., and Treit, D. (2003). Septal gabaergic and hippocampal cholinergic systems interact in the modulation of anxiety. Neuroscience 117, 493–501. doi: 10.1016/S0306-4522(02)00651-6
13. El Rawas, R., Klement, S., Salti, A., Fritz, M., Dechant, G., and Saria, A. (2012). Preventive role of social interaction for cocaine conditioned place preference: correlation with FosB/DeltaFosB and pCREB expression in rat mesocorticolim-bic areas. Front. Behav. Neurosci. 6:8. doi: 10.3389/fnbeh.2012.00008
14. Estelles, J., Lluch, J., Rodriguez-Arias, M., Aguilar, M. A., and Minarro, J. (2007). Cocaine exposure during adolescence affects anxiety in adult mice. Brain Res. Bull. 71, 393–403. doi: 10.1016/j.brainresbull.2006.10.008
15. Franklin, K. B. J., and Paxinos, G. (2007). The Mouse Brain in Stereotaxic Coordinates, 3rd Edn. New York; London; Burlington; California: Academic Press.
16. Fritz, M., El Rawas, R., Salti, A., Klement, S., Bardo, M. T., Kemmler, G., et al. (2011). Reversal of cocaine-conditioned place preference and mesocorticolimbic Zif268 expression by social interaction in rats. Addict. Biol. 16, 273–284. doi: 10.1111/j.1369-1600.2010.00285.x
17. Golden, S. A., Christoffel, D. J., Heshmati, M., Hodes, G. E., Magida, J., Davis, K., et al. (2013). Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nat. Med. 19, 337–344. doi: 10.1038/nm.3090
18. Grant, B. F., Stinson, F. S., Dawson, D. A., Chou, S. P., Dufour, M. C., Compton, W., et al. (2004). Prevalence and co-occurrence of substance use disorders and independent mood and anxiety disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Arch Gen. Psychiatry 61, 807–816. doi: 10.1001/archpsyc.61.8.807
19. Haber, S. N., and Rauch, S. L. (2010). Neurocircuitry: a window into the networks underlying neuropsychiatric disease. Neuropsychopharmacology 35, 1–3. doi: 10.1038/npp.2009.146
20. Heimer, L., Alheid, G. F., De Olmos, J. S., Groenewegen, H. J., Haber, S. N., Harlan, R. E., et al. (1997). The accumbens: beyond the core-shell dichotomy. J. Neurospsychiatry Neurosci. 9, 354–381.
21. Herdegen, T., and Leah, J. D. (1998). Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Rev. 28, 370–490. doi: 10.1016/S0165-0173(98)00018-6
22. Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., and Lüthi, A. (2010). Neuronal circuits of fear extinction. Eur. J. Neurosci. 31, 599–612. doi: 10.1111/j.1460-9568.2010.07101.x
23. Hope, B. T., Kosofsky, B. E., Hyman, S. E., and Nestler, E. J. (1992). Regulation of immediate early gene expression and AP-1 binding in the rat nucleus accumbens by chronic cocaine. Neurobiology 89, 5764–5768.
24. Ishida, Y., Hashiguchi, H., Ishizuka, Y., Kuwahara, I., Mitsuyama, Y., and Nishimori, T. (2000). Basal expression of c-fos and ZIF268 in the rat basal ganglia immunohistochemical characterization of striatal ZIF268-positive neurons. Eur. J. Neurosci. 12, 771–775. doi: 10.1046/j.1460-9568.2000.00968.x
25. Joseph, B., and Venero, J. L. (2013). Microglia. New York, NY: Springer Science+Business Media.
26. Khantzian, E. (1985). The self-medication hypothesis of addictive disorders: focus on heroin and cocaine dependence. Am. J. Psychiatry 142, 1259–1264.
27. Ko, S. W., Hu-Shan, A., Gallitaneo-Mendel, A., Chang-Shen, Q., Feng, W., Milbrandt, J., et al. (2005). Transcription factor Egr-1 is required for long-term fear memory and anxiety. Acta Physiol. Sin. 57, 421–432.
28. Krömer, S. A., Kessler, M. S., Milfay, D., Birg, I. N., Bunck, M., Czibere, L., et al. (2005). Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety. J. Neurosci. 25, 4375–4384. doi: 10.1523/JNEUROSCI.0115-05.2005
29. Kummer, K., Hofhansel, L., Barwitz, C. M., Schardl, A., Prast, J. M., Salti, A., et al. (2014). Differences in social interaction- vs. cocaine reward in mouse vs. rat. Front. Behav. Neurosci. 8:363. doi: 10.3389/fnbeh.2014.00363
30. Kummer, K., Klement, S., Eggart, V., Mayr, M. J., Saria, A., and Zernig, G. (2011). Conditioned place preference for social interaction in rats: contribution of sensory components. Front. Behav. Neurosci. 5:80. doi: 10.3389/fnbeh.2011.00080
31. Landgraf, R., Kessler, M. S., Bunck, M., Murgatroyd, C., Spengler, D., Zimbelmann, M., et al. (2007). Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glyoxalase-I. Neurosci. Biobehav. Re v. 31, 89–102. doi: 10.1016/j.neubiorev.2006.07.003
32. Lee, J. L. C., Di Ciano, P., Thomas, K. L., and Everitt, B. J. (2005). Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47, 795–801. doi: 10.1016/j.neuron.2005.08.007
33. Lembke, A. (2012). Time to abandon the self-medication hypothesis in patients with psychiatric disorders. Am. J. Drug Alcohol Abuse 38, 524–529. doi: 10.3109/00952990.2012.694532
34. Levin, J. R., Serlin, R. C., and Seaman, M. A. (1994). A controlled, powerful multiple-comparison strategy for several situations. Psychol. Bull. 115, 153–159. doi: 10.1037/0033-2909.115.1.153
35. Levita, L., Hoskin, R., and Champi, S. (2012). Avoidance of harm and anxiety: a role for the nucleus accumbens. Neuroimage 62, 189–198. doi: 10.1016/j.neuroimage.2012.04.059
36. Lüthi, A., and Lüscher, C. (2014). Pathological circuit function underlying addiction and anxiety disorders. Nat. Neurosci. 17, 1635–1643. doi: 10.1038/nn.3849
37. Mahler, S.V., and Aston-Jones, G.S. (2012). Fos activation of selective afferents to ventral tegmental area during cue-induced reinstatement of cocaine seeking in rats. J. Neurosci. 32, 13309–13325. doi: 10.1038/nn.3849
38. Mariani, J., Khantzian, E., and Levin, F. (2014). The self-medication hypothesis and psychostimulant treatment of cocaine dependence: an update. Am. J. Addict. 23, 189–193. doi: 10.1111/j.1521-0391.2013
39. Menard, J., and Dallas, T. (1996). Lateral and medial septal lesions reduce anxiety in the plus-maze and probe-burying tests. Physiol. Behav. 60, 845–853.
40. Muigg, P., Scheiber, S., Salchner, P., Bunck, M., Landgraf, R., and Singewald, N. (2009). Differential stress-induced neuronal activation patterns in mouse lines selectively bred for high, normal or low anxiety. PLoS ONE 4:e5346. doi: 10.1371/journal.pone.0005346
41. Mullen, R. J., Buck, C. R., and Smith, A. M. (1991). NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201–211.
42. Najm, F. J., Lager, A. M., Zaremba, A., Wyatt, K., Caprariello, A. V., Factor, D. C., et al. (2013). Transcription factor–mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat. Biotechnol. 31, 426–433. doi: 10.1038/nbt.2561
43. Nguyen, T. V., Kosofsky, B. E., Birnbaum, R., Cohen, B. M., and Hyman, S. E. (1992). Differential expression of c-Fos and Zif268 in rat striatum after haloperidol, clozapine, and amphetamine. Neuobiology 89, 4270–4274.
44. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. New York, NY: Academic Press.
45. Pelloux, Y., Costentin, J., and Duterte-Boucher, D. (2009). Anxiety increases the place conditioning induced by cocaine in rats. Behav. Brain Res. 197, 311–316. doi: 10.1016/j.bbr.2008.08.029
46. Perez-Cadahia, B., Drobic, B., and Davie, J. R. (2011). Activation and function of immediate-early genes in the nervous system. Biochem. Cell Biol. 89, 61–73. doi: 10.1139/O10-138
47. Prast, J. M., Kummer, K. K., Barwitz, C. M., Humpel, C., Dechant, G., and Zernig, G. (2012). Acetylcholine, drug reward and substance use disorder treatment: intra- and interindividual striatal and accumbal neuron ensemble heterogeneity may explain apparent discrepant findings. Pharmacology 90, 264–273. doi: 10.1159/000342636
48. Prast, J. M., Schardl, A., Schwarzer, C., Dechant, G., Saria, A., and Zernig, G. (2014). Reacquisition of cocaine conditioned place preference and its inhibition by previous social interaction preferentially affect D1-medium spiny neurons in the accumbens corridor. Front. Behav. Neurosci. 8:317. doi: 10.3389/fnbeh.2014.00317
49. Rapee, R. M. (1991). Generalized anxiety disorder: a review of clinical features and theoretical concepts. Clin. Psychol. Rev. 11, 419–440. doi: 10.1016/0272-7358(91)90116-C
50. Razavi, S., Haeri-Rohani, A., Eidi, A., and Zarrindast, M. R. (2014). Involvement of D1/D2 dopamine antagonists upon open-arms exploratory behaviours induced by intra-nucleus accumbens shell administration of N-methyl-D-aspartate. Folia Neuropathol. 52, 164–178. doi: 10.5114/fn.2014.43788
51. Salamone, J. D., and Correa, M. (2012). The mysterious motivational functions of mesolimbic dopamine. Neuron 76, 470–485. doi: 10.1016/j.neuron.2012.10.021
52. Sartori, S. B., Hauschild, M., Bunck, M., Gaburro, S., Landgraf, R., and Singewald, N. (2011a). Enhanced Fear Expression in a PsychopathologicalMouse Model of Trait Anxiety: pharmacological Interventions. PLoS ONE 6:e16849. doi: 10.1371/journal.pone.0016849
53. Sartori, S. B., Landgraf, R., and Singewald, N. (2011b). The clinical implications of mouse models of enhanced anxiety. Future Neurol. 6, 531–571. doi: 10.2217/fnl.11.34
54. Sassone-Corsi, P., Sisson, J. C., and Verma, I. M. (1988). Transcriptional autoregu-lation of the proto-oncogene fos. Nature 334, 314–319. doi: 10.1038/334314a0
55. Schmuckermair, C., Gaburro, S., Sah, A., Landgraf, R., Sartori, S. B., and Singewald, N. (2013). Behavioral and neurobiological effects of deep brain stimulation in a mouse model of high anxiety- and depression-like behavior. Neuropsychopharmacology 38, 1234–1244. doi: 10.1038/npp.2013.21
56. Singewald, N. (2007). Altered brain activity processing in high-anxiety rodents revealed by challenge paradigms and functional mapping. Neurosci. Biobehav. Rev. 31, 18–40. doi: 10.1016/j.neubiorev.2006.02.003
57. Slattery, D. A., Morrow, J. A., Hudson, A. L., Hill, D. R., Nutt, D. J., and Henry, B. (2005). Comparison of alterations in c-fos and Egr-1 (zif268) expression throughout the rat brain following acute administration of different classes of antidepressant compounds. Neuropsychopharmacology 30, 1278–1287. doi: 10.1038/sj.npp.1300717
58. Sturm, V., Lenartz, D., Koulousakis, A., Treuer, H., Herholz, K., Klein, J. C., et al. (2003). The nucleus accumbens: a target for deep brain stimulation in obsessive–compulsive- and anxiety-disorders. J. Chem. Neuroanat. 26, 293–299. doi: 10.1016/j.jchemneu.2003.09.003
59. Valjent, E., Aubier, B., Corbillé, A. G., Brami-Cherrier, K., Caboche, J., Topilko, P., et al. (2006). Plasticity-associated gene Krox24/Zif268 is required for long-lasting behavioral effects of cocaine. J. Neurosci. 26, 4956–4960. doi: 10.1523/jneurosci.4601-05.2006
60. Wang, Y.-F., Sun, M.-Y., Hou, Q., and Hamilton, K. A. (2013). GABAergic inhibition through synergistic astrocytic neuronal interaction transiently decreases vasopressin neuronal activity during hypoosmotic challenge. Eur. J. Neurosci. 37, 1260–1269. doi: 10.1111/ejn.12137
61. Zangenehpour, S., and Chaudhuri, A. (2002). Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps. Mol. Brain Res. 109, 221–225. doi: 10.1016/S0169-328X(02)00556-9
62. Zernig, G., Ahmed, S. H., Cardinal, R. N., Morgan, D., Acquas, E., Foltin, R. W., et al. (2007). Explaining the escalation of drug use in substance dependence: models and appropriate animal laboratory tests. Pharmacology 80, 65–119. doi: 10.1159/000103923
63. Zhai, H., Li, Y., Wang, X., and Lu, L. (2008). Drug-induced alterations in the extracellular signal-regulated kinase (erk) signalling pathway: implications for reinforcement and reinstatement. Cell. Mol. Neurobiol. 28, 157–172. doi: 10.1007/s10571-007-9240-3