Neurochemical Research

, Volume 41, Issue 5, pp 945–950 | Cite as

Frequency-Dependent Modulation of Dopamine Release by Nicotine and Dopamine D1 Receptor Ligands: An In Vitro Fast Cyclic Voltammetry Study in Rat Striatum

  • W. Goutier
  • J. P. Lowry
  • A. C. McCreary
  • J. J. O’Connor
Short Communication
First Online:
Received:
Revised:
Accepted:

Abstract

Nicotine is a highly addictive drug and exerts this effect partially through the modulation of dopamine release and increasing extracellular dopamine in regions such as the brain reward systems. Nicotine acts in these regions on nicotinic acetylcholine receptors. The effect of nicotine on the frequency dependent modulation of dopamine release is well established and the purpose of this study was to investigate whether dopamine D1 receptor (D1R) ligands have an influence on this. Using fast cyclic voltammetry and rat corticostriatal slices, we show that D1R ligands are able to modulate the effect of nicotine on dopamine release. Nicotine (500 nM) induced a decrease in dopamine efflux at low frequency (single pulse or five pulses at 10 Hz) and an increase at high frequency (100 Hz) electrical field stimulation. The D1R agonist SKF-38393, whilst having no effect on dopamine release on its own or on the effect of nicotine upon multiple pulse evoked dopamine release, did significantly prevent and reverse the effect of nicotine on single pulse dopamine release. Interestingly similar results were obtained with the D1R antagonist SCH-23390. In this study we have demonstrated that the modulation of dopamine release by nicotine can be altered by D1R ligands, but only when evoked by single pulse stimulation, and are likely working via cholinergic interneuron driven dopamine release.

Keywords

Fast cyclic voltammetry Dopamine release Nicotine Dopamine D1 receptor SCH-23390 SKF-38393 

Abbreviations

D1R

Dopamine D1 receptor

nAChR

Nicotinic acetylcholine receptors

ChI

Cholinergic interneuron

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

Notes

Acknowledgments

This study was financially supported by Abbott Healthcare Products B.V. WG and ACMcC were employees of Abbott.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflicts of interest.

References

  1. 1.
    Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241–263CrossRefPubMedGoogle Scholar
  2. 2.
    Zhou FM, Liang Y, Dani JA (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4:1224–1229CrossRefPubMedGoogle Scholar
  3. 3.
    Grenhoff J, Aston-Jones G, Svensson TH (1986) Nicotinic effects on the firing pattern of midbrain dopamine neurons. Acta Physiol Scand 128:351–358CrossRefPubMedGoogle Scholar
  4. 4.
    Mansvelder HD, De Rover M, McGehee DS, Brussaard AB (2003) Cholinergic modulation of dopaminergic reward areas: upstream and downstream targets of nicotine addiction. Eur J Pharmacol 480:117–123CrossRefPubMedGoogle Scholar
  5. 5.
    Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7:583–584CrossRefPubMedGoogle Scholar
  6. 6.
    Zhang H, Sulzer D (2004) Frequency-dependent modulation of dopamine release by nicotine. Nat Neurosci 7:581–582CrossRefPubMedGoogle Scholar
  7. 7.
    Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ (2012) Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75(1):58–64CrossRefPubMedGoogle Scholar
  8. 8.
    Cachope R, Mateo Y, Mathur BN, Irving J, Wang HL, Morales M, Lovinger DM, Cheer JF (2012) Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep 2(1):33–41CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Wang L, Shang S, Kang X, Teng S, Zhu F, Liu B, Wu Q, Li M, Liu W, Xu H, Zhou L, Jiao R, Dou H, Zuo P, Zhang X, Zheng L, Wang S, Wang C, Zhou Z (2014) Modulation of dopamine release in the striatum by physiologically relevant levels of nicotine. Nat Commun 5:3925PubMedGoogle Scholar
  10. 10.
    O’Neill C, Nolan BJ, Macari A, O’Boyle KM, O’Connor JJ (2007) Adenosine A1 receptor-mediated inhibition of dopamine release from rat striatal slices is modulated by D1 dopamine receptors. Eur J Neurosci 26:3421–3428CrossRefPubMedGoogle Scholar
  11. 11.
    Stouffer MA, Ali S, Reith ME, Patel JC, Sarti F, Carr KD, Rice ME (2011) SKF-83566, a D1-dopamine receptor antagonist, inhibits the dopamine transporter. J Neurochem 118(5):15–20CrossRefGoogle Scholar
  12. 12.
    Lim SA, Kang UJ, McGehee DS (2014) Striatal cholinergic interneuron regulation and circuit effects. Front Synaptic Neurosci 6:22CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Robinson DL, Hermans A, Seipel AT, Wightman RM (2008) Monitoring rapid chemical communication in the brain. Chem Rev 108:2554–2584CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Kruk ZL, O’Connor JJ (1995) Fast electrochemical studies in isolated tissues. Trends Pharmacol Sci 16:145–149CrossRefPubMedGoogle Scholar
  15. 15.
    O’Connor JJ, O’Neill C (2008) A role for adenosine A1 receptors in GABA and NMDA-receptor mediated modulation of dopamine release: studies using fast cyclic voltammetry. Sensors 8:5516–5534CrossRefPubMedCentralGoogle Scholar
  16. 16.
    Goutier W, O’Connor JJ, Lowry JP, McCreary AC (2015) The effect of nicotine induced behavioral sensitization on dopamine D1 receptor pharmacology: an in vivo and ex vivo study in the rat. Eur Neuropsychopharmacol 25:933–943CrossRefPubMedGoogle Scholar
  17. 17.
    Zhang L, Doyon WM, Clark JJ, Phillips PE, Dani JA (2009) Controls of tonic and phasic dopamine transmission in the dorsal and ventral striatum. Mol Pharmacol 76:396–404CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85:5274–5278CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Pidoplichko VI, DeBiasi M, Williams JT, Dani JA (1997) Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390:401–404CrossRefPubMedGoogle Scholar
  20. 20.
    Komal P, Estakhr J, Kamran M, Renda A, Nashmi R (2015) cAMP-dependent protein kinase inhibits α7 nicotinic receptor activity in layer 1 cortical interneurons through activation of D1/D5 dopamine receptors. J Physiol 593:3513–3532CrossRefPubMedGoogle Scholar
  21. 21.
    Brewster WK, Nichols DE, Riggs RM, Mottola DM, Lovenberg TW, Lewis MH, Mailman RB (1990) Trans-10,11-dihydroxy-5,6,6a,7,8,12b-hexahydrobenzo[a]phenanthridine: a highly potent selective dopamine D1 full agonist. J Med Chem 33(6):1756–1764CrossRefPubMedGoogle Scholar
  22. 22.
    Heidenreich BA, Mailman RB, Nichols DE, Napier TC (1995) Partial and full dopamine D1 agonists produce comparable increases in ventral pallidal neuronal activity: contribution of endogenous dopamine. J Pharmacol Exp Ther 273:516–525PubMedGoogle Scholar
  23. 23.
    Millan MJ, Newman-Tancredi A, Quentric Y, Cussac D (2001) The “selective” dopamine D1 receptor antagonist, SCH23390, is a potent and high efficacy agonist at cloned human serotonin2C receptors. Psychopharmacology 156(1):58–62CrossRefPubMedGoogle Scholar
  24. 24.
    Livingstone PD, Wonnacott S (2009) Nicotinic acetylcholine receptors and the ascending dopamine pathways. Biochem Pharmacol 78:744–755CrossRefPubMedGoogle Scholar
  25. 25.
    Seipel AT, Yakel JL (2010) The frequency-dependence of the nicotine-induced inhibition of dopamine is controlled by the α7 nicotinic receptor. J Neurochem 114:1659–1666CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R (2002) Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114:475–492CrossRefPubMedGoogle Scholar
  27. 27.
    Muscat R, Patel J, Trout SJ, Wieczorek W, Kruk ZL (1993) Dissociation of the effects of amphetamine and quinpirole on dopamine release in the nucleus accumbens following behavioural sensitization: an ex vivo voltammetric study. Behav Pharmacol 4:411–418PubMedGoogle Scholar
  28. 28.
    Ito HT, Schuman EM (2007) Frequency-dependent gating of synaptic transmission and plasticity by dopamine. Front Neural Circuits 1:1CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • W. Goutier
    • 1
    • 2
  • J. P. Lowry
    • 2
  • A. C. McCreary
    • 1
  • J. J. O’Connor
    • 2
    • 3
  1. 1.Abbott Healthcare Products B.V. (formerly Solvay Pharmaceuticals B.V.)WeespThe Netherlands
  2. 2.Maynooth University Department of ChemistryMaynooth UniversityMaynoothIreland
  3. 3.UCD School of Biomolecular and Biomedical ScienceUCD Conway Institute of Biomolecular and Biomedical ResearchBelfield, Dublin 4Ireland

Personalised recommendations