Intravenous cocaine self-administration in a panel of inbred mouse strains differing in acute locomotor sensitivity to cocaine

  • Amanda J. Roberts
  • Linzy Casal
  • Salvador Huitron-Resendiz
  • Trey Thompson
  • Lisa M. Tarantino
Original Investigation
  • 31 Downloads

Abstract

Rationale

Initial sensitivity to drugs of abuse often predicts subsequent use and abuse, but this relationship is not always observed in human studies. Moreover, studies examining the relationship between initial locomotor sensitivity and the rewarding and reinforcing effects of drugs in animal models have also been equivocal. Understanding the relationship between initial drug effects and propensity to continue use, potentially resulting in the development of a substance use disorder, may help to identify key targets for prevention and treatment.

Objectives

We examined intravenous cocaine self-administration in a set of mouse strains that were previously identified to be at the phenotypic extremes for cocaine-induced locomotor activation to determine if initial locomotor sensitivity predicted acquisition, extinction, dose response, or progressive ratio (PR) breakpoint.

Methods

We selected eight inbred mouse strains based on locomotor sensitivity to 20 mg/kg cocaine. These strains, designated as low and high responders, were tested in an intravenous self-administration paradigm that included acquisition of 0.5 mg/(kg*inf) under a FR1 schedule, extinction, re-acquisition, dose response to 0.125, 0.25, 0.5, 1, and 2 mg/(kg*inf), and progressive ratio.

Results

We observed overall differences in self-administration behavior between high and low responders. Low responders self-administered less cocaine and had lower breakpoints under the PR schedule. However, we also observed strain differences within each group. Self-administration in the low responder, LG/J, more closely resembled the behavior of the high-responding group, and the high responder, P/J, had self-administration behavior that more closely resembled the low-responding group.

Conclusions

We conclude that acute cocaine-induced locomotor activation does predict self-administration behavior, but in a strain-specific manner. These data support the idea that genetic background influences the relationship among addiction-related behaviors.

Keywords

Cocaine Inbred mice Locomotor sensitivity Intravenous self-administration 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

213_2018_4834_Fig7_ESM.gif (11 kb)
Supplemental Figure 1

Cocaine-induced locomotor activation dose response for saline control, 30 and 40 mg/kg. Asterisks indicate significant difference from C57BL/6 J at the same dose. Error bars are SEM. (GIF 10 kb)

213_2018_4834_MOESM1_ESM.eps (122 kb)
High resolution image (EPS 122 kb)
213_2018_4834_Fig8_ESM.gif (16 kb)
Supplemental Figure 2

Number of inactive lever presses (A) and time out responding (B) during the last day of extinction (“D10”) and the final day of re-acquisition (“R”). Data points are individual animals and error bars are SEM. (C) Number of infusions self-administered on the last day of acquisition and during reacquisition. Each data point is a strain mean. (GIF 15 kb)

213_2018_4834_MOESM2_ESM.eps (278 kb)
High resolution image (EPS 277 kb)

References

  1. Ahmari SE (2016) Using mice to model obsessive compulsive disorder: from genes to circuits. Neuroscience 321:121–137.  https://doi.org/10.1016/j.neuroscience.2015.11.009 CrossRefPubMedGoogle Scholar
  2. Campbell UC, Carroll ME (2000) Acquisition of drug self-administration: environmental and pharmacological interventions. Exp Clin Psychopharmacol 8(3):312–325.  https://doi.org/10.1037/1064-1297.8.3.312 CrossRefPubMedGoogle Scholar
  3. Carney JM, Landrum RW, Cheng MS, Seale TW (1991) Establishment of chronic intravenous drug self-administration in C57bl/6j mouse. Neuroreport 2(8):477–480.  https://doi.org/10.1097/00001756-199108000-00017 CrossRefPubMedGoogle Scholar
  4. (CASA), National Ctr on Addiction and Substance Abuse at Columbia University (2009) Shoveling up II: the impact of substance abuse on federal, state and local budgets. Columbia University, New YorkGoogle Scholar
  5. Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, Beatty J, . . . Complex Trait, Consortium (2004) The Collaborative Cross, a community resource for the genetic analysis of complex traits. Nat Genet, 36(11):1133–1137.  https://doi.org/10.1038/ng1104-1133
  6. Contet C, Whisler KN, Jarrell H, Kenny PJ, Markou A (2010) Patterns of responding differentiate intravenous nicotine self-administration from responding for a visual stimulus in C57BL/6J mice. Psychopharmacology 212(3):283–299.  https://doi.org/10.1007/s00213-010-1950-4 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Crabbe JC (2016) Progress with nonhuman animal models of addiction. J Stud Alcohol Drugs 77(5):696–699.  https://doi.org/10.15288/jsad.2016.77.696 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Davidson ES, Finch JF, Schenk S (1993) Variability in subjective responses to cocaine: initial experiences of college students. Addict Behav 18(4):445–453.  https://doi.org/10.1016/0306-4603(93)90062-E CrossRefPubMedGoogle Scholar
  9. de Wit H, Phillips TJ (2012) Do initial responses to drugs predict future use or abuse? Neurosci Biobehav Rev 36(6):1565–1576.  https://doi.org/10.1016/j.neubiorev.2012.04.005 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Deminiere JM, Piazza PV, Le Moal M, Simon H (1989) Experimental approach to individual vulnerability to psychostimulant addiction. Neurosci Biobehav Rev 13(2–3):141–147.  https://doi.org/10.1016/S0149-7634(89)80023-5 CrossRefPubMedGoogle Scholar
  11. Deroche V, Caine SB, Heyser CJ, Polis I, Koob GF, Gold LH (1997) Differences in the liability to self-administer intravenous cocaine between C57BL/6xSJL and BALB/cByJ mice. Pharmacol Biochem Behav 57(3):429–440.  https://doi.org/10.1016/S0091-3057(96)00439-X CrossRefPubMedGoogle Scholar
  12. Dickson PE, Ndukum J, Wilcox T, Clark J, Roy B, Zhang L, . . . Chesler EJ (2015) Association of novelty-related behaviors and intravenous cocaine self-administration in Diversity Outbred mice. Psychopharmacology, 232(6):1011–1024.  https://doi.org/10.1007/s00213-014-3737-5
  13. Falcone M, Lee B, Lerman C, Blendy JA (2016) Translational research on nicotine dependence. Curr Top Behav Neurosci 28:121–150.  https://doi.org/10.1007/7854_2015_5005 CrossRefPubMedGoogle Scholar
  14. Grahame NJ, Cunningham CL (1995) Genetic differences in intravenous cocaine self-administration between C57BL/6J and DBA/2J mice. Psychopharmacology 122(3):281–291.  https://doi.org/10.1007/BF02246549 CrossRefPubMedGoogle Scholar
  15. Grahame NJ, Phillips TJ, Burkhart-Kasch S, Cunningham CL (1995) Intravenous cocaine self-administration in the C57BL/6J mouse. Pharmacol Biochem Behav 51(4):827–834.  https://doi.org/10.1016/0091-3057(95)00047-Z CrossRefPubMedGoogle Scholar
  16. Griffin WC 3rd, Middaugh LD (2003) Acquisition of lever pressing for cocaine in C57BL/6J mice: effects of prior Pavlovian conditioning. Pharmacol Biochem Behav 76(3–4):543–549.  https://doi.org/10.1016/j.pbb.2003.09.010 CrossRefPubMedGoogle Scholar
  17. Gutierrez-Cuesta J, Burokas A, Mancino S, Kummer S, Martin-Garcia E, Maldonado R (2014) Effects of genetic deletion of endogenous opioid system components on the reinstatement of cocaine-seeking behavior in mice. Neuropsychopharmacology 39(13):2974–2988.  https://doi.org/10.1038/npp.2014.149 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Haertzen CA, Kocher TR, Miyasato K (1983) Reinforcements from the first drug experience can predict later drug habits and/or addiction: results with coffee, cigarettes, alcohol, barbiturates, minor and major tranquilizers, stimulants, marijuana, hallucinogens, heroin, opiates and cocaine. Drug Alcohol Depend 11(2):147–165.  https://doi.org/10.1016/0376-8716(83)90076-5 CrossRefPubMedGoogle Scholar
  19. Katz JL, Higgins ST (2003) The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology 168(1–2):21–30.  https://doi.org/10.1007/s00213-003-1441-y CrossRefPubMedGoogle Scholar
  20. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35(1):217–238.  https://doi.org/10.1038/npp.2009.110 CrossRefPubMedGoogle Scholar
  21. Kumar V, Kim K, Joseph C, Kourrich S, Yoo SH, Huang HC, Vitaterna MH, Pardo-Manuel de Villena F, Churchill G, Bonci A, Takahashi JS (2013) C57BL/6N mutation in cytoplasmic FMRP interacting protein 2 regulates cocaine response. Science 342(6165):1508–1512.  https://doi.org/10.1126/science.1245503 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kuzmin A, Johansson B (2000) Reinforcing and neurochemical effects of cocaine: differences among C57, DBA, and 129 mice. Pharmacol Biochem Behav 65(3):399–406.  https://doi.org/10.1016/S0091-3057(99)00211-7 CrossRefPubMedGoogle Scholar
  23. Lambert NM, McLeod M, Schenk S (2006) Subjective responses to initial experience with cocaine: an exploration of the incentive-sensitization theory of drug abuse. Addiction 101(5):713–725.  https://doi.org/10.1111/j.1360-0443.2006.01408.x CrossRefPubMedGoogle Scholar
  24. Lynch WJ, Nicholson KL, Dance ME, Morgan RW, Foley PL (2010) Animal models of substance abuse and addiction: implications for science, animal welfare, and society. Comp Med 60(3):177–188PubMedPubMedCentralGoogle Scholar
  25. Mandt BH, Johnston NL, Zahniser NR, Allen RM (2012) Acquisition of cocaine self-administration in male Sprague-Dawley rats: effects of cocaine dose but not initial locomotor response to cocaine. Psychopharmacology 219(4):1089–1097.  https://doi.org/10.1007/s00213-011-2438-6 CrossRefPubMedGoogle Scholar
  26. Miller T, Hendrie D (2008) Substance abuse prevention dollars and cents: a cost-benefit analysis. ((SMA) 07-4298). RockvilleGoogle Scholar
  27. Nugent AL, Anderson EM, Larson EB, Self DW (2017) Incubation of cue-induced reinstatement of cocaine, but not sucrose, seeking in C57BL/6J mice. Pharmacol Biochem Behav 159:12–17.  https://doi.org/10.1016/j.pbb.2017.06.017 CrossRefPubMedGoogle Scholar
  28. Olsen CM, Winder DG (2009) Operant sensation seeking engages similar neural substrates to operant drug seeking in C57 mice. Neuropsychopharmacology 34(7):1685–1694.  https://doi.org/10.1038/npp.2008.226 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Paneda C, Huitron-Resendiz S, Frago LM, Chowen JA, Picetti R, de Lecea L, Roberts AJ (2009) Neuropeptide S reinstates cocaine-seeking behavior and increases locomotor activity through corticotropin-releasing factor receptor 1 in mice. J Neurosci 29(13):4155–4161.  https://doi.org/10.1523/JNEUROSCI.5256-08.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Parker CC, Chen H, Flagel SB, Geurts AM, Richards JB, Robinson TE . . ., Palmer AA (2014). Rats are the smart choice: rationale for a renewed focus on rats in behavioral genetics. Neuropharmacology 76 Pt B:250-258.  https://doi.org/10.1016/j.neuropharm.2013.05.047
  31. Preacher KJ, Rucker DD, MacCallum RC, Nicewander WA (2005) Use of the extreme groups approach: a critical reexamination and new recommendations. Psychol Methods 10(2):178–192.  https://doi.org/10.1037/1082-989X.10.2.178 CrossRefPubMedGoogle Scholar
  32. Roberts AJ, Polis IY, Gold LH (1997) Intravenous self-administration of heroin, cocaine, and the combination in Balb/c mice. European Journal of Pharmacology, 326(2-3), 119-125. Doi.  https://doi.org/10.1016/S0014-2999(97)85405-2
  33. Roberts DC, Morgan D, Liu Y (2007) How to make a rat addicted to cocaine. Prog Neuro-Psychopharmacol Biol Psychiatry 31(8):1614–1624.  https://doi.org/10.1016/j.pnpbp.2007.08.028 CrossRefGoogle Scholar
  34. Robison AJ, Nestler EJ (2011) Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12(11):623–637.  https://doi.org/10.1038/nrn3111 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Malenka RC, Nestler EJ (2010) The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 33(6):267–276.  https://doi.org/10.1016/j.tins.2010.02.002 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sharpe AL, Varela E, Bettinger L, Beckstead MJ (2014) Methamphetamine self-administration in mice decreases GIRK channel-mediated currents in midbrain dopamine neurons. Int J Neuropsychopharmacol 18(5):pyu073.  https://doi.org/10.1093/ijnp/pyu073 CrossRefPubMedGoogle Scholar
  37. Thanos PK, Subrize M, Lui W, Puca Z, Ananth M, Michaelides M, . . . Volkow ND (2011) D-cycloserine facilitates extinction of cocaine self-administration in C57 mice. Synapse 65(10):1099–1105.  https://doi.org/10.1002/syn.20944
  38. Thomsen M, Caine SB (2006) Cocaine self-administration under fixed and progressive ratio schedules of reinforcement: comparison of C57BL/6J, 129X1/SvJ, and 129S6/SvEvTac inbred mice. Psychopharmacology 184(2):145–154.  https://doi.org/10.1007/s00213-005-0207-0 CrossRefPubMedGoogle Scholar
  39. Thomsen M, Caine SB (2011a) False positive in the intravenous drug self-administration test in C57BL/6J mice. Behav Pharmacol 22(3):239–247.  https://doi.org/10.1097/FBP.0b013e328345f8f2 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Thomsen M, Caine SB (2011b) Psychomotor stimulant effects of cocaine in rats and 15 mouse strains. Exp Clin Psychopharmacol 19(5):321–341.  https://doi.org/10.1037/a0024798 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Thomsen M, Han DD, Gu HH, Caine SB (2009) Lack of cocaine self-administration in mice expressing a cocaine-insensitive dopamine transporter. J Pharmacol Exp Ther 331(1):204–211.  https://doi.org/10.1124/jpet.109.156265 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Vargas-Irwin C, van den Oord EJ, Beardsley PM, Robles JR (2006) A method for analyzing strain differences in acquisition of IV cocaine self-administration in mice. Behav Genet 36(4):525–535.  https://doi.org/10.1007/s10519-006-9068-5 CrossRefPubMedGoogle Scholar
  43. Volkow ND, Morales M (2015) The brain on drugs: from reward to addiction. Cell 162(4):712–725.  https://doi.org/10.1016/j.cell.2015.07.046 CrossRefPubMedGoogle Scholar
  44. Volkow ND, Koob G, Baler R (2015) Biomarkers in substance use disorders. ACS Chem Neurosci 6(4):522–525.  https://doi.org/10.1021/acschemneuro.5b00067 CrossRefPubMedGoogle Scholar
  45. Ward SJ, Rosenberg M, Dykstra LA, Walker EA (2009) The CB1 antagonist rimonabant (SR141716) blocks cue-induced reinstatement of cocaine seeking and other context and extinction phenomena predictive of relapse. Drug Alcohol Depend 105(3):248–255.  https://doi.org/10.1016/j.drugalcdep.2009.07.002 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wiltshire T, Ervin RB, Duan H, Bogue MA, Zamboni WC, Cook S, . . . Tarantino LM (2015) Initial locomotor sensitivity to cocaine varies widely among inbred mouse strains. Genes Brain Behav 14(3): 271–280.  https://doi.org/10.1111/gbb.12209
  47. Yamamoto DJ, Nelson AM, Mandt BH, Larson GA, Rorabaugh JM, Ng CM, . . . Zahniser NR (2013). Rats classified as low or high cocaine locomotor responders: a unique model involving striatal dopamine transporters that predicts cocaine addiction-like behaviors. Neurosci Biobehav Rev 37(8):1738–1753.  https://doi.org/10.1016/j.neubiorev.2013.07.002
  48. Yan Y, Nitta A, Mizoguchi H, Yamada K, Nabeshima T (2006) Relapse of methamphetamine-seeking behavior in C57BL/6J mice demonstrated by a reinstatement procedure involving intravenous self-administration. Behav Brain Res 168(1):137–143.  https://doi.org/10.1016/j.bbr.2005.11.030 CrossRefPubMedGoogle Scholar
  49. Yazdani N, Parker CC, Shen Y, Reed ER, Guido MA, Kole LA, . . . Bryant CD (2015) Hnrnph1 is a quantitative trait gene for methamphetamine sensitivity. PLoS Genet 11(12): e1005713.  https://doi.org/10.1371/journal.pgen.1005713

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Animal Models Core Facility, The Scripps Research InstituteLa JollaUSA
  2. 2.Neurosurgery and Behavior, Allen Institute for Brain ScienceSeattleUSA
  3. 3.Division of Pharmacotherapy and Experimental Therapeutics, Eshelman School of PharmacyUniversity of North CarolinaChapel HillUSA
  4. 4.Department of Genetics, School of MedicineUniversity of North CarolinaChapel HillUSA

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