Skip to main content
SpringerLink
Log in

Characterization of genetically complex Collaborative Cross mouse strains that model divergent locomotor activating and reinforcing properties of cocaine

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

Few effective treatments exist for cocaine use disorders due to gaps in knowledge about its complex etiology. Genetically defined animal models provide a useful tool for advancing our understanding of the biological and genetic underpinnings of addiction-related behavior and evaluating potential treatments. However, many attempts at developing mouse models of behavioral disorders were based on overly simplified single gene perturbations, often leading to inconsistent and misleading results in pre-clinical pharmacology studies. A genetically complex mouse model may better reflect disease-related behaviors.

Objectives

Screening defined, yet genetically complex, intercrosses of the Collaborative Cross (CC) mice revealed two lines, RIX04/17 and RIX41/51, with extreme high and low behavioral responses to cocaine. We characterized these lines as well as their CC parents, CC004/TauUnc and CC041/TauUnc, to evaluate their utility as novel model systems for studying the biological and genetic mechanisms underlying behavioral responses to cocaine.

Methods

Behavioral responses to acute (initial locomotor sensitivity) and repeated (behavioral sensitization, conditioned place preference, intravenous self-administration) exposures to cocaine were assessed. We also examined the monoaminergic system (striatal tissue content and in vivo fast scan cyclic voltammetry), HPA axis reactivity, and circadian rhythms as potential mechanisms for the divergent phenotypic behaviors observed in the two strains, as these systems have a previously known role in mediating addiction-related behaviors.

Results

RIX04/17 and 41/51 show strikingly divergent initial locomotor sensitivity to cocaine with RIX04/17 exhibiting very high and RIX41/51 almost no response. The lines also differ in the emergence of behavioral sensitization with RIX41/51 requiring more exposures to exhibit a sensitized response. Both lines show conditioned place preference for cocaine. We determined that the cocaine sensitivity phenotype in each RIX line was largely driven by the genetic influence of one CC parental strain, CC004/TauUnc and CC041/TauUnc. CC004 demonstrates active operant cocaine self-administration and CC041 is unable to acquire under the same testing conditions, a deficit which is specific to cocaine as both strains show operant response for a natural food reward. Examination of potential mechanisms driving differential responses to cocaine show strain differences in molecular and behavioral circadian rhythms. Additionally, while there is no difference in striatal dopamine tissue content or dynamics, there are selective differences in striatal norepinephrine and serotonergic tissue content.

Conclusions

These CC strains offer a complex polygenic model system to study underlying mechanisms of cocaine response. We propose that CC041/TauUnc and CC004/TauUnc will be useful for studying genetic and biological mechanisms underlying resistance or vulnerability to the stimulatory and reinforcing effects of cocaine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abarca C, Albrecht U, Spanagel R (2002) Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc Natl Acad Sci U S A 99:9026–9030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanchard MM, Mendelsohn D, Stamp JA (2009) The HR/LR model: further evidence as an animal model of sensation seeking. Neurosci Biobehav Rev 33:1145–1154

    Article  PubMed  Google Scholar 

  • Boileau I, Dagher A, Leyton M, Gunn RN, Baker GB, Diksic M, Benkelfat C (2006) Modeling sensitization to stimulants in humans: an [11C]raclopride/positron emission tomography study in healthy men. Arch Gen Psychiatry 63:1386–1395

    Article  CAS  PubMed  Google Scholar 

  • Cervantes MC, Laughlin RE, Jentsch JD (2013) Cocaine self-administration behavior in inbred mouse lines segregating different capacities for inhibitory control. Psychopharmacology 229:515–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen R, Tilley MR, Wei H, Zhou F, Zhou FM, Ching S, Quan N, Stephens RL, Hill ER, Nottoli T, Han DD, Gu HH (2006) Abolished cocaine reward in mice with a cocaine-insensitive dopamine transporter. Proc Natl Acad Sci U S A 103:9333–9338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Churchill GA, Airey DC, Allayee H, Angel JM, Attie AD, Beatty J, Beavis WD, Belknap JK, Bennett B, Berrettini W, Bleich A, Bogue M, Broman KW, Buck KJ, Buckler E, Burmeister M, Chesler EJ, Cheverud JM, Clapcote S, Cook MN, Cox RD, Crabbe JC, Crusio WE, Darvasi A, Deschepper CF, Doerge RW, Farber CR, Forejt J, Gaile D, Garlow SJ, Geiger H, Gershenfeld H, Gordon T, Gu J, Gu W, de Haan G, Hayes NL, Heller C, Himmelbauer H, Hitzemann R, Hunter K, Hsu HC, Iraqi FA, Ivandic B, Jacob HJ, Jansen RC, Jepsen KJ, Johnson DK, Johnson TE, Kempermann G, Kendziorski C, Kotb M, Kooy RF, Llamas B, Lammert F, Lassalle JM, Lowenstein PR, Lu L, Lusis A, Manly KF, Marcucio R, Matthews D, Medrano JF, Miller DR, Mittleman G, Mock BA, Mogil JS, Montagutelli X, Morahan G, Morris DG, Mott R, Nadeau JH, Nagase H, Nowakowski RS, O'Hara BF, Osadchuk AV, Page GP, Paigen B, Paigen K, Palmer AA, Pan HJ, Peltonen-Palotie L, Peirce J, Pomp D, Pravenec M, Prows DR, Qi Z, Reeves RH, Roder J, Rosen GD, Schadt EE, Schalkwyk LC, Seltzer Z, Shimomura K, Shou S, Sillanpaa MJ, Siracusa LD, Snoeck HW, Spearow JL, Svenson K, Tarantino LM, Threadgill D, Toth LA, Valdar W, de Villena FP, Warden C, Whatley S, Williams RW, Wiltshire T, Yi N, Zhang D, Zhang M, Zou F, Complex Trait C (2004) The collaborative cross, a community resource for the genetic analysis of complex traits. Nat Genet 36:1133–1137

    Article  CAS  PubMed  Google Scholar 

  • Clinton SM, Turner CA, Flagel SB, Simpson DN, Watson SJ, Akil H (2012) Neonatal fibroblast growth factor treatment enhances cocaine sensitization. Pharmacol Biochem Behav 103:6–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox SM, Benkelfat C, Dagher A, Delaney JS, Durand F, McKenzie SA, Kolivakis T, Casey KF, Leyton M (2009) Striatal dopamine responses to intranasal cocaine self-administration in humans. Biol Psychiatry 65:846–850

    Article  CAS  PubMed  Google Scholar 

  • Davidson ES, Finch JF, Schenk S (1993) Variability in subjective responses to cocaine: initial experiences of college students. Addict Behav 18:445–453

    Article  CAS  PubMed  Google Scholar 

  • de Wit H, Phillips TJ (2012) Do initial responses to drugs predict future use or abuse? Neurosci Biobehav Rev 36:1565–1576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delfs JM, Zhu Y, Druhan JP, Aston-Jones GS (1998) Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat. Brain Res 806:127–140

    Article  CAS  PubMed  Google Scholar 

  • DePoy LM, McClung CA, Logan RW (2017) Neural mechanisms of circadian regulation of natural and drug reward. Neural Plast 2017:5720842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dickson PE, Ndukum J, Wilcox T, Clark J, Roy B, Zhang L, Li Y, Lin DT, Chesler EJ (2015) Association of novelty-related behaviors and intravenous cocaine self-administration in diversity outbred mice. Psychopharmacology 232:1011–1024

    Article  CAS  PubMed  Google Scholar 

  • Falcon E, McClung CA (2009) A role for the circadian genes in drug addiction. Neuropharmacology 56(Suppl 1):91–96

    Article  CAS  PubMed  Google Scholar 

  • Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606–612

    Article  CAS  PubMed  Google Scholar 

  • Goldman D, Oroszi G, Ducci F (2005) The genetics of addictions: uncovering the genes. Nat Rev Genet 6:521–532

    Article  CAS  PubMed  Google Scholar 

  • Graham JB, Thomas S, Swarts J, McMillan AA, Ferris MT, Suthar MS, Treuting PM, Ireton R, Gale M Jr, Lund JM (2015) Genetic diversity in the collaborative cross model recapitulates human West Nile virus disease outcomes. MBio 6:e00493–e00415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gralinski LE, Ferris MT, Aylor DL, Whitmore AC, Green R, Frieman MB, Deming D, Menachery VD, Miller DR, Buus RJ, Bell TA, Churchill GA, Threadgill DW, Katze MG, McMillan L, Valdar W, Heise MT, Pardo-Manuel de Villena F, Baric RS (2015) Genome wide identification of SARS-CoV susceptibility loci using the collaborative cross. PLoS Genet 11:e1005504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:147–165

    Article  CAS  PubMed  Google Scholar 

  • Hasler BP, Wallace ML, White SJ, Molina BSG, Pedersen SL (2019) Preliminary evidence that real world sleep timing and duration are associated with laboratory-assessed alcohol response. Alcohol Clin Exp Res 43:1575–1584

    Article  PubMed  PubMed Central  Google Scholar 

  • Hooks MS, Jones GH, Smith AD, Neill DB, Justice JB Jr (1991) Response to novelty predicts the locomotor and nucleus accumbens dopamine response to cocaine. Synapse 9:121–128

    Article  CAS  PubMed  Google Scholar 

  • Howard MO, Kivlahan D, Walker RD (1997) Cloninger's tridimensional theory of personality and psychopathology: applications to substance use disorders. J Stud Alcohol 58:48–66

    Article  CAS  PubMed  Google Scholar 

  • Izumo M, Johnson CH, Yamazaki S (2003) Circadian gene expression in mammalian fibroblasts revealed by real-time luminescence reporting: temperature compensation and damping. Proc Natl Acad Sci U S A 100:16089–16094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jimenez-Rivera CA, Feliu-Mojer M, Vazquez-Torres R (2006) Alpha-noradrenergic receptors modulate the development and expression of cocaine sensitization. Ann N Y Acad Sci 1074:390–402

    Article  CAS  PubMed  Google Scholar 

  • Kendler KS, Karkowski LM, Corey LA, Prescott CA, Neale MC (1999) Genetic and environmental risk factors in the aetiology of illicit drug initiation and subsequent misuse in women. Br J Psychiatry 175:351–356

    Article  CAS  PubMed  Google Scholar 

  • Kendler KS, Karkowski LM, Neale MC, Prescott CA (2000) Illicit psychoactive substance use, heavy use, abuse, and dependence in a US population-based sample of male twins. Arch Gen Psychiatry 57:261–269

    Article  CAS  PubMed  Google Scholar 

  • Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 101:713–725

    Article  PubMed  Google Scholar 

  • Levy R, Mott RF, Iraqi FA, Gabet Y (2015) Collaborative cross mice in a genetic association study reveal new candidate genes for bone microarchitecture. BMC Genomics 16:1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Logan RW, Williams WP 3rd, McClung CA (2014) Circadian rhythms and addiction: mechanistic insights and future directions. Behav Neurosci 128:387–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Logan RW, Parekh PK, Kaplan GN, Becker-Krail DD, Williams WP 3rd, Yamaguchi S, Yoshino J, Shelton MA, Zhu X, Zhang H, Waplinger S, Fitzgerald E, Oliver-Smith J, Sundarvelu P, Enwright JF 3rd, Huang YH, McClung CA (2018) NAD+ cellular redox and SIRT1 regulate the diurnal rhythms of tyrosine hydroxylase and conditioned cocaine reward. Mol Psychiatry

  • Mabrouk OS, Han JL, Wong JT, Akil H, Kennedy RT, Flagel SB (2018) The in vivo neurochemical profile of selectively bred high-responder and low-responder rats reveals baseline, cocaine-evoked, and novelty-evoked differences in Monoaminergic systems. ACS Chem Neurosci 9:715–724

    Article  CAS  PubMed  Google Scholar 

  • Mosedale M, Kim Y, Brock WJ, Roth SE, Wiltshire T, Eaddy JS, Keele GR, Corty RW, Xie Y, Valdar W, Watkins PB (2017) Editor's highlight: candidate risk factors and mechanisms for Tolvaptan-induced liver injury are identified using a collaborative cross approach. Toxicol Sci 156:438–454

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muller CP, Carey RJ, Huston JP, De Souza Silva MA (2007) Serotonin and psychostimulant addiction: focus on 5-HT1A-receptors. Prog Neurobiol 81:133–178

    Article  CAS  PubMed  Google Scholar 

  • Ozburn AR, Larson EB, Self DW, McClung CA (2012) Cocaine self-administration behaviors in ClockDelta19 mice. Psychopharmacology 223:169–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozburn AR, Falcon E, Twaddle A, Nugent AL, Gillman AG, Spencer SM, Arey RN, Mukherjee S, Lyons-Weiler J, Self DW, McClung CA (2015) Direct regulation of diurnal Drd3 expression and cocaine reward by NPAS2. Biol Psychiatry 77:425–433

    Article  CAS  PubMed  Google Scholar 

  • Parekh PK, Logan RW, Ketchesin KD, Becker-Krail D, Shelton MA, Hildebrand MA, Barko K, Huang YH, McClung CA (2019) Cell-type-specific regulation of nucleus accumbens synaptic plasticity and cocaine reward sensitivity by the circadian protein, NPAS2. J Neurosci 39:4657–4667

    Article  PubMed  PubMed Central  Google Scholar 

  • Philip VM, Sokoloff G, Ackert-Bicknell CL, Striz M, Branstetter L, Beckmann MA, Spence JS, Jackson BL, Galloway LD, Barker P, Wymore AM, Hunsicker PR, Durtschi DC, Shaw GS, Shinpock S, Manly KF, Miller DR, Donohue KD, Culiat CT, Churchill GA, Lariviere WR, Palmer AA, O'Hara BF, Voy BH, Chesler EJ (2011) Genetic analysis in the collaborative cross breeding population. Genome Res 21:1223–1238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piazza PV, Deminiere JM, Le Moal M, Simon H (1989) Factors that predict individual vulnerability to amphetamine self-administration. Science 245:1511–1513

    Article  CAS  PubMed  Google Scholar 

  • Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237:1219–1223

    Article  CAS  PubMed  Google Scholar 

  • Ritz MC, Cone EJ, Kuhar MJ (1990) Cocaine inhibition of ligand binding at dopamine, norepinephrine and serotonin transporters: a structure-activity study. Life Sci 46:635–645

    Article  CAS  PubMed  Google Scholar 

  • Roberts A, Pardo-Manuel de Villena F, Wang W, McMillan L, Threadgill DW (2007) The polymorphism architecture of mouse genetic resources elucidated using genome-wide resequencing data: implications for QTL discovery and systems genetics. Mamm Genome 18:473–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts AJ, Casal L, Huitron-Resendiz S, Thompson T, Tarantino LM (2018) Intravenous cocaine self-administration in a panel of inbred mouse strains differing in acute locomotor sensitivity to cocaine. Psychopharmacology 235:1179–1189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha BA, Fumagalli F, Gainetdinov RR, Jones SR, Ator R, Giros B, Miller GW, Caron MG (1998) Cocaine self-administration in dopamine-transporter knockout mice. Nat Neurosci 1:132–137

    Article  CAS  PubMed  Google Scholar 

  • Schoenrock SA, Oreper D, Farrington J, McMullan RC, Ervin R, Miller DR, Pardo-Manuel de Villena F, Valdar W, Tarantino LM (2017) Perinatal nutrition interacts with genetic background to alter behavior in a parent-of-origin dependent manner in adult collaborative cross mice. Genes Brain Behav

  • Schwartz WJ, Zimmerman P (1990) Circadian timekeeping in BALB/c and C57BL/6 inbred mouse strains. J Neurosci 10:3685–3694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shnitko TA, Spear LP, Robinson DL (2016) Adolescent binge-like alcohol alters sensitivity to acute alcohol effects on dopamine release in the nucleus accumbens of adult rats. Psychopharmacology 233:361–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sittig LJ, Carbonetto P, Engel KA, Krauss KS, Barrios-Camacho CM, Palmer AA (2016) Genetic background limits generalizability of genotype-phenotype relationships. Neuron 91:1253–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slawson MH, Taccogno JL, Foltz RL, Moody DE (2002) Quantitative analysis of selegiline and three metabolites (N-desmethylselegiline, methamphetamine, and amphetamine) in human plasma by high-performance liquid chromatography-atmospheric pressure chemical ionization-tandem mass spectrometry. J Anal Toxicol 26:430–437

    Article  CAS  PubMed  Google Scholar 

  • Sora I, Wichems C, Takahashi N, Li XF, Zeng Z, Revay R, Lesch KP, Murphy DL, Uhl GR (1998) Cocaine reward models: conditioned place preference can be established in dopamine- and in serotonin-transporter knockout mice. Proc Natl Acad Sci U S A 95:7699–7704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava A, Morgan AP, Najarian ML, Sarsani VK, Sigmon JS, Shorter JR, Kashfeen A, McMullan RC, Williams LH, Giusti-Rodriguez P, Ferris MT, Sullivan P, Hock P, Miller DR, Bell TA, McMillan L, Churchill GA, de Villena FP (2017) Genomes of the mouse collaborative cross. Genetics 206:537–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan PF, Agrawal A, Bulik CM, Andreassen OA, Borglum AD, Breen G, Cichon S, Edenberg HJ, Faraone SV, Gelernter J, Mathews CA, Nievergelt CM, Smoller JW, O'Donovan MC, Psychiatric Genomics C (2018) Psychiatric Genomics: an update and an agenda. Am J Psychiatry 175:15–27

    Article  PubMed  Google Scholar 

  • Thomsen M, Hall FS, Uhl GR, Caine SB (2009a) Dramatically decreased cocaine self-administration in dopamine but not serotonin transporter knock-out mice. J Neurosci 29:1087–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomsen M, Han DD, Gu HH, Caine SB (2009b) Lack of cocaine self-administration in mice expressing a cocaine-insensitive dopamine transporter. J Pharmacol Exp Ther 331:204–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Threadgill DW, Churchill GA (2012) Ten years of the collaborative cross. Genetics 190:291–294

    Article  PubMed  PubMed Central  Google Scholar 

  • Venkatratnam A, Furuya S, Kosyk O, Gold A, Bodnar W, Konganti K, Threadgill DW, Gillespie KM, Aylor DL, Wright FA, Chiu WA, Rusyn I (2017) Editor's highlight: collaborative cross mouse population enables refinements to characterization of the variability in Toxicokinetics of trichloroethylene and provides genetic evidence for the role of PPAR pathway in its oxidative metabolism. Toxicol Sci 158:48–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vered K, Durrant C, Mott R, Iraqi FA (2014) Susceptibility to Klebsiella pneumonaie infection in collaborative cross mice is a complex trait controlled by at least three loci acting at different time points. BMC Genomics 15:865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ (1999) Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans. J Psychopharmacol 13:337–345

    Article  CAS  PubMed  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F (2011) Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci U S A 108:15037–15042

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiltshire T, Ervin RB, Duan H, Bogue MA, Zamboni WC, Cook S, Chung W, Zou F, Tarantino LM (2015) Initial locomotor sensitivity to cocaine varies widely among inbred mouse strains. Genes Brain Behav 14:271–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto DJ, Nelson AM, Mandt BH, Larson GA, Rorabaugh JM, Ng CM, Barcomb KM, Richards TL, Allen RM, 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 37:1738–1753

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Zoe McElligott at UNC for assistance in instruction and interpretation of monoamine tissue content analysis and The Jackson Laboratory Surgical Services team for performing the jugular catheter implantation on IVSA animals. Funding for this work was provided by the UNC Bowles Center for Alcohol Studies to DR, R01MH100241 from NIMH to WV and LT, R01DA023690 from NIDA to LT and P50DA039841 from NIDA to EJC, JDJ, RWL, CAM, and LT. PED was supported on K99DA043573, SN was supported on R25GM089569, LB was supported on T32AA025606 and KR was supported on T32GM008719. The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Genetics, School of Medicine, University of North Carolina, 120 Mason Farm Road, CB7361, Chapel Hill, NC, 27599, USA

    Sarah A. Schoenrock, Padam Kumar, Joseph Farrington, Christiann H. Gaines, Saad Khan, William Valdar, Fernando Pardo-Manuel de Villena & Lisa M. Tarantino

  2. Neuroscience Curriculum, University of North Carolina, Chapel Hill, NC, USA

    Sarah A. Schoenrock, Sofia Neira & Christiann H. Gaines

  3. Center for Systems Neurogenetics of Addiction, The Jackson Laboratory, Bar Harbor, ME, USA

    Sarah A. Schoenrock, Price E. Dickson, Sam-Moon Kim, Lauren Bailey, Troy D. Wilcox, Tyler A. Roy, Michael R. Leonardo, Ashley A. Olson, Leona H. Gagnon, Vivek M. Philip, James D. Jentsch, Ryan W. Logan, Colleen A. McClung, Elissa J. Chesler & Lisa M. Tarantino

  4. Bowles Center for Alcohol Studies, University of North Carolina, Chapel Hill, NC, USA

    Alexander Gómez-A, Sofia Neira, Kyle D. Riker & Donita L. Robinson

  5. The Jackson Laboratory, Bar Harbor, ME, USA

    Price E. Dickson, Troy D. Wilcox, Tyler A. Roy, Michael R. Leonardo, Ashley A. Olson, Leona H. Gagnon, Vivek M. Philip & Elissa J. Chesler

  6. Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

    Sam-Moon Kim, Ryan W. Logan & Colleen A. McClung

  7. Department of Psychology, Binghamton University, Binghamton, NY, USA

    Lauren Bailey & James D. Jentsch

  8. Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, NC, USA

    William Valdar & Fernando Pardo-Manuel de Villena

  9. Department of Psychiatry, School of Medicine, University of North Carolina, Chapel Hill, NC, USA

    Donita L. Robinson

  10. Division of Pharmacotherapy and Experimental Therapeutics, Eshelman School of Pharmacy, University of North Carolina, Chapel Hill, NC, USA

    Lisa M. Tarantino

Authors
  1. Sarah A. Schoenrock
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Padam Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander Gómez-A
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Price E. Dickson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sam-Moon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lauren Bailey
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sofia Neira
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kyle D. Riker
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joseph Farrington
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Christiann H. Gaines
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Saad Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Troy D. Wilcox
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tyler A. Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Michael R. Leonardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Ashley A. Olson
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Leona H. Gagnon
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Vivek M. Philip
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. William Valdar
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Fernando Pardo-Manuel de Villena
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. James D. Jentsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Ryan W. Logan
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Colleen A. McClung
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Donita L. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Elissa J. Chesler
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Lisa M. Tarantino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisa M. Tarantino.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 1447 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schoenrock, S.A., Kumar, P., Gómez-A, A. et al. Characterization of genetically complex Collaborative Cross mouse strains that model divergent locomotor activating and reinforcing properties of cocaine. Psychopharmacology 237, 979–996 (2020). https://doi.org/10.1007/s00213-019-05429-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-019-05429-3

Keywords

Search

Navigation